Nucleation increases understory species and functional diversity in early tropical forest restoration
Introduction
Large areas of primary and secondary tropical forest have been converted to agricultural fields or pastures (Gibbs et al., 2010; Ramankutty et al., 2018). The pastures often consist of African grasses, e.g. Cenchrus clandestinus (Hochst. ex Chiov.) Morrone or Melinis minutiflora P.Beauv., which invade other degraded habitats or forest gaps (Fine, 2002; van Ausdal, 2009). These grasses effectively prevent the recovery of the structure, composition, and functioning of forest ecosystems (Williams and Baruch, 2000; Holly et al., 2009). Thus, abandoned pastures enter a state of arrested succession (Sarmiento, 1997; Zahawi and Augspurger, 1999), under which passive restoration based on natural plant regeneration is unlikely to succeed (Holl and Aide, 2011; Zahawi et al., 2014). Restoration of abandoned pastures focuses mostly on standard afforestation, i.e. planting (non-native) trees over large areas (Rodrigues et al., 2011). However, tree plantations are usually characterized by an impoverished understory (Rodrigues et al., 2009), in which the dominance of exotic grasses compromises natural regeneration of forest plants in the first years of succession (de Souza and Batista, 2004; Royo and Carson, 2006; Chazdon and Guariguata, 2016). Therefore, more effective alternatives for restoration of abandoned pastures are needed.
Recently, nucleation has been introduced as a promising restoration strategy in abandoned pastures (Zahawi et al., 2013; Boanares and Azevedo, 2014), by establishing patches of target vegetation that simulate natural colonization during succession (Yarranton and Morrison, 1974). Nucleation aims at overcoming seed and site limitations on a small fraction of the degraded land. This is believed to be ecologically more efficient and cheaper than planting an entire community or waiting for the slower process of natural recovery to proceed (Zahawi et al., 2013). In practice, nucleation often starts by planting groups of trees or shrubs (Rey Benayas et al., 2008; Corbin and Holl, 2012). More recently, this is complemented by herbs, artificial perches, brush piles, translocated seed bank, and enhanced seed rain (Reis et al., 2010; Bechara et al., 2016). These measures aim at promoting plant recruitment within the abandoned pastures, e.g. seed dispersal by frugivorous birds that perch on isolated trees and shrubs (Holl, 2017). Nucleation also creates suitable microclimatic conditions that promote the establishment and survival of seedlings of forest species (Corbin and Holl, 2012; Teixeira et al., 2016), while promoting different growth forms in the understory that support a range of ecosystem functions (Reis et al., 2010). Overall, this method is more complex but also less costly than traditional large-scale planting of trees (Bechara et al., 2016; Holl and Zahawi, 2018). However, there is little understanding on the interaction of nucleation with plant traits and its effects on functional diversity (FD).
The inclusion of a trait-based approach and FD aspects is important when planning ecological restoration (Laughlin, 2014). In the case of abandoned pastures, it is necessary to include species whose traits enable them to outcompete invasive alien grasses (Ammondt and Litton, 2012). Promoting FD can help restore the complexity of degraded vegetation (Palomeque et al., 2017), and increase ecosystem stability and resilience (Laureto et al., 2015). Furthermore, restoration practices accounting for trait diversity will also support ecosystem functionality by promoting pollination and seed dispersal (Garcia et al., 2015; Kollmann et al., 2016). There is a need for further research to improve the understanding of FD in overcoming thresholds during ecological restoration.
Studies depicting changes in FD, i.e. the value and range of those species and individual traits that influence ecosystem functioning during secondary succession, are abundant in tropical forests (Lohbeck et al., 2012; Dent et al., 2013; Craven et al., 2015). Yet, more studies monitoring FD changes in restoration projects applying different treatments are required (Brudvig, 2011). Most assessments of ecological restoration focus on species richness, abundance and composition (Wortley et al., 2013), while there is mounting evidence that FD metrics provide greater explanatory power to predict restoration success and ecosystem functioning (Brancalion and Holl, 2016; Derhé et al., 2016; Díaz-García et al., 2017). The present study addresses this research gap.
The mountain ranges of the tropical Andes are a biodiversity hotspot (Myers et al., 2000), where forests and Páramo grasslands prevail with high species density and endemism (Särkinen et al., 2012; Madriñán et al., 2013). Moreover, tropical mountain ecosystems regulate the provision of freshwater (Buytaert and de Bièvre, 2012) and serve as major carbon sinks (Hofstede, 1995; Minaya et al., 2016), while large areas have been transformed due to urbanization and other land-use changes (Rodríguez Eraso et al., 2013; Gaglio et al., 2017). Although some restoration projects have been conducted in the tropical Andes (Murcia et al., 2017), the outcome of different restoration strategies need to be compared to determine which methods produce the most gains in species diversity, forest functionality and resilience.
