Biol. Rev. (2021), 96, pp. 1114–1134. 1114 doi: 10.1111/brv.12694 The role of land-use history in driving successional pathways and its implications for the restoration of tropical forests Catarina C. Jakovac1,2* , André B. Junqueira1,3, Renato Crouzeilles1,4,5, Marielos Peña-Claros2, Rita C. G. Mesquita6 and Frans Bongers2 1 International Institute for Sustainability, Estrada Dona Castorina, 124, Rio de Janeiro, 22460-320, Brazil 2 Forest Ecology and Management Group, Wageningen University & Research, Wageningen, 6700 AA, The Netherlands 3 Institut de Ciència i Tecnologia Ambientals, Universitat Autònoma de Barcelona, Carrer de les Columnes s/n, Cerdanyola del Vallès, Barcelona, 08193, Spain 4 International Institute for Sustainability Australia, Canberra, ACT, 2602, Australia 5 Mestrado Profissional em Ciências do Meio Ambiente, Universidade Veiga de Almeida, Rio de Janeiro, 20271-901, Brazil 6 Instituto Nacional de Pesquisas da Amazônia, Av. André Araújo, 2936, Manaus, 69083-000, Brazil ABSTRACT Secondary forests are increasingly important components of human-modified landscapes in the tropics. Successional pathways, however, can vary enormously across and within landscapes, with divergent regrowth rates, vegetation struc- ture and species composition. While climatic and edaphic conditions drive variations across regions, land-use history plays a central role in driving alternative successional pathways within human-modified landscapes. How land use affects succession depends on its intensity, spatial extent, frequency, duration and management practices, and is mediated by a complex combination of mechanisms acting on different ecosystem components and at different spatial and temporal scales. We review the literature aiming to provide a comprehensive understanding of the mechanisms underlying the long-lasting effects of land use on tropical forest succession and to discuss its implications for forest restoration. We orga- nize it following a framework based on the hierarchical model of succession and ecological filtering theory. This review shows that our knowledge is mostly derived from studies in Neotropical forests regenerating after abandonment of shift- ing cultivation or pasture systems. Vegetation is the ecological component assessed most often. Little is known regarding how the recovery of belowground processes and microbiota communities is affected by previous land-use history. In pub- lished studies, land-use history has been mostly characterized by type, without discrimination of intensity, extent, dura- tion or frequency. We compile and discuss the metrics used to describe land-use history, aiming to facilitate future studies. The literature shows that (i) species availability to succession is affected by transformations in the landscape that affect dispersal, and by management practices and seed predation, which affect the composition and diversity of propagules on site. Once a species successfully reaches an abandoned field, its establishment and performance are dependent on resistance to management practices, tolerance to (modified) soil conditions, herbivory, competition with weeds and inva- sive species, and facilitation by remnant trees. (ii) Structural and compositional divergences at early stages of succession remain for decades, suggesting that early communities play an important role in governing further ecosystem functioning and processes during succession. Management interventions at early stages could help enhance recovery rates and manipulate successional pathways. (iii) The combination of local and landscape conditions defines the limitations to suc- cession and therefore the potential for natural regeneration to restore ecosystem properties effectively. The knowledge summarized here could enable the identification of conditions in which natural regeneration could efficiently promote forest restoration, and where specific management practices are required to foster succession. Finally, characterization of the landscape context and previous land-use history is essential to understand the limitations to succession and there- fore to define cost-effective restoration strategies. Advancing knowledge on these two aspects is key for finding * Address for correspondence (Tel: +31 317 48 61 95; E-mail: catacj@gmail.com) Biological Reviews 96 (2021) 1114–1134 © 2021 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society. This is an open access article under the terms of the Creative Commons Attribution‐NonCommercial License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes. Land-use effects on secondary succession 1115 generalizable relations that will increase the predictability of succession and the efficiency of forest restoration under dif- ferent landscape contexts. Key words: ecological filter, human-modified landscapes, secondary succession, natural regeneration, resilience, forest restoration, tropical forests, ecosystem functioning CONTENTS I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1115 II. A framework describing successional pathways . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1116 III. The socio-economic drivers of site availability to succession . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1116 IV. How land-use history defines successional pathways . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1118 (1) Descriptors of land-use history . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .1118 (2) Vegetation patterns defined by previous land-use history . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .1119 (3) Land-use effects on species availability to succession . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .1120 (a) Seed dispersal limitation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1120 (b) Seed and sprout resistance to management practices . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1121 (c) Seed predation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1122 (4) Land-use effects on species establishment and performance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .1122 (a) Modified soil chemical and physical properties . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1122 (b) Modified soil biology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1123 (c) Competition with weeds and invasive plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1123 (d) Facilitation by remnant trees . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1124 (e) Herbivory . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1124 V. Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1124 (1) Land-use effects on ecosystem functioning . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .1124 (2) Implications for forest restoration based on natural regeneration . . . . . . . . . . . . . . . . . . . . . . . . . . .1125 VI. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1127 VII Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1127 VIII. References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1127 IX. Supporting information . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1134 I. INTRODUCTION restoration initiatives where natural forest regeneration is being considered as a low-cost alternative to tree planting and a prom- Across the tropics, large extents of forests have been converted ising means to foster large-scale restoration (e.g. Lamb, 2014; to other land uses, mainly agriculture and pastures. Once agri- Chazdon & Guariguata, 2016; Crouzeilles et al., 2017; Chaz- cultural and pastoral use cease and fields are abandoned, they don et al., 2020). The success of natural regeneration as a strat- can be covered by natural forest regeneration giving place to egy to restore ecosystems, however, is very variable (Crouzeilles secondary forests (also called regrowth or successional forests). et al., 2019) and depends on having favourable socio-economic Successional forests are increasingly widespread in tropical and biophysical conditions for regrowth (Holl & Aide 2011, regions, estimated to cover ca. 600 million hectares around the Crouzeilles et al., 2017, Meli et al., 2017, Chazdon et al., 2020). world, together with selectively logged forests (Brown & The rate at which different vegetation attributes recover and Lugo, 1990; Pan et al., 2011). Immersed in human-modified the capacity of successional forests to attain levels similar to landscapes, secondary forests can maintain important ecosys- old-growth forests is highly variable. Within a successional path- tem services including carbon sequestration (Chazdon way, differential recovery of vegetation attributes is related to et al., 2016; Poorter et al., 2016), nutrient cycling (Powers & the complexity of underlying processes. For example, biomass Marín-Spiotta, 2017), hydrological regulation (Ziegler recovers around three times faster than species richness et al., 2009), biodiversity recovery (Strassburg et al., 2016; (Poorter et al., 2016; Rozendaal et al., 2019), because the later Rozendaal et al., 2019), and connectivity between forest frag- depends on the re-establishment of more complex biotic inter- ments (Stouffer et al., 2006; Arroyo-Rodríguez et al., 2017). Sec- actions. Across successional pathways, differences in recovery ondary forests may also deliver direct resources to local rates of vegetation attributes can indicate differential resilience, populations such as timber, firewood, non-timber forest prod- i.e. capacity to recover to old-growth forest levels (Mesquita ucts (NTFPs) (Junqueira, Shepard & Clement, 2011), as well et al., 2001; Norden et al., 2015; Arroyo-Rodrígues as sustaining crop productivity in swidden-fallow systems et al., 2017). Some pathways can have extremely slow recovery (Silva-Forsberg & Fearnside, 1997; Junqueira et al., 2011; of all vegetation attributes and be considered in an arrested suc- Jakovac et al., 2016b). Regrowth is gaining importance also in cessional stage (Mesquita et al., 2015). While part of this Biological Reviews 96 (2021) 1114–1134 © 2021 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society. 