8 Restoration Success Of Tropical Forests: The Search For Indicators

Jerônimo Boelsums Barreto Sansevero and Mário Luís Garbin

8.1 Introduction

Human activities are viewed as a main cause for the planet’s current environmental crisis (Millennium Ecosystem Assessment – MA, 2005; Ellis et al., 2010). Deforestation, forest fragmentation, agricultural activities, pollution and expansion of urban areas have changed about two thirds of earth’s ecosystems (MA, 2005) and, as a consequence, have led to biodiversity loss, species’ extinctions and reduction of the resilience capacity of many ecosystems (Peterson et al., 1998; Silva and Tabarelli, 2000; Laliberté et al., 2010). Indirectly, such transformations affect the provision of many ecosystem services such as soil fertility, water quality, pollination, and recreation (MA, 2005; Ditt et al., 2010). Based on this condition, ecosystem restoration is crucial not only to conserve biodiversity, but also to provide ecosystem services (Rey Benayas et al., 2009; Palmer and Filoso, 2009). This is particularly problematic for tropical forests due to their high diversity and habitat loss (Laurance, 1999; Myers et al., 2000; Chazdon 2008). Currently, there are some ambitious restoration goals to revert this scenario of environmental degradation (Calmon et al., 2011). The Convention on Biological Diversity aimed to restore 15% of world’s degraded areas until 2020, whereas the Bonn Challenge plans to restore 150 million hectares around the world (GPFLR, 2014). This scenario provides a moment of great challenges and opportunities to implement restoration efforts and to revert the current trend of degradation of earth’s ecosystems. Edward O. Wilson stated: “The next century will, I believe, be the era of restoration in ecology” (Wilson, 1992).

Despite the increase in the number of restoration efforts in the last decade in tropical forests (Chazdon, 2008), there are some fundamental questions linked to this science that remain unanswered. Amongst them, two are worth highlighting: how to measure the success of ecological restoration? What are the variables to be used as indicators of the success? Answering these questions will shape our understanding of the restoration process, as well as the selection of indicators used to measure success. However, these questions were not conclusively answered due to two main issues. First, restoration ecology is quite a young discipline and, as such, it still presents conceptual issues (Hobbs and Norton 1996; Miller and Hobbs 2007). Conceptual limitation was also attributed to the science of ecology as a whole (Peters, 1991; Shrader-Frechette and McCoy, 1993), even though ecology is currently viewed as robust enough to provide strong patterns and even laws (Dodds, 2009).

Nevertheless, such limitation is one factor that contributes to the gap between scientific knowledge and decision making (Barbosa et al., 2004). Secondly, there is a small number of long term monitoring programs for restoration projects (Bash and Ryan, 2002; Suding, 2011). This state of affairs presents a great challenge for the development and validation of restoration efforts because it coincides with a time of great opportunities for the implementation of restoration projects (e.g. Cabin, 2007). Therefore, there is a need for tools to make restoration ecology a more robust scientific enterprise. The objectives of this chapter are threefold: (1) to present the main ideas for the evaluation of restoration success and the indicators used; (2) to discuss the main advantages and drawbacks of the main strategies of restoration - active and passive; and (3) to emphasize the need for a more widespread use of functional approaches to evaluate success in restoring tropical forests.

8.2 Restoration Ecology: Definitions, Indicators And Strategies

The Society for Ecological Restoration defines restoration as “the process of assisting the recovery of an ecosystem that has been degraded, damaged, or destroyed” (SER, 2004: pp 2). They highlight the final objective of a restoration project as the formation of self-supporting ecosystems that are resilient to perturbations without human assistance. However, as discussed by Ruiz-Jaen and Aide (2005), the main issue is to know how we reach this objective. The Primer of Restoration Ecology (SER, 2004) suggests a list of nine attributes to be considered when evaluating the restoration success of ecosystems: (1) similar diversity and community structure in comparison with reference sites; (2) presence of indigenous species; (3) presence of functional groups necessary for long-term stability; (4) capacity of the physical environment to sustain reproducing populations; (5) normal functioning; (6) integration with the landscape; (7) elimination of potential threats; (8) resilience to natural disturbances; and (9) self-sustainability.