This study evaluates the effects of nucleation to promote an understory with different growth forms that will perform ecosystem functions during early stages of abandoned tropical pastures restoration. We hypothesized that nucleation techniques would enhance functional and species diversity of the understory layer when applied in an abandoned pasture because of favoring ecological processes and different growth forms in the short term. Therefore, we conducted a field experiment in a peri-urban area to compare the effects of four nucleation techniques on species functional and structural diversity. We investigated the following questions: (i) Does nucleation improve species and functional diversity compared to natural forest regeneration? (ii) Do the nucleation techniques differ in terms of species and functional diversity? (iii) Does nucleation lead to more flowering and fruiting species, and a higher proportion of native species in comparison to natural regeneration? (iv) Are the effects on FD more pronounced than on species diversity? (v) How do the different nucleation treatments shift over time compared to controls?
Section snippets
Study area
The study was conducted in the Andean region of Colombia, in the mountain range of the Eastern Cordillera, specifically in the Eastern Forest Reserve of Bogota (Fig. A1a) that borders the city to the East (4°36′42” N, 74°3′35”W). The Forest Reserve ranges in altitude of 2600–3500 m and contains Andean Forest and Páramo ecosystems. Large parts of the forest cover were cleared since European settlement (García Castro et al., 2006). At present, the reserve contains scattered remnants of disturbed
Species diversity and community composition
Nucleation technique (χ2 = 10.9, df = 3, p < 0.012) and time (χ2 = 172.8, df = 3, p < 0.001) had significant effects on species richness (Fig. 1). Seed bank transfer showed significantly greater species richness than the control treatment by the end of the study (z.ratio = 3.13, df = Inf, p = 0.009), while overall species richness was greatest by month 12 and significantly greater than in the previous months (M9: z.ratio = 5.14, df = Inf, p < 0.001; M6: z.ratio = 9.93, df = Inf, p < 0.001; M3:
Discussion
Species richness increased with time in all nucleation techniques, and seed bank transfer was the only treatment to differ substantially from the control (i.e. natural regeneration) during the first year of restoration. Even though species richness was not as large as in the established sapling clusters, which occupied larger areas, nucleation steadily increased the number of species over time. It has been shown that removing the biomass of invasive grasses and overturning the soil (as in our
Conclusion
This study shows that nucleation increases species richness and FD in abandoned pastures where succession is arrested. The transfer of seed bank from secondary or well-preserved forests fosters FD, site heterogeneity and resource offer. However, the presence of undesired non-native species in nucleation techniques can limit their benefit. Even though nucleation promotes a rapid species turnover and functional composition already within 1 year, the convergence in species and trait composition
Funding statement
This study was funded in 2015 by the Jardín Botánico de Bogotá José Celestino Mutis within the framework of restoration ecology, biodiversity and ecosystem services research conducted in the scientific sub-direction.
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgments
Thanks to the field workers of the Jardín Botánico de Bogotá José Celestino Mutis supporting the setup and maintenance of the experiment. We thank Ana María Medina, José López and Carlos Fonseca for collecting and processing the plant material to obtain trait data. Luis Ávila supported the design and preparation of the plant mats. The Universidad Distrital Francisco José de Caldas and the project “Insumos técnicos para la delimitación de ecosistemas estratégicos, páramos y humedales” signed
Author contributions
SRB and JS conceived and designed the research; SRB performed the experiments; SRB and JS monitored the experiment and collected data on functional traits; SRB and LHT analyzed the data; SRB, JK and LHT wrote and edited the manuscript.
References (97)
- et al.
The use of nucleation techniques to restore the environment: a bibliometric analysis
Nat. Conserv.
(2014) - et al.
Generalized linear mixed models: a practical guide for ecology and evolution
Trends Ecol. Evol.
(2009) - et al.
Applied nucleation as a forest restoration strategy
For. Ecol. Manag.
(2012) - et al.
Restoration of seasonal semideciduous forests in Brazil: influence of age and restoration design on forest structure
For. Ecol. Manag.
(2004) - et al.
Topsoil for restoration: resprouting of root fragments and germination of pioneers trigger tropical dry forest regeneration
Ecol. Eng.
(2017) - et al.
When and where to actively restore ecosystems?
For. Ecol. Manag.
(2011) - et al.
Functional diversity: an overview of its history and applicability
Nat. Conserv.
(2015) - et al.
Functional diversity changes during tropical forest succession
Perspect. Plant Ecol. Evol. Syst.
(2012) - et al.
Towards a standardized Rapid Ecosystem Function Assessment (REFA)
Trends Ecol. Evol.
(2015) - et al.
Forest restoration in southern Amazonia: Soil preparation triggers natural regeneration
For. Ecol. Manag.
(2019)