1116 Catarina C. Jakovac et al. variation is driven by idiosyncratic and stochastic processes, suc- and on models describing succession in human-modified land- cessional pathways are strongly influenced by biophysical condi- scapes (e.g. Chazdon, 2014; Mesquita et al., 2015; Martínez- tions, landscape context and how the land was used prior to its Ramos et al., 2016; Arroyo-Rodríguez et al., 2017). abandonment for regrowth (hereafter called previous land-use This framework illustrates the idea that a combination of history). Climatic and edaphic conditions best explain differ- socio-economic and biophysical factors defines where and ences in successional pathways at regional and continental scales when regrowth will occur, i.e. site availability to succession (Moran et al., 2000; Poorter et al., 2016), while landscape context (Fig. 1, arrow 1). These factors also define (and are partly and previous land-use history largely drive successional path- defined by) land-use patterns and landscape context (Fig. 1, ways at local and landscape scales (Mesquita et al., 2015; Martí- arrow 2). Ecological processes governed by characteristics nez-Ramos et al., 2016; Arroyo-Rodríguez et al., 2017). At local of the landscape and by management practices associated scales, management practices affect the legacies from former with land-use history define filtering processes that act upon vegetation such as seeds, roots and stumps, and modify soil con- species availability (Fig. 1, arrow 3) and species establishment ditions and biotic interactions (Hooper, Legendre & and performance (Fig. 1, arrow 4), finally shaping succes- Condit, 2004; Styger et al., 2007). At regional scales, land use sional communities. In an interactive process, we use the out- modifies landscape context, i.e. composition and configuration, comes of this review to complement the framework with the affecting the seed rain and environmental conditions major processes underlying the effects of land-use history (e.g. temperature, moisture and wind) under which succession on succession (Fig. 1, white boxes). can proceed (Nepstad et al., 1996; Arroyo-Rodríguez In Section III we provide an overview of knowledge on the et al., 2017). The effects of previous land-use history on succes- socio-economic drivers of regrowth, aiming to contextualize sion will also depend on the intensity, spatial extent, frequency, where, when and for how long regrowth is allowed in current and duration of land use (Turner, 2010; Chazdon, 2014). human-modified landscapes. In Section IV.1, we provide a liter- Therefore, what is broadly called ‘land-use effects’ is actually ature review on studies that explicitly investigated the role of a complex combination of processes and mechanisms acting land-use history on secondary succession. The aim was to: iden- on different ecosystem components and at different spatial tify the descriptors used to characterize land-use history and temporal scales. Understanding the ecological processes (Section IV.1); describe successional pathways associated with and mechanisms underlying land-use effects on succession is land-use history (Section IV.2); and present the mechanisms crucial for predicting the potential for natural regeneration as underlying the effects of land-use history on successional commu- a forest restoration strategy, and for designing practices to assist nities (Sections IV.3 and IV.4). We used the databases Web of Sci- succession and enhance its ecological quality and economic ence and Scopus using the search strings “land use” AND benefits for landowners (Forero-Montaña et al., 2019). “succession*” AND “tropic*” in the title, abstract and key words. In this review we synthesize knowledge on how land-use We did not restrict the search by publication date, returning history affects tropical forest succession in human-modified 565 published studies up to November 2020. We screened the landscapes. We focus on succession after clear cut, and there- title and abstract to select only studies that explicitly addressed fore do not include studies evaluating regeneration after log- the role of variation in previous land-use history on tropical sec- ging or in degraded forest fragments. The main aim is to ondary forests. Studies that addressed only temporal changes elucidate the mechanisms underlying the divergence of succes- over succession or comparisons of secondary forests solely with sional pathways in human-modified landscapes, and to discuss old-growth forests were not included [see Chazdon (2014) for a the implications for ecosystem functioning and forest restora- comprehensive review]. After eliminating non-relevant articles tion based on natural regeneration. This study complements and complementing with references cited therein, a total of previous reviews that focused on successional processes 196 articles were assessed for full content. Results of this search (Chazdon, 2014), on specific regions (e.g. Mártinez-Ramos are presented in Section IV and provided as online supporting et al., 2016) and on landscape context (Arroyo-Rodríguez information (Table S1). We discuss these results in the context et al., 2017), by providing a comprehensive overview of descrip- of the implications for ecosystem functioning and for forest resto- tors of land-use history and their effects on different ecological ration based on natural regeneration in Section V. components in secondary forests across the tropics. III. THE SOCIO-ECONOMIC DRIVERS OF SITE II. A FRAMEWORK DESCRIBING AVAILABILITY TO SUCCESSION SUCCESSIONAL PATHWAYS The occurrence, distribution and permanence of secondary This review is organized following a framework that summa- forests are driven by complex interactions between ecologi- rizes the main drivers of successional pathways in human- cal, environmental, socio-cultural, economic and political modified landscapes (Fig. 1, solid grey boxes). The framework factors operating at different spatial, temporal and organiza- is founded on previous studies on the hierarchical basis of suc- tional scales (Perz & Almeyda, 2010; Latawiec et al., 2016) cession (Pickett, Collins & Armesto, 1987), community assembly (Fig. 1, arrow 1). Forest regrowth typically occurs when pressure rules (Grime, 1998; Lortie et al., 2004; Peterson & Carson, 2008) on land diminishes, which may happen as a consequence of Biological Reviews 96 (2021) 1114–1134 © 2021 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society. Land-use effects on secondary succession 1117 Socio-economic and (1) Site availability to biophysical factors succession (2) Dispersal limitation On-site dispersal (3) Propagule resistance Species availability Disperser attraction Seed predation (6) Land-use history and landscape integrity Soil resource availability Nutrient cycling (4) Competition with weeds Species establishment and Competition/facilitation Facilitation by remnants performance Abiotic conditions Herbivory (5) Successional communities Fig 1. Main pathways through which land-use structures successional communities in human-modified landscapes. Socioeconomic and biophysical factors determine the abandonment of agricultural fields and availability of space for succession to proceed (1), as well as land-use patterns that define landscape integrity and management practices (2). Land use affects species availability (3) and species establishment and performance (4) through direct effects of landscape integrity and management practices and indirect effects of modified resources availability and biotic interactions. Land-use-mediated ecological filters reduce the set of species available in the seed and sprouts bank and seed rain (3), constrain the species able to establish successfully (4) and, combined with species life history, determine which species will perform best and dominate. The established plant community will then feed back (5, 6) the successional process by modifying on-site seed rain, environmental conditions and biotic interactions in the understorey. The resulting successional communities can follow different successional pathways. rural–urban migration (e.g. Aide & Grau, 2004; López land-use regulations and subsidies for agriculture also influence et al., 2006; Schmook & Radel, 2008; Rudel et al., 2009; Hecht the decision on allowing regrowth to proceed (Díaz et al., 2011; et al., 2015), changes to other production systems and increased Chazdon et al., 2020). Although decisions on where and when availability of off-farm labour (e.g. Rudel, 2010) or, most often, to abandon land are essentially taken at the household level, the (temporary) abandonment of agricultural lands and pastures these decisions are also triggered by drivers operating at larger (e.g. Arroyo-Mora et al., 2005; Wright & Muller-Landau, 2006; scales, such as regional and national policies (Vieira Chazdon et al., 2020). ‘Marginal’ areas for agriculture such as et al., 2014), land opportunity cost (Crk et al., 2009; Hecht steep slopes (Helmer et al., 2008; Asner et al., 2009; Crk et al., 2015; Chazdon & Guariguata, 2016), land tenure et al., 2009; Rudel et al., 2009), low-fertility soils (Chinea, 2002; (McClellan et al., 2018), market fluctuations (Aide & Arroyo-Mora et al., 2005; Helmer et al., 2008) and/or poorly Grau, 2004; Walsh et al., 2008), conservation initiatives accessible areas are more likely to be permanently abandoned (Harvey et al., 2008), and economic and political changes and to develop forest regrowth (Thomlinson et al., 1996; (Rudel, 2012; Chazdon, 2014). Most often, the trigger