Restoration success can be summarized by three general indicators (see Ruiz-Jaen and Aide, 2005a; Wortley et al., 2013): (1) diversity and abundance; (2) vegetation structure; and (3) ecological processes (see Box 1). A measure of success can be obtained by comparing one, two or these three indicators with reference ecosystems (White and Walker, 1997; SER, 2004; Ruiz-Jaen and Aide, 2005b). A reference ecosystem is considered as the target of restoration and should represent the community structure, species composition, and ecosystem functioning prior to a disturbance (White and Walker, 1997). This perspective, known as the recovery paradigm (see Suding, 2011), assumes that restoring communities present a directional trajectory towards a stable state (e.g. old-growth forest). Due to the generality of these three indicators, there is a need to specify what will be in fact measured in the field and the biological meaning of these measures to restoration success.

Diversity indicators are those related with species (or any other operational taxonomic unit) richness and abundance at different trophic levels. Vegetation structure can be characterized by measuring its cover biomass, basal area, leaf area index, and dominance of different ecological groups (e.g. pioneer and shade tolerant species), at different layers (herbs, shrubs, trees). Ecological processes are those directly related with ecosystem functioning (Ruiz-Jaen and Aide, 2005a) such as: nutrient cycling, carbon flux, seed dispersal, pollination, herbivory, etc. Thus, the measurement of this set of indicators provides a detailed diagnosis of the restored community (Elmqvist et al., 2003; Ruiz-Jaen and Aide, 2005b), and allows checking for the need of new interventions. However, because ecosystems are dynamic, a single measurement in time is of limited power to evaluate the success of restoration (Parker, 1997). Long term monitoring is crucial to understand the successional trajectory of a community (e.g. Parker, 1997; Zedler and Callaway, 1999; see also chapter 3) and to develop predictive models (Anand and Desrochers, 2004; Tucker and Anand, 2004; Peng et al., 2010) (Fig. 1). Severely degraded ecosystems can arrest ecological succession and lead to alternative stable states (Suding et al., 2004) (Fig. 1). When stable states that differ from the reference system are reached, the actions required to return the system towards the planned trajectory can be more complicated when compared to that required for the initial degraded state. Thus, understanding how these indicators vary in time is of fundamental importance in order to: 1) choose appropriate restoration strategies (e.g. passive or active restoration); 2) select species to be used; 3) characterize the successional trajectory and ecosystem resilience (Suding et al., 2004).

BOX. 1 - Measuring restoration success An important aspect in measuring restoration success is the definition of the indicators (diversity, vegetation structure and ecological processes) to be quantified. There are two review studies that analyzed how restoration success has been measured in terrestrial ecosystems (Ruiz-Jaen and Aide, 2005a; Wortley et al., 2013). The results showed that only 15% of published data measured restoration success (Ruiz-Jaen and Aide, 2005a). Most of these studies were done in North America (53%), whereas the continents with higher extents of tropical forests (South America, Africa and Asia) encompassed only 12% of the studies (Ruiz-Jaen and Aide, 2005a). These results emphasize the need to increase the research characterizing the success of ecological restoration, especially for tropical forests. Moreover, it is noteworthy that the time interval used to evaluate success is about 1-15 years in 71% of the studies (Wortley et al., 2013). This short period can be a limiting factor to observe changes in diversity, vegetation structure and ecological processes, especially in heavily degraded sites (Guariguata and Ostertag, 2001; Holl, 2007; Dias et al., 2012). The most used indicator was diversity (29%; Wortley et al., 2013; Fig. 2). Only in 11% of the studies the three indicators were evaluated altogether (Fig. 2). This is critical because it shows that the overall picture about measuring restoration success around the world is incomplete, and it is not clear whether we are measuring success in a reliable and efficient way for most of the restoration initiatives.