is an Daniels, 2010, but see Sloan, Goosem & Laurance, 2015). In interaction of socio-economic and biophysical factors operating other contexts, young secondary forests dominate the land- at multiple spatial and temporal scales. The example of forest scape, driven for example by the intensification of shifting culti- transitions in Puerto Rico in the last 50 years illustrates these vation agriculture (Metzger, 2002; Jakovac et al., 2017). interactions: rapid economic development after the Second Besides their occurrence, the permanence of secondary forests World War led to a shift away from agricultural activities, lead- in the landscape is also a product of socio-economic drivers. ing to an overall increase in forest cover; at local scales, biophys- Recent studies have shown that most regrowth in human- ical factors such as topography ultimately influenced the areas modified landscapes is allowed to proceed for only two decades that were actually abandoned and where forest regeneration or less (Chazdon et al., 2016; Schwartz et al., 2017, 2020; Reid took place (Rudel, Perez-Lugo & Zichal, 2000; Brandeis, et al., 2019; Nunes et al., 2020; Schwartz et al., 2020). The perma- Helmer & Oswalt, 2007; Yackulic et al., 2011). Despite our grow- nence of regrowth is higher in landscapes with lower accessibility, ing understanding and recognition of the relevance of forest population density and demand for agricultural production regrowth, the environmental and socioeconomic factors – and (Metzger, 2002; Jakovac et al., 2017). At the governance sphere, the complex interactions between them that influence the Biological Reviews 96 (2021) 1114–1134 © 2021 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society. 1118 Catarina C. Jakovac et al. likelihood of forest regeneration – are not yet fully understood rainforests and evaluated vegetation attributes (Fig. 2A, B, E). (Aide et al., 2013). This is a promising and necessary pathway The literature review shows that most of our knowledge comes for future research to support the design of governance strategies from succession in abandoned pastures, shifting cultivation sys- for forest restoration (Guariguata & Brancalion, 2014). tems, and cropping fields (Fig. 2D). Most studies evaluated the effects of differential previous land-use history using same-age comparisons and chronosequences (Fig. 2F). Details regarding the 196 articles reviewed are provided in Table S1. IV. HOW LAND-USE HISTORY DEFINES SUCCESSIONAL PATHWAYS (1) Descriptors of land-use history The majority of studies evaluating the effects of previous land- Evaluating the effects of land-use history on succession use history on succession were conducted in Neotropical requires assessing the disturbance regimes, which refer to (A) (B) (C) (D) (E) (F) Fig 2. Quantitative description of reviewed studies according to: Continent (A) and forest type (B) where the study was conducted, the descriptors of previous land-use (LU) history assessed (C), the type of previous land use (D), the response variables analysed (E), and the study approaches used (F; similar-age comparison refers to comparisons across land-use histories with control for age during sampling, chronosequence refers to sampling using space-for-time substitution, longitudinal refers to temporal monitoring of successional patch(es), review/meta-analyses refer to studies that used results from other studies, experimental refers to studies that explicitly manipulated factors, and others refers to modelling, remote sensing and assessment of multiple drivers. Biological Reviews 96 (2021) 1114–1134 © 2021 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society. Land-use effects on secondary succession 1119 the spatial and temporal dynamics of events that disrupt the [see Jakovac et al. (2015) and Zermeño-Hernández structure of an ecosystem, community or population, and et al. (2015)]. The number of burning events has been used change the resource availability or the physical environment as a proxy for the frequency and intensity of previous land (Turner, 2010). In anthropogenic contexts, disturbance use (e.g. Nepstad et al., 1996; Zarin et al., 2005; Jakovac regimes are also defined by qualitative descriptors, such as et al., 2015). Time since deforestation started is usually posi- management practices and crop type. Assessing previous tively correlated with land-use intensity and duration land-use history, therefore, is challenging and ideally (Zermeño-Hernández et al., 2015; Arroyo-Rodríguez requires a combination of field data and remote-sensing et al., 2017; Jakovac et al., 2017). Duration of land use is often approaches (e.g. Dias et al., 2016; Dutrieux et al., 2016). positively correlated with frequency of disturbance and dis- Most studies on secondary succession only reported the tance to forest remnants (Zermeño-Hernández et al., 2015) type of previous land use (61%) but did not assess other and negatively correlated with the amount of forest in the descriptors (Fig. 2C, Table S1). The type of land use is easy landscape (e.g. Moran et al., 2000; Robiglio & Sinclair, 2011). to identify, usually correlates with one or more disturbance Because descriptors of landscape cover are easier to assess descriptors (Zermeño-Hernández et al., 2015), and is com- than land-use history itself, further research should investi- monly used as a proxy for land-use intensity or the severity gate correlations among those in different contexts to estab- of the impact on succession (see Section IV.2). A few articles lish proxies for land-use history. Such proxies could be (10%) explicitly used land-use type as a proxy for land-use retrieved from maps and satellite images in areas where intensity (e.g. Aragón & Morales, 2003; Lakshmipathy, information on land-use history is not available. Accounting Balakrishna & Bagyari, 2012; Ding et al., 2012b; Prieto for descriptors of landscape context and land-use history et al., 2015; Fig. 2C, Table S1). It is important to note that (Table 1) will increase our capacity to predict successional succession studies often refer to land-use intensity as a syno- pathways (Norden et al., 2015; Arroyo-Rodríguez nym for severity referring to the overall ecological effects on et al., 2017) and consequently contribute to the design of res- successional communities rather than to the actual amount toration practices to enhance natural regeneration (see of energy or input implied in the disturbance Section V.2). Therefore, we encourage future studies to (Turner, 2010). This definition differs from those used in assess both local and landscape factors and to try to identify agronomic and land-use studies (see Erb et al., 2013). how they are linked and their relative roles in defining succes- When indicated, the main land-use descriptors were the sional pathways and the potential for natural regeneration. number and frequency of burning events or cropping cycles (e.g. Lawrence, 2004; Zarin et al., 2005; Jakovac et al., 2015; Fig. 2C), the length of the previous fallow period (27 studies; (2) Vegetation patterns defined by previous land-use history e.g. Dalle & de Blois, 2006), and the duration of continuous land use (e.g. Moran et al., 2000; Erb et al., 2013; Table S1). Studies show that different types of previous land-use history Few studies (19%) assessed other management practices, lead to distinct rates of recovery of vegetation structure and bio- such as weeding frequency, soil amendment, machinery diversity. The rates of recovery of biomass and species diversity use, and type of crop to describe previous land-use history in early secondary forests tend to be lower on fields previously (Fig. 2; Table S1). Three studies used vegetation attributes used as pasturelands and subject to mechanized agriculture as proxies for previous land-use impact, such as the identity than on fields in shifting cultivation and low-input agriculture of dominant species, the abundance of remaining crops and (e.g. Ding et al., 2012b; Martínez-Ramos et al., 2016). Biomass canopy cover (Table S1). As indicated by the incomplete recovery rate in Amazonian rain forests, for instance, was information provided by most studies, assessing the complete 40–50% slower on abandoned pastures than on clear cuts land-use history is not trivial and may not always be possible. (Zarin et al., 2005; Mesquita et al., 2015) and 70% slower on Acquisition of such information depends on interviews with mechanized agriculture than on shifting cultivation systems long-term local inhabitants or remote-sensing analysis of (Moran et al., 2000). Succession in non-mechanized agricul- time series, both of which have limitations and can be time tural fields had a twofold higher diversity of native species consuming. Therefore, identifying correlations among and half the percentage of exotic species than bulldozed fields descriptors and finding proxies that are easy to acquire will (Chinea, 2002). Species richness was lower or similar in forests allow more studies to incorporate the effects of previous land regenerating on abandoned pastures compared to low-input use in understanding regrowth patterns and in predicting the agricultural fields, while species composition was consistently potential for natural regeneration as a restoration strategy. divergent (Mesquita et al., 2015; Martínez-Ramos et al., 2016). Correlations among descriptors were often identified. The Land-use types such as agroforestry systems can have longer the duration of land use, the higher the frequency of opposing effects on the recovery of vegetation structure and fire, and the larger the extent of the transformed landscape diversity. Studies in Central America and the Caribbean (Rossi et al., 2010; Zermeño-Hernández et al., 2015). Land- found that the recovery of basal area and biomass is faster use intensity has been described in different ways including after the abandonment of agroforestry systems based on cof- fire intensity (e.g. de Rouw, 1993), grazing intensity fee or cacao than after pastures or palm plantations (Bactris (e.g. Carpenter et al., 2001; Marinho et al., 2016) and combi- gasipaes) (Fernandes & Sanford, 1995; Pascarella et al., 2000; nations of frequency, duration, and management practices Rivera, Zimmerman & Aide, 2000; Marcano-Vega, Aide & Biological Reviews 96 (2021) 1114–1134 © 2021 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society. 1120 Catarina C. Jakovac et al. Báez, 2002). The crop trees remaining from the agroforestry Schwartz, 2011; Ding et al., 2012b; Longworth et al., 2014) system contributed to the more rapid recovery of biomass and differential species composition (e.g. Mesquita and basal area. However, the shaded environment under et al., 2001; Lawrence, 2005b; Styger et al., 2007; Jakovac their canopies constrained the regeneration of native species, et al., 2016a). Additionally, studies show an increase in the rela- leading to lower stem density and species richness of native tive abundance of herbs, invasive ferns, shrubs and lianas at species when compared to pastures (Pascarella et al., 2000; early stages of succession (e.g. Buschbacher, Uhl & Rivera et al., 2000; Marcano-Vega et al., 2002). Serrao, 1988; Rivera et al., 2000; Lawrence, 2005b; Dalle & Besides land-use type, variations in intensity, frequency and de Blois, 2006; Styger et al., 2007; Vieira & Proctor, 2007; duration of previous land use play an important role in defining Klanderud et al., 2009; Hogan et al., 2016; Sanchez-Tapia recovery rates and successional pathways. Historically, shifting et al., 2020). Concomitantly, the species composition of under- cultivation was considered a low-intensity land-use system serv- storey herbs (Bergman et al., 2006; Styger et al., 2007; Ribeiro, ing as a model to describe successional processes in tropical for- Bruna & Mantovani, 2010) and the identity of the canopy- ests (e.g. Uhl & Jordan, 1984; Uhl, 1987; Guariguata & dominant tree species change with previous land-use intensity Ostertag, 2001). Recent studies, however, depicted that even (Zimmerman et al., 1995; Pascarella et al., 2000; Rivera slight increases in management intensity and cut-and-burn fre- et al., 2000; Boucher et al., 2001; Mesquita et al., 2001; Thomp- quency result in strong changes in plant communities and son et al., 2002; Lawrence, 2005b; Franklin et al., 2006; Chai & recovery rates of tropical dry and rain forests, potentially lead- Tanner, 2011; Wallenfang et al., 2015; Hogan et al., 2016). ing to secondary forests with similar characteristics to those Studies in rain forests found that after intensive land use, suc- found in pasturelands (e.g. Gehring, Denich & Vlek, 2005; cession is initiated by long-living pioneers such as Vismia spp. Lawrence et al., 2007; Styger et al., 2007; Ding et al., 2012a; in Central Amazon (e.g. Mesquita et al., 2015; Jakovac Jakovac et al., 2016a). In systems managed with short fallow et al., 2016a), Byrsonima spp. in Mexico (Martínez-Ramos periods (<5 years), the basal area and canopy height of et al., 2016), Moquiniastrum polymorphum in the Atlantic forest secondary-forest fallows are reduced by ca. 14% after each (Sanchez-Tapia et al., 2020) and Psiadia spp. shrubs in Mada- additional cropping cycle (Jakovac et al., 2015). Also, studies gascar (Styger et al., 2007) instead of the classical short-lived suggest that fields used for more than 4–6 cropping cycles pioneers, like Cecropia spp., Trema spp. in the Americas and may converge to arrested successional states where rates of Harungana spp. and Musanga spp. in Africa. Indicator species asso- change in structure, diversity and composition are extremely ciated with different levels of land-use impact have been reported low (Lawrence, 2005a; Styger et al., 2007; Jakovac et al., 2016a). (Chinea, 2002; Styger et al., 2007; Jakovac et al., 2016a), and could Variations in land-use history within land-use types generate be used together with other metrics to classify the ecological variation in the rates of recovery of vegetation structure. integrity of successional pathways and identify the need for resto- Increased intensity, frequency, spatial extension and duration ration actions to foster regrowth and species diversity. of previous land use leads to reduced regrowth rates of tree bio- Different frequencies of fire also lead to divergence in func- mass, basal area, canopy height and species richness (Hughes, tional traits in secondary forests regenerating in pastures Kauffman & Jaramillo, 1999; Lawrence, 2004; Gehring (Fernandes Neto et al., 2019; Sanchez-Tapia et al., 2020; Sanse- et al., 2005; Lawrence et al., 2007; Styger et al., 2007; Williams- vero et al., 2020). In Central Amazon, fire-managed pastures Linera et al., 2011; Jakovac et al., 2015; Zermeño-Hernández gave place to secondary forests with higher wood density, and et al., 2015; Villa et al., 2018; Cabral-Gomes et al., 2020). It also lower leaf dry matter content and seed mass than those follow- leads to lower plant density (Williams-Linera et al., 2011; Zer- ing clear cut (Fernandes Neto et al., 2019). In the Atlantic For- meño-Hernández et al., 2015; Sanchez-Tapia et al., 2020) but est, increased frequency of fire led to communities with lower higher density of stems (e.g. Pascarella et al., 2000; Gehring wood density and leaf area index and higher bark thickness et al., 2005; Longworth et al., 2014; Sanchez-Tapia and seed mass (Sanchez-Tapia et al., 2020). More studies are et al., 2020). This apparent contradiction is probably a result needed to verify how land-use history affects functional compo- of the impoverishment of the soil seed bank and increased sition in other biogeographic and landscape contexts. dependency on resprouters, as suggested by the increased pro- The reviewed studies show that previous land-use history portion of multi-stemmed trees and lianas (Gehring is strongly associated with vegetation structure, diversity et al., 2005; Jakovac et al., 2015; Sanchez-Tapia et al., 2020). and composition of moist and dry secondary forests. Overall The few studies that found no significant effects of land-use his- the studies support that longer and/or more intensive previ- tory on regrowth rate or species diversity (Zimmerman ous land-use history leads to secondary forests with reduced et al., 1995; Peña & Duque, 2013; Derroire et al., 2016b; Poorter recovery rates, an impoverished plant community and a et al., 2016; Wood, Rhemtulla & Coomes, 2017) attributed these characteristic species taxonomic and functional composition. results to the lack of detailed information on previous land-use history or to narrow variation in its descriptors. (3) Land-use effects on species availability to Land-use history not only affects vegetation structure, but succession also regulates the variation of species composition among path- (a) Seed dispersal limitation ways. With increasing intensity, frequency or duration of previ- ous land use, there is a slower species turnover (Peterson & Dispersal limitation defines the quantity and quality of seed Carson, 2008; Klanderud et al., 2009; Mwampamba & rain in successional fields (Fig. 1). According to reviewed Biological Reviews 96 (2021) 1114–1134 © 2021 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society. Land-use effects on secondary succession 1121 studies, dispersal limitation is one of the most important con- Chapman, 1999; Slocum, 2001; Guevara et al., 2004; straints to regeneration in pastures and agricultural fields Hooper et al., 2004). (e.g. Holl et al., 2000; Hooper et al., 2004; Palomeque The landscape composition, i.e. the distribution of land- et al., 2017). The conversion of native vegetation into differ- use types in the landscape, also affects the amount and com- ent types of land use inevitably modifies the sources of seed position of the seed rain in successional fields. Agricultural rain by transforming landscape configuration and composi- fields and pastures immersed in the landscape contribute tion through forest fragmentation, reduction of forest cover, with seeds from pioneer herbs, shrubs, climbers, potentially expansion of young secondary forests and the presence of iso- invasive species and from a few bat-dispersed species typical lated trees in the agricultural matrix (Lawrence, Peart & of disturbed areas (Dupuy & Chazdon, 1998; Duncan & Leighton, 1998; Metzger, 2002; Robiglio & Sinclair, 2011; Chapman, 1999). Secondary forest patches immersed in Arroyo-Rodrigues et al., 2017; N’Guessan et al., 2019). The agricultural landscapes mostly contribute early-successional amount of forest cover in the landscape and the distance of species to regenerating sites (Hooper et al., 2004; Nascimento forest remnants to successional patches influences the seed et al., 2006). The age distribution of such patches in the land- rain in successional fields. scape, however, will influence the composition of the seed Studies show that the density and diversity of regenerating rain as it is related to species turnover over time trees decreases sharply with distance from the forest edge (Lawrence, 2004; van Breugel et al., 2013). The floristic com- (e.g. Guariguata et al., 1997; Martínez-Garza & González- position across the landscape also defines the availability and Montagut, 1999; Holl et al., 2000; Mesquita et al., 2001; Bení- species composition of animal dispersers (Bobrowiec & tez-Malvido et al., 2005; Jakovac et al., 2015). Studies suggest Gribel, 2010). Additionally, the dominant tree species in that most seed dispersal in human-modified landscapes these secondary forests will influence the composition of dis- occurs