Restoration strategies can be classified into two groups: passive and active (Holl and Aide, 2011). Active restoration is made by using interventionist techniques, such as tree plantations, seeding, topsoil application and artificial patches (Parrotta and Knowles, 2001; Camargo et al., 2002; Zanini and Ganade, 2005; Rodrigues et al., 2009; Dias et al., 2012). Plantation is the most common approach of active restoration in tropical areas (Rodrigues el al., 2009) whereas passive restoration occurs through natural regeneration (Holl and Aide, 2011). On one hand, the increased forest cover in some tropical areas (see Aide et al., 2012), also known as forest transitions, is a demonstration that passive restoration has great potential due to low implementation costs (Holl and Aide, 2011). Forest transitions in the tropics result from rural-urban migration, and consequent abandonment of agricultural lands (Aide and Grau, 2004). On the other hand, in some areas where the degradation processes were more intense, active restoration techniques may become necessary. Therefore, land use history, surrounding matrix, types of disturbances, and the presence of natural regenerating native species should be considered when deciding which will be the best restoration strategy in a given site, whether active or passive (Holl and Aide, 2011). The understanding of the regeneration process in time is crucial to predict the restoration success, regardless of the chosen strategy.

The factors affecting natural regeneration, i.e. passive restoration, can be summarized in: intensity and frequency of disturbance (Pickett and White, 1985), land use history (Guariguata and Ostertag, 2001; Holl, 2007), and dispersal limitation (Tabarelli and Peres, 2002; Pereira et al., 2013). Moreover, the interaction among these factors has been pointed as the main cause of the large observed variation in species richness and abundance, basal area, and nutrient cycling in tropical secondary forests (Brown and Lugo, 1990; Guariguata and Ostertag, 2001). Secondary forests originated from abandoned pastures can take 20 to 60 years to reach similar values of species richness and biomass from that found in old growth forests (Guariguata et al., 1997; Finegan and Delgado, 2000; Letcher and Chazdon, 2009). However, the recovery of species composition or groups of species (endemic and non-pioneer species) can take more than 100 years (Finegan, 1996; Liebsch et al., 2008). For example, abandoned pastures affected by fire in Brazilian Atlantic forest show low species richness, high dominance and the presence of invasive grass species, even after 20 years since the last fire event (Fig. 3c). Thus, a precise diagnostic analysis in the field is of fundamental importance to allow proper decision making about the effectiveness of passive restoration initiatives.

Active restoration (e.g. tree plantation) is an efficient strategy for areas subjected to drastic abiotic changes (Rodrigues et al., 2009; Holl and Aide, 2011). Plantations of tree species can catalyze forest succession, increasing species richness, improving soil fertility and restoring ecological interactions (Parrotta et al., 1997; Harrington, 1999; Ruiz-Jaen and Aide, 2005b; Sansevero et al., 2011; Suganuma et al., 2014). Abundance of tree/shrubs species in 11 years old forest plantations can reach similar values to that of old-growth forests (Sansevero et al., 2011 – Fig. 3a). Natural regeneration can contribute in more than 40% to total basal area in 11 years old forest plantations (Sansevero et al., 2011), and with 69% of tree species abundance in 28 years old plantations (Pulitano and Durigan, 2004). Therefore, even in planted forests, natural regeneration has a key role in the recovering of vegetation structure. Nevertheless, the effects of the number of planted species in the restoration success are debatable due to the large variation in responses showed by different studies (Lugo, 1997; Aronson et al., 2011). Despite the importance of biodiversity in ecosystem functioning and stability (Naeem, 1998), forest plantations with low diversity (1-10 tree species) can lead to a rapid recovery of species richness and abundance (Silva-Junior et al., 1995; Lugo, 1997; Ruiz-Jaén and Aide, 2005b). This is mainly due to the fact that restoring communities are affected by external factors as the distance to forest fragments, differences in soil attributes, and climate conditions. Overall, the interaction among these different factors and the chosen strategy, whether passive or active, can produce very different responses leading to uncertainty about successional trajectories and the success of ecological restoration.