within 300 m of the forest border towards open areas persers and potentially feed back in the composition of the (e.g. Cubiña & Aide, 2001; Hooper et al., 2004; successional plant community (Bobrowiec & Gribel, 2010). Lawrence, 2004). The rate of seed arrival and the composi- Post-dispersal by cattle and insects play a minor role in re- tion of the seed rain at different distances from the forest will distributing seeds across open fields but may contribute to depend on dispersal modes and the niche of dispersers. Most changes in the species composition of regrowth (Esquivel animal-dispersed seeds reach shorter distances from the for- et al., 2008; L.C. Leal, Andersen & Leal, 2014b). est edge (e.g. average 4 m in Cubiña & Aide, 2001) than wind-dispersed seeds (e.g. average 250 m in Holl, 1998). (b) Seed and sprout resistance to management practices Overall, generalist dispersers can reach longer distances than forest frugivorous vertebrates (Howe & Smallwood, 1982; The seed and sprout bank in the soil is a result of the accumu- Holl et al., 2000; Benítez-Malvido, Martínez-Ramos & lated seed rain and of the legacies of the original forest left Ceccon, 2001; Robiglio & Sinclair, 2011). As a consequence, after disturbance, such as seeds, sprouts and seedlings, and the proportion of late-successional species and the density of is the other main source of species in tropical forest succession seed rain declines with distance to the forest (Uhl et al., 1981; Cubiña & Aide, 2001; Klanderud (Lawrence, 2004). Studies found that the seed rain in agricul- et al., 2009; Sousa et al., 2017). The composition and density tural fields and pastures is mainly from early-successional of soil seed banks, however, depends not only on legacies species (>85%), which are mostly dispersed by wind or gen- from the previous forest but also on the arrival of species dis- eralist birds and bats (Benítez-Malvido et al., 2001; persed from surrounding sources, either from forest frag- Martínez-Garza et al., 2011; Wieland et al., 2011). In dry for- ments or from other types of land use. The viability of ests, the prevalence of wind dispersal over animal dispersal recalcitrant seeds from late-successional species, which are (Vieira & Scariot, 2006) makes the plant community less often legacies from the previous forest, is reduced with the affected by dispersal limitations than in moist forests duration of land use (Garwood, 1989; Cubiña & (Lebrija-Trejos et al., 2010; Griscom & Ashton, 2011). Aide, 2001), while the seed bank from herbs and shrubs is Dispersal limitation can be reduced by the management boosted (Guevara, Moreno-Casasola & Sanchez- practice of allowing isolated trees in pastures and cropping Rios, 2005). fields. Remnant trees left in the fields increase the rate of bio- Management practices during land use also impact the mass recovery (N’Guessan et al., 2019), and provide perches legacies by reducing the viability of seeds and sprouts and for dispersers, enhancing the seed rain dispersed by frugivo- by differentially favouring certain species (Fig. 1, arrow 4). rous bats and birds (e.g. Vieira, Uhl & Nepstad, 1994; In large-scale agriculture, bulldozing and repeated plough- Otero-Arnaiz et al., 1999; Benítez-Malvido et al., 2001; Gue- ing eliminate stumps and sprouting roots (Chinea, 2002). In vara, Laborde & Sanchez-Rios, 2004), thus increasing the small-scale low-input agriculture, field management usually diversity and density of seeds from tree species (Guevara relies on manual weeding, which has a lower impact on et al., 2005). The morphological and phenological character- regenerating sources than machinery, but still eliminates spe- istics of the remnant trees affect the abundance and species cies with a transient seed bank or low sprouting ability composition of the seed rain below their crowns (Sandor & (e.g. Uhl et al., 1981; de Rouw, 1993; Jakovac et al., 2016b), Chazdon, 2014), due to differential attraction of dispersers and favours the persistence of native tree species that are use- (Guariguata, Rheingans & Montagnini, 1995; Duncan & ful for farmers (Junqueira, Shepard & Clement, 2010). Biological Reviews 96 (2021) 1114–1134 © 2021 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society. 1122 Catarina C. Jakovac et al. Recurrent cutting and burning is a common practice in and erosion reduces the concentration mainly of N, potas- tropical agricultural fields and pasturelands that gradually sium and phosphorus (P) in the topsoil (Arnason, 1982; Jor- selects for fire-resistant species (Vieira et al., 1994; Holl dan et al., 1983; Holscher et al., 1997; Runyan, et al., 2000; Hooper et al., 2004; Kalaba et al., 2013; D’Odorico & Lawrence, 2012). Leaching and erosion Sanchez-Tapia et al., 2020), and along with grazing and become more important with extended cropping period weeding selects for strong sprouters and clonal species (Kleinman, Pimentel & Bryant, 1995), in permanent cultiva- (Uhl et al., 1981; de Rouw, 1993; Aide & Cavelier, 1994; Pas- tion systems and pastures (Buschbacher et al., 1988; Holscher carella et al., 2000; Hooper et al., 2004; Lawrence, 2005b; et al., 1997), and in areas with steep slopes (Ramakrishnan & Dalle & de Blois, 2006; Klanderud et al., 2009; Williams- Toky, 1981). Bulldozing and repeated burning eliminate Linera et al., 2011; Massad et al., 2013; Jakovac dead logs, which are important long-term sources of cations et al., 2016a). The presence of sprouters has been shown to and soil carbon (Jordan et al., 1983; Uhl & Jordan, 1984; facilitate the recovery of species composition in dry forests Buschbacher et al., 1988; Ribeiro-Filho, Adams & (Williams-Linera et al., 2011). Murrieta, 2013). The longer the duration of continuous land use, the lower the levels of organic matter and nutrients in the soil, and the higher the degradation of soil structure, includ- (c) Seed predation ing reduced porosity, aeration, soil carbon content and water The environment transformed by land use favours seed pred- infiltration capacity. Studies suggest that pastures result in ators and pathogens, reducing the rate of seed survival by larger changes in the soil nutrients pool than small-scale agri- 30–90% (Alvarez-Buylla & Martínez-Ramos, 1990; Martí- culture or agroforestry systems (Moreira et al., 2009). nez-Garza & González-Montagut, 1999). This significantly Land-use practices could potentially improve soils and constrains the accumulation of forest species in the soil seed enhance regrowth, but in general soil improvements during banks of pastures and agricultural fields, reducing species land use do not last for long (but see Glaser & Birk, 2012). availability for succession (Nepstad et al., 1996; Holl, 1998; Although fertilization increases nutrient availability in the Cubiña & Aide, 2001). A higher number of seeds tend to short term (Buschbacher et al., 1988; MacDonald, Bennett & be lost to predation than to pathogens (Myster, 2003), but Taranu, 2012; Ribeiro-Filho, Adams & Murrieta, 2013), the role of pathogens has received less attention and remains nutrients are rapidly taken up by the crops or regrowing veg- unclear (Dalling et al., 2011). Studies in the Neotropics show etation (Abadın et al., 2002), adsorbed to clay particles and that 42–80% of woody species from the seed bank of pastures metal (hydr-)oxides, and gradually lost by leaching and ero- and shifting cultivation fields are consumed by predators sion (Holscher et al., 1997; MacDonald et al., 2012). such as ants, grasshoppers and small rodents (Alvarez- Reduced soil fertility after different land-use histories has Buylla & Martínez-Ramos, 1990; Aide & Cavelier, 1994; been associated with slower regrowth [Uhl & Jordan, 1984; Nepstad et al., 1996; Wijdeven & Kuzee, 2000). The rate of Aide & Cavelier, 1994; Laurence et al., 1999; Kanowski seed predation varies with plant and predator species et al., 2003; Lawrence, 2005a; Villa et al., 2018; but see John- (Uhl, 1987; Aide & Cavelier, 1994; Myster, 2003), possibly son et al. (2001) and Ding et al. (2012b)], lower species rich- leading to differential success of successional plant species ness, altered species composition (Chinea, 2002; Styger in abandoned fields. The magnitude of such impacts on suc- et al., 2007; Ding et al., 2012b; Wallenfang et al., 2015; Jakovac cessional pathways, however, remains unclear – and may be et al., 2016a), and lower seedling survival and growth context-dependent – and should be investigated further. (Román-Dañobeytia et al., 2012; Wood et al., 2017). Reduced P availability due to intensive land use has been specifically linked to a decrease in regrowth rate in Central America (4) Land-use effects on species establishment and (Arnason, 1982), Asia (Lawrence et al., 2010; Runyan performance et al., 2012) and the Amazon (Jordan et al., 1983; Gehring Once a species has arrived at a site, its establishment success et al., 1999; Davidson et al., 2004), as well as to reduced spe- and performance will depend on the species’ life-history cies richness and changes in species composition strategies combined with resource availability and biotic (Uhl, 1987; Lawrence, 2005b; Ding et al., 2012b; Jakovac interactions (Pickett et al., 1987), which are both influenced et al., 2016a; Villa et al., 2018). by management practices and landscape context (Fig. 1, It is difficult to disentangle the role of soils in forest arrows 3 and 4). regrowth in observational studies, as soil properties often cor- relate with management intensity, distance from the forest and soil type (e.g. MacDonald et al., 2012). Fertilization (a) Modified soil chemical and physical properties experiments, on the other hand, provide direct evidence Conventional agriculture and cattle ranching gradually showing that regrowth in pastures is limited by N and P avail- reduce soil fertility due to nutrient losses by different prac- ability (Davidson et al., 2004) and that N and P fertilization tices (Sommer et al., 2004; Bruun, Mertz & Elberling, 2006; increased the biomass dominance of a few pioneer species Styger et al., 2007; Wallenfang et al., 2015). Burning volatil- (Gehring et al., 1999) reducing community evenness and izes organic matter, carbon, nitrogen (N) and sulfur diversity (Siddique et al., 2010). Such results were related to (Holscher et al., 1997; Certini, 2005). Harvesting, leaching differential growth responses to fertilization among tree Biological Reviews 96 (2021) 1114–1134 © 2021 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society. Land-use effects on secondary succession 1123 species, with P limiting the growth of Inga macrophylla but not conclusions. The role of soil microbial communities in suc- of Vismia guianensis, for example (Gehring et al., 1999). cessional pathways remains unclear and deserves further Reduced soil P availability may also restrict the performance investigation (for an extended discussion see Powers & of nitrogen-fixing legumes (Gehring et al., 1999; Hedin Marín-Spiotta, 2017). et al., 2009) significantly affecting nitrogen availability and Among macrofauna, earthworms have received higher nutrient cycling during succession (Erickson, Keller & attention due to their importance as soil engineers that help sus- Davidson, 2001; Batterman et al., 2013). tain the soil microbiota and improve soil quality for plant The intensity of previous land use, therefore, affects the growth (Fragoso et al., 2016). Across the tropics, agriculture relationship between soil and regrowth: if regrowth is and pasture lead to reductions in the abundance and diversity allowed just after burning or after low-intensity land use of native earthworms, to local loss of entire functional groups there may be no nutrient limitation to native tree species and to the spread of invasive exotic species (Fragoso (Jordan et al., 1983; Uhl & Jordan, 1984; Johnson et al., 2016; Rossi et al., 2010), with consequences such as et al., 2001; Lawrence, 2005b), but when regrowth occurs long-lasting soil compaction (Chauvel et al., 1999) and reduced on intensively used cropping fields or pasturelands, it will decomposition rate (Geissen & Guzman, 2006). Low diversity be slower and with lower species diversity mainly due to N and slow recovery of native macrofauna are related to longer and P limitation (Gehring et al., 1999; McGrath et al., 2001; duration of land use, more intense soil transformation, more Davidson et al., 2004). Current scientific knowledge supports frequent fires, and larger extent of transformed landscape the idea that soil conditions transformed by land use are (Castaño-Meneses & Palacios-Vargas, 2003; Sánchez-de important drivers of alternative successional pathways. More León & Zou, 2004; Rossi et al., 2010). The current knowledge experimental studies carried out in different contexts are suggests that land-use-induced changes in soil biology might needed to separate the effects of nutrient limitation from contribute to alternative successional pathways, particularly management practices and landscape factors. at early stages, but that this effect may vanish within the first decades of succession. (b) Modified soil biology During land use, intense tillage, continuous cropping, (c) Competition with weeds and invasive plants replacement of trees with annual species or exotic pasture grasses and lack of a litter layer all contribute to reduced soil Previous land-use practices affect seed germination, seedling organic matter content (McGrath et al., 2001; Moreira establishment and the performance of tree species by et al., 2009; Smith et al., 2014; Smith, Marín-Spiotta & strengthening biotic interactions such as competition. Recur- Balser, 2015). Such loss along with the use of pesticides rent fire events and continuous cultivation favour coloniza- reduces the abundance and diversity of soil macro- and tion by weeds, lianas and invasive species (de Rouw, 1995; microbiota and changes their community composition Jakovac et al., 2016b; Palomeque et al., 2017), which rapidly (Templer et al., 2005; Ayuke et al., 2011; Smith et al., 2014; cover the ground and reduce light availability at ground Fragoso et al., 2016; Birhane et al., 2017; Zhou, Wang & level. This environment may restrict the germination of Luo, 2018). many pioneer species with germination triggered by light Changes in soil microbiota may imply a reduction in nutri- (Alvarez-Buylla & Martinez-Ramos, 1992; Benítez-Malvido ent availability to plants, especially through organic P pools et al., 2001; Bentos, Nascimento & Williamson, 2013), such (Hamer et al., 2013) and reduced N fixation (Gavito as Cecropia and Trema, for example (Suazo-Ortuño et al., 2008; Batterman et al., 2013), which may negatively et al., 2015). It is important to note, though, that under affect seedling survival and growth (Gavito et al., 2008; extreme degradation, the presence of any vegetation cover Menge & Chazdon, 2016). Moreover, infestation by arbus- may favour the germination of forest species as it ameliorates cular mycorrhiza can promote differential species survival the harsh environmental conditions (Catterall, 2016). during regeneration (Menge & Chazdon, 2016; Bachelot After seed germination, competition for light and nutrients et al., 2018). The few studies available suggest that recovery with climbers and invasive species reduce seedling perfor- of soil microbial communities happens relatively rapidly, tak- mance of successional forest species. Climbers and bamboos ing between 5 and 15 years after succession starts to reach (not all invasive) are usually resistant to disturbance and tol- similar levels to old-growth forests (Guggenberger & erant to high light availability, being favoured by repeated Zech, 1999; Templer et al., 2005; Hamer et al., 2013; Cai burning, and intensive and continuous land use (Gehring et al., 2018). Higher intensity of land use can, however, et al., 2005; Sovu et al., 2009; Jakovac et al., 2015). At early reduce the recovery rates of arbuscular mycorrhizal commu- stages of succession climbers can spread over tree crowns nities [Carpenter et al., 2001; but see Carrillo-Saucedo, and infest >80% of regenerating trees (Kuzee & Gavito & Siddique (2018)]. Nevertheless, there are very few Bongers, 2005; Lawrence, 2005b; Jakovac et al., 2015), reduc- studies relating soil microbiota to succession (eight studies; ing tree growth (Schnitzer & Bongers, 2002; Lai et al., 2017; Fig. 2E, Table S1), which together with high spatial and sea- Estrada-Villegas et al., 2020), and contributing to slower sonal heterogeneity (Lakshmipathy et al., 2012; Cai overall forest regrowth (Paul & Yavitt, 2011). Studies on et al., 2018; Zhou et al., 2018) may hinder generalizable management of secondary forests show that removing Biological Reviews 96 (2021) 1114–1134 © 2021 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society. 1124 Catarina C. Jakovac et al. climbers significantly increases tree growth (Villegas et al., 2014b). Herbivory was shown to cause more damage et al., 2009; César et al., 2016). to the plant community at earlier than later stages of succes- Invasive species can spread easily and densely across agri- sion (Silva et al., 2009; Villa-Galaviz, Boege & del-Val, 2012; cultural landscapes, competing for space, light and nutrients Hahn et al., 2016), because of the higher digestibility of leaves with native species and potentially reducing their establish- from pioneer than late successional species (Poorter ment success and performance (Colón & Lugo, 2006; et al., 2004), and the greater impact of herbivory on the per- Catterall, 2016; Palomeque et al., 2017). For instance, formance of seedlings than adult trees (Massad et al., 2013; Leucaena leucocephala is a pan-tropical invasive tree native to Hahn et al., 2016). In the Neotropics, leaf-cutting ants from central America, in which high resistance to fire, rapid the genus Atta, for example, prefer regenerating tree seed- growth rates and high continuous production of seeds allow lings over pasture grasses and can remove 8–15% of avail- it to outcompete native successional species in tropical rain able leaf area, significantly reducing seedling survival of and dry forests (Erickson, Davidson & Keller, 2002; Colón & certain species (e.g. nutrient-rich leaves) (Nepstad Lugo, 2006; Wolfe & van Bloem, 2012). Other invasive spe- et al., 1996; I.R. Leal, Wirth & Tabarelli, 2014a). The role cies are known to hinder succession and affect species compo- of herbivory in seedling survival, however, will depend on sition, such as the grass Imperata spp. (Styger et al., 2007), the plant investment in protection, which in some species may shrub Chromolaena odorata in Africa (Robiglio & Sinclair, 2011; increase with physiological stress (Leal, Andersen & Norgrove & Hauser, 2015), the fern Pteridium spp. in the Neo- Leal, 2015), infestation by arbuscular mycorrhiza (Bachelot tropics (e.g. Silva & Matos, 2006; Schneider & et al., 2018) and exposure to fire (Massad et al., 2013). Fernando, 2010; Suazo-Ortuño et al., 2015; Palomeque In pastures, grazing reduces the density of seedlings et al., 2017) and exotic pasture grasses across the tropics (Marinho et al., 2016) and favours the persistence of unpalat- (e.g. Guariguata et al., 1995; Holl et al., 2000; Hooper able species (Griscom, Griscom & Ashton, 2009). A model- et al., 2004; Palomeque et al., 2017). Differential density and ling exercise indicated that grazing and fire had synergistic species composition of competitors may, therefore, contrib- effects causing greater reduction in regrowth when combined ute to the divergence of successional pathways. than the sum of their