The recovery of vegetation structure is faster when compared to the recovery of species diversity and ecological processes for both, passive and active strategies (Guariguata et al., 1997; Suganuma et al., 2014). However, it is noteworthy that the high spatial and temporal variation in species diversity and composition of tropical forests (Leigh et al., 2004) is a complicating factor in determining the reference ecosystem (e.g. Suganuma et al., 2013), because of the increased analytical complexity required. Consequently, there will be no reliable indicators to evaluate the success of the restoration efforts due to such variation. In order to solve this limitation, two solutions have been proposed. The first one is based on using a range of values measured in several reference ecosystems, for a given indicator, instead of single measures. However, such approach is unsatisfactory for indicators with high variation (e.g. percentage of zoochorous plants – 47% – Suganuma et al., 2013). The second possibility is to use integrative measures of vegetation structure, diversity and ecological processes as proposed by functional approaches and that have seldom been used in restoration ecology (Aerts and Honnay, 2011; Cadotte et al., 2011).

8.3 How Functional Ecology Can Contribute With Restoration Ecology?

The functional approach is represented by the set of species’ traits in a given community and the relationship between these traits and environmental conditions (Solbrig, 1992; Weiher et al., 1999; McGill et al., 2006). These traits can be morphological, physiological or architectural and can be classified into response or effect traits (Lavorel and Garnier, 2002; Cornelissen et al., 2003). Response traits are those related to dispersal capacity, establishment and persistence (see Weiher et al., 1999). Therefore, functional traits are likely to affect the performance of a species (usually abundance) in response to changes in environmental conditions (e.g. climate, soil, landscape and disturbance) and biotic interactions (e.g. competition, facilitation) (Díaz and Cabido, 2001; Moran and Catterall, 2009; Garbin et al., 2014). Effect traits are those related with ecosystem productivity, nutrient cycling, carbon storage and resource availability (see Finegan et al., 2014). The distribution, abundance and diversity of functional traits (functional diversity) directly affect ecosystem functioning (Díaz and Cabido, 2001). Thus, restoration ecology can greatly benefit from a functional approach (Gondard et al., 2003; Cadotte et al., 2011). It can be used to select species for restoration projects, and as a tool for measuring restoration success. This can be done by comparing the functional structure and diversity of the restoring community with that from reference systems.

Table 1 presents examples of functional traits with their responses and effects in plant communities. Response traits provide an important tool when restoring plant communities because they allow understanding plant survival and development under field conditions, especially for seedling planting (Grossnickle, 2012). The selection of traits associated with higher survival and optimal seedling development can help choose adequate plant species and increase the probability of success of the restoration project. For example, a seeding experiment in Amazon showed that species with higher seed mass were positively associated with germination and seedling survivorship (Camargo et al., 2002). The same functional approach can be used to maximize desirable effects in the communities being restored. For example, the provision of ecosystem services is positively associated with plant functional diversity (see Díaz et al., 2007). Moreover, ecosystem resilience and stability could also be analyzed through this same conceptual model.

The examples shown in Table 1 are a small sample of functional traits that can be used to assess functional responses or effects in ecosystems (see Pérez-Harguindeguy et al., 2013). Considering the large number of possibilities, trait selection is not trivial (Violle et al., 2007), but it should consider practical aspects as easiness of measurement (soft and hard traits – Lavorel and Garnier, 2002), and the responses and effects of the traits in face of environmental variations (Violle et al., 2007; Pillar et al., 2009). However, trait variation alone is not sufficient to understand ecological patterns. What makes a trait functional is how it impacts fitness through its effects on growth, survival and reproduction (Violle, 2007), and how such variation in both trait and performance relates to environmental gradients (e.g. Pillar et al., 2009). Nevertheless, the importance of a given trait can vary in response not only to environmental conditions, but also in response to interaction patterns with other species (Garbin et al., 2014). Thus, the next step in order to strengthen the use of functional approaches in restoration ecology is to consolidate a list of functional traits capable to explain key processes for restoration ecology (e.g. Funk et al., 2008), such as: seedling survival, growth, disturbance tolerance, plant-plant (e.g. competition, facilitation) and fauna (pollination, dispersal and herbivory) interactions, nutrient cycling and carbon storage.