individual effects, and consequently yielding large variation depending on the intensity, fre- quency and extent of fire (Cantarello et al., 2011). It is (d) Facilitation by remnant trees expected, therefore, that interactions between land-use his- Besides attracting dispersers and enhancing species availabil- tory and herbivory will affect species performance and estab- ity (see Section IV.3a), remnant trees also affect species per- lishment during early colonization, altering species density, formance during succession in abandoned fields. Remnant diversity and composition of successional plant communities. trees shade out pasture grasses, reduce temperatures, increase humidity and improve soil nutrient availability under their crowns, consequently favouring seedling estab- lishment and performance (Vieira et al., 1994; Guariguata V. DISCUSSION et al., 1995; Hooper et al., 2004), particularly in tropical dry forests (Guevara et al., 2004; Griscom & Ashton, 2011; (1) Land-use effects on ecosystem functioning Mwampamba & Schwartz, 2011; Williams-Linera et al., 2011). The density of remnant trees is usually reduced The reviewed studies show that land-use history defines suc- with intensive land use, such as in mechanized agriculture cessional pathways through impacts on multiple processes (Chazdon, 2014). Therefore, through its effects on seed rain that define species availability to succession, species perfor- (Section IV.3a) and on species performance, the density mance and local environmental conditions. Studies also show and composition of remnant trees may affect the density that the impacts of previous land-use history on regrowth can and species composition of the regenerating community at last for decades after land use has ceased (e.g. Zimmerman the onset of succession. et al., 1995; Mesquita et al., 2015; Hogan et al., 2016; Estrada-Villegas et al., 2020). The integration of knowledge provided in this review suggests that land-use history alters (e) Herbivory ecosystem functioning and favours feedbacks that sustain Herbivory is an important interaction structuring plant com- alternative successional pathways for decades (Fig. 1, arrows munities in tropical forests (Coley & Barone, 1996). Agricul- 5 and 6). Initial site conditions left after land use define the tural fields and early successional communities harbour early successional communities that interact with the trans- higher abundances of herbivores compared to natural forests formed surrounding landscape to define environmental con- (Silva et al., 2009; Massad et al., 2013; Hahn, Orrock & ditions and species turnover over time. Wardle, 2016), probably due to high resource availability This review showed that land-use history strongly deter- provided by the nutritious and/or palatable leaves of crops mines the assembly of early dominant species (e.g. Styger and pioneer species (Poorter et al., 2004), facilitated host- et al., 2007; Martínez-Ramos et al., 2016; Estrada-Villegas searching in the simplified ecosystem, and high availability et al., 2020), possibly affecting ecosystem functioning during of suitable nesting sites (Silva et al., 2009; L.C. Leal succession (Fig. 1). The identity and functional characteristics Biological Reviews 96 (2021) 1114–1134 © 2021 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society. Land-use effects on secondary succession 1125 of these dominant species strongly drive ecosystem function- throughout succession (Gei et al., 2018; Poorter et al., 2019). ing (Lohbeck et al., 2016; Mora et al., 2017), microclimatic For instance, dry forests might be more resilient to manage- conditions in the understorey (Kabakoff & Chazdon, 1996; ment practices such as cutting and burning as most species Lebrija-Trejos et al., 2011), and biotic interactions are able to resprout repeatedly compared with only a few (Bobrowiec & Gribel, 2010; van Breugel et al., 2011). Case species with these traits in rainforests (Kauffman, 1991; studies showed that species dominating after intensive land- Bond & Midgley, 2001). On the other hand, dry forests might use history hold traits such as long-lived leaves with low nutri- be less resilient to bulldozing and ploughing, given their ent content (Uhl, 1987; Gomes & Luiz~ao, 2012), differential higher dependency on local legacies (sprouts) than on dis- crown architecture (Vester & Cleef, 1998), tick barks persal from surrounding sources (Griscom & Ashton, 2011; (Sanchez-Tapia et al., 2020), high wood density (Fernandes Pulla et al., 2015). Understanding of successional differences Neto et al., 2019) and high sprouting ability (e.g. Uhl across forest types is recent and deserves additional attention et al., 1981; Dalle & de Blois, 2006; Williams-Linera in future studies. et al., 2011). Traits like wood density and sprouting ability Hence, advancing our knowledge of succession in human- trade off with regrowth rates (Bond & Midgley, 2001; modified landscapes requires a multidimensional approach Lohbeck et al., 2015; Pinho et al., 2018). As a consequence, that depicts ecosystem functioning in alternative successional these communities might show slow nutrient cycling pathways in multiple forest types. Additionally, we invite (Erickson et al., 2002; Gomes & Luiz~ao, 2012), as well as slow future research to evaluate the impacts of manipulating early rates of change in vegetation structure, diversity and environ- successional communities on recovery rates (e.g. Brown & mental conditions (Section IV.2). These successional com- Ewel, 1987; Palomeque et al., 2017). Such knowledge will munities and the associated environmental conditions be needed to support the definition of management alterna- interact with the surrounding landscape to define species tives to enhance natural regeneration in forest restoration turnover (Fig. 1, arrow 6): a crucial element for successional programs. progress (Finegan, 1996; Chazdon, 2014). Therefore, cas- cading effects resulting from initial site conditions and land- scape context lead to feedbacks that help sustain divergent (2) Implications for forest restoration based on communities over decades (Fig. 1, arrow 5). natural regeneration The consequences of land-use history for ecosystem func- In this review we provide an integrated understanding of the tioning, however, might differ between rain and dry forests mechanisms driving succession (Fig. 1) and defining alterna- because of intrinsic differences in community assembly tive successional pathways. Here, we apply this (A) Limitations to succession (B) Restoration strategies 1 2 1 2 NR ANR: Landscape integrity ↑ Species availability ↑ Species availability Landscape integrity soil amendment, ↑ Species performance ↓ Species performance perching 3 4 3 4 ANR: TP ↓ Species availability ↓ Species availability enrichment planting + + landscape restoration ↑ Species performance ↓ Species performance landscape restoration Intensity of previous land use Intensity of previous land use Fig 3. The interaction between landscape integrity and previous land-use history defines the limitations to succession (A), and restoration requirements (B). Here landscape integrity represents the amount and quality of sources of propagules, meaning that higher landscape integrity involves higher forest cover, lower forest fragmentation and higher tree cover in agricultural fields. The axis of intensity of previous land use summarizes an increase in the spatial extent, frequency, duration and intensity of management practices. (A) Species availability for succession is strongly reduced by reduction in landscape integrity as well as by intensive, extensive and long-term land use. Limitations to species performance increases with land-use intensity due to reduced resource availability and increased competition with invaders, for example. As a response to these driving factors, succession follows different pathways with varying rates of biomass regrowth and species turnover. (B) Along the gradients of landscape integrity and intensity of previous land use within and across human-modified landscapes, different restoration strategies will be required: unassisted natural regeneration (NR), assisted natural regeneration (ANR) or tree planting (TP). In each quadrant we provide examples of management practices that can help to overcome the limitations to succession (A) for effective restoration of ecosystem functions. Biological Reviews 96 (2021) 1114–1134 © 2021 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society. 