Table 1: Functional traits relevant for restoration ecology with their respective responses and effects in ecosystems.

Functional traits	Response and effects in ecosystems
Dispersal syndrome; and Seed mass	Dispersal ability (a,b); Spatial distribution patterns (c); Resource availability for frugivores (d); Seed mass – positively associated with seedling establishment (e)
Leaf dry matter content (LDMC)	Correlate negatively with potential growth rate (a); Resistance to physical hazards (e.g. herbivory, wind, hail) (a); Nutrient cycling - leaves with high LDMC also tends to decompose more slowly than that from leaves with low LDMC
Stem-specific density	Stem density is related to the growth-survival tradeoff; a low stem density leads to a fast growth whereas a high stem density leads to resistance against pathogens or physical damage. Carbon gain is influenced by species stem-specific density (f);
Bark thickness (and bark quality)	Thick bark provides protection of vital tissues against attack by pathogens, herbivores, frost or drought. In general, this trait has special relevance in trees or large shrubs in environments subjected to fire (a)
Root-system morphology	Root system (depth, diameter, lateral extent, and root biomass) is related with capacity of acquire resources and competitive ability (a)

(a) Pérez-Harguindeguy et al., 2013; (b) Howe & Smallwood, 1982; (c) Seidler & Plotkin, 2006; (d) Hasui et al., 2007; (e) Moles & Westoby, 2004; (f) Shimamoto et al., 2014;

Traits can also be used to classify plants into functional groups, or types (Díaz and Cabido, 2001; Pillar and Sosinski, 2003). Plant functional types can be defined as groups of plant species sharing similar functioning, similar responses to environmental factors and/or similar roles in (or effects on) communities or ecosystems (Pillar and Sosinski, 2003). In high diversity systems, the classification of species into functional groups is a strategy to “simplify” communities in the search for more robust patterns. Using this tool, it is possible to compare communities sharing a small number of species (Díaz et al., 2004), analyze the response to disturbances (Muller et al., 2007), assess the resilience of communities (Laliberté et al., 2010), and predict successional trajectories (Chazdon et al., 2009). The prediction of successional trajectories from species composition has been considered a hard task in tropical forests due to their high variation in species diversity and composition (Finegan, 1996; Chazdon et al., 2007). The application of predictive models to the functional structure of plant communities in restoration allows the estimation of the time needed to restore a given area as well as the trajectory of the system; both are important aspects to properly manage communities in restoration, and to redirect successional trajectories. Moreover, as ecosystem services are the basis of the earth’s life supporting systems, effective restoration has crucial implications for human wellbeing.

8.4 Conclusions

Two contrasting features can describe the current scenario for tropical restoration ecology. First, there is a challenge imposed by the drastic changes and degradation of ecosystems. Secondly, there are also opportunities created by several restoration initiatives at local and global scales. Given the difficulties associated with current indicators of restoration success based on species diversity, vegetation structure and ecological processes, it is extremely timely to consider that functional approaches play an important role in providing reliable and simplified indicators for restoration success. The use of such indicators can catalyze more restoration initiatives, because they offer insurance that such efforts will in fact accomplish their initial goals, as to provide ecosystem services, contribute for biodiversity conservation and increase ecosystem resilience in response to climate change.

Acknowledgments

We thank FAPES/CNPq for fellowship to M.L. Garbin; NUTRE (Núcleo de Tecnologias de Recuperação de Ecossistemas – UFRJ/COPPETEC/Petrobras) for being the seed of several ideas we presented here, specially, to all researchers who participated of the 1st Workshop about Successional Trajectories of Tropical Forests in 2008.

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