1126 Catarina C. Jakovac et al. understanding to identify in which contexts natural regener- vegetation structure, diversity and composition is bound to be ation could lead to effective forest restoration and which slow. In this context, speeding up succession would require management practices would be required to foster restora- the restoration of local and landscape conditions. An active res- tion. This review shows that the recovery of multiple eco- toration approach to improve local soil conditions and intro- logical attributes, i.e. the potential for natural duce species diversity (e.g. tree planting) will be required to regeneration to take place and to restore ecosystems, is con- kick-start successional processes. Additionally, improving land- text dependent and is a product of interactions between scape integrity will guarantee higher and more diverse seed local and landscape conditions (Fig. 3). Secondary succes- dispersal and therefore higher restoration success (Martínez- sion will proceed at higher rates where limitations to spe- Garza & Howe, 2003; Crouzeilles et al., 2019). A landscape cies availability, establishment and performance are lower restoration approach, therefore, is needed especially where (Fig. 3). The few studies evaluating interactions between landscape integrity is low (Fig. 3B, quadrants 3 and 4). local and landscape factors suggest that dispersal limitation It is important to note that spatial auto-correlations between is a stronger driver of species richness and turnover while local and landscape factors often result in synergistic effects. local-level filtering effects mainly drive regrowth rate and Distance to the forest is often positively correlated with the species composition (Table S1; e.g. Martínez-Garza & intensity, frequency and duration of previous land use (see Howe, 2003; Robiglio & Sinclair, 2011; Jakovac Section IV.1). As a consequence, landscapes with higher integ- et al., 2016a). With an increasing amount of forest in the rity and locations closer to the forest edge promote higher nat- landscape (landscape integrity), there is lower dispersal lim- ural regeneration (Goosem et al., 2016), higher predictability of itation and therefore higher species availability for natu- rally regenerating forests. With increasing intensity of previous land use, availability of species is narrowed down Table 1. Main descriptors of land-use history influencing by filtering effects mediated by management practices, and succession following agriculture or pasture land use, and species performance is reduced by limited soil nutrients examples of how to quantify them. One or more metrics can be and competition with invasive species (Fig. 3A). The limita- used to describe previous land use; the choice of which metric to tions to succession imposed by local and landscape condi- use being dependent on research question and data availability tions can guide decisions on how to manage natural regeneration for effective forest restoration. Descriptors of previous Unassisted natural regeneration will be an optimal resto- Metrics land-use history ration strategy in contexts of high landscape integrity and Type Pasture, shifting cultivation, low intensity of previous land use (Fig. 3B, quadrant 1). In conventional agriculture, other contexts, assisted natural regeneration or tree planting agroforestry, etc. are likely the way forward (Shono, Cadaweng & Durst, 2007; Crop(s) species/pasture grass species/ Chazdon et al., 2020). Natural regeneration can be assisted livestock species by management practices appropriate to each context Intensity Number of slash and/or burning events (Fig. 3B, quadrants 2 and 3). Where seed sources are abun- Livestock density dant but local conditions are deteriorated (Fig. 3B, quadrant Use of machinery, pesticides or herbicides 2), practices to amend soil conditions (Allen, Allen & Gómez- Length of the fallow period Pompa, 2005), enhance seed rain (Zanini & Ganade, 2005; Weeding practice (clear or selective Toh, Gillespie & Lamb, 1999) and/or stimulate seed germi- weeding) nation (Dupuy & Chazdon, 2008) will be needed to assist nat- Weeding frequency ural regeneration (Fig. 3B, quadrant 2). Presence of remnant trees (% cover or Where seed sources are scarce but local conditions are not density) Indices combining frequency and deeply transformed (Fig. 3B, quadrant 3), enrichment planting duration (Lascurain-Rangel et al., 2019) could effectively enhance species Frequency Burning events frequency diversity. Additional management practices might be required Slash-and-burn frequency depending on specific biophysical conditions and on the resto- Land cleaning/ploughing frequency ration goal (Holl et al., 2000; Chazdon et al., 2020). Recovery Cropping frequency rates and species turnover can be fostered through the selective Duration Amount of time since old-growth forest removal of invasive species (Uebel, Wilson & Shoo, 2017; Palo- clear cut Amount of time in continuous use meque et al., 2017) and lianas (César et al., 2016; Palomeque (e.g. as agriculture or pasture) et al., 2017) and through silvicultural treatments (Swinfield Average length of the cropping period et al., 2016; dos Santos & Ferreira, 2020). When economic over the period of land use returns are desired, possible management practices include Length of the last cropping phase planting or favouring the regeneration of commercial species previous to abandonment (Fantini et al., 2019; Forero-Montaña et al., 2019). Spatial extent Size of the agricultural field or In the situation where seed sources are scarce and local con- pastureland Size of the agricultural mosaic ditions are deteriorated (Fig. 3B, quadrant 4), recovery of Biological Reviews 96 (2021) 1114–1134 © 2021 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society. Land-use effects on secondary succession 1127 succession (Arroyo-Rodríguez et al., 2017) and higher restora- conditions and species availability and performance tion success (Crouzeilles et al., 2017, 2020b). Therefore, the may lead to differential ecosystem functioning. It amount of surrounding forest and proximity to forest fragments remains unclear, however, how the early-successional could be easy-to-assess proxies for the potential of natural assemblages favoured by previous land use foster or regeneration in human-modified landscapes (see Crouzeilles hold back further successional processes. The func- et al., 2019, 2020a). Further studies are needed to identify the tional characteristics and biotic interactions of species main proxies better for the potential for natural regeneration that thrive after different land-use histories should be across regions. a research priority to advance knowledge on the Finally, the success of restoration initiatives based on natu- impacts of land use on ecosystem functioning and to ral regeneration will also depend on the restoration goals and assist the design of management practices that enhance on socio-economic aspects that govern the decision to allow natural regeneration in forest restoration programs. regrowth to proceed (Section III). Environmental policies (5) Our knowledge on succession after land use is strongly play an important role in determining the fate of regrowth biased towards Neotropical wet forests, and low- to and in constraining management practices (see Guariguata & mid-intensity land-use history. More studies on Brancalion, 2014; Chazdon et al., 2020). Therefore, natural degraded landscapes, on dry forests and covering the regeneration can be an effective strategy to restore forest Paleotropics must be pursued to identify idiosyncrasies landscapes where there are lower limitations to succession and generalities of tropical forest succession and to help (Fig. 3) and under appropriate governance systems. define restoration strategies suited to local conditions. (6) Moving forward in the mechanistic understanding of succession in human-modified landscapes requires the assessment of land-use history (Table 1), long-term VI. CONCLUSIONS monitoring of successional patches, and careful exper- imental design to control for correlations between local (1) In human-modified landscapes, successional pathways and landscape factors. Special attention to variations are largely defined by land-use history. Although ran- in these factors is required when selecting secondary dom processes contribute to define successional assem- forest patches in chronosequence studies. The mecha- blages, land use imposes constraints on species nistic framework proposed here on how land use drives availability and performance during regrowth. This successional pathways will help update successional review highlights that the most important underlying theory to the current context of extensive anthropo- processes include dispersal limitation, ecological filter- genic influence and will support restoration science to ing, competition, facilitation, herbivory and tolerance identify key pathways to manage natural regeneration. to disturbance and environmental conditions. (7) Finally, based on the knowledge summarized herein, we (2) The impact of previous land-use history on regrowth describe the potential for natural regeneration in differ- will depend on variations in the intensity, frequency, ent contexts of previous land-use history and landscape duration, extent and type of previous land use. Here integrity (Fig. 3). Natural regeneration will be more suc- we provide examples of how specific land-use practices cessful where there are lower barriers to succession. In in agricultural and pastoral fields constrain the avail- other situations, assisted natural regeneration, tree plant- ability of species and lead to differential species perfor- ing and landscape restoration are required. mance. Slight variations in land-use history can lead to different successional pathways within a landscape. Hence, descriptors of land-use history (Table 1) and landscape configuration and composition must be VII ACKNOWLEDGEMENTS accessed in studies evaluating drivers of successional communities and predicting the potential for natural The authors thank the reviewers of previous versions of this regeneration. manuscript. This study was supported by funding from (3) Within the set of species available to succession, a nar- Cnpq-SinBiose 442371/2019-5 (Br) to R.C.G.M. and rower set will be able to overcome competition for C.C.J., PANTROP/ERC.834775 (NL) to C.C.J., NWO- light, nutrients and space with weeds, lianas and inva- NEWFOR.17418 (NL-Br) to F.B. and M.P.-C., NFP- sive species and to establish and grow successfully. PhD.11/ 606 (NL) to C.C.J., and INREF-FOREFRONT More experimental studies are needed to understand (WUR) to F.B., and FP7-771056-LICCI (ABJ). how biotic interactions lead to differential species per- formance and drive community assembly. 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(Received 15 April 2020; revised 3 February 2021; accepted 4 February 2021; published online 12 March 2021) Biological Reviews 96 (2021) 1114–1134 © 2021 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society.