Opinion
Uniting niche differentiation and dispersal limitation predicts tropical forest succession

https://doi.org/10.1016/j.tree.2021.04.001Get rights and content

Highlights

  • Current theories of tropical forest succession have focused on niche differentiation among plants but have not adequately addressed how dispersal limitation shapes succession.

  • We describe dispersal limitation in terms of seed source and disperser limitation; these two factors determine the production of seeds throughout succession and the arrival of seeds to suitable recruitment sites.

  • We present a framework to better understand how seed sources interact with animal abundance, behavior, and diet preferences across the landscape to determine seed movement and deposition during forest regeneration.

  • Using technological advances in animal tracking and molecular tools, the proposed framework will improve models of tropical forest succession beyond niche differentiation.

Tropical secondary forests are increasingly important for carbon sequestration and biodiversity conservation worldwide; yet, we still cannot accurately predict community turnover during secondary succession. We propose that integrating niche differentiation and dispersal limitation will generate an improved theoretical explanation of tropical forest succession. The interaction between seed sources and dispersers regulates seed movement throughout succession, and recent technological advances in animal tracking and molecular analyses enable us to accurately monitor seed movement as never before. We propose a framework to bridge the gap between niche differentiation and dispersal limitation. The Source-Disperser Limitation Framework (SDLF) provides a way to better predict secondary tropical forest succession across gradients of landscape disturbance by integrating seed sources and frugivore behavior.

Section snippets

Classic theories of succession do not incorporate seed dispersers

In tropical forests, where 65–95% of tree species depend on animals for seed dispersal [1,2], the assembly of plant and animal communities is intrinsically linked during the first decades of succession [3]. However, classical theories of tropical succession are founded in temperate ecology and focus on plant community assembly while neglecting biotic drivers that modulate species turnover (e.g., seed dispersal) [4., 5., 6.]. Contemporary succession theories emphasize plant functional traits and

Uniting niche-based models with dispersal limitation

We propose that by combining niche-based models with concepts of dispersal limitation we can provide a better theoretical explanation of tropical forest succession [9]. Niche differentiation explains how plant species exploit shifting resource availability over succession via tradeoffs [5,13]. However, community reassembly may be thwarted at the onset or during succession because seeds are unable to reach a site and establish [9,13,14]. Thus, dispersal limitation may be a stronger determinant

Components of dispersal limitation: seed and dispersal vector

Dispersal limitation can be divided into two core components: the reproductive unit that is dispersed (seed or diaspore) and the vector of dispersal (animal or wind). Typically, seed limitation is assessed as source limitation and dispersal limitation [16,19]. We suggest a nuanced way to address the same phenomena by focusing on ‘source limitation’ and ‘disperser limitation’ because it is the interaction between the seed and the vector that results in the movement and eventual establishment of

Source limitation

Source limitation proposes that insufficient seeds are produced to saturate available recruitment sites [19]. Seed availability in secondary forests is dictated by the abundance, location, and species composition of adult trees in the surrounding landscapes [3]. Seed source limitation is higher in landscapes with lower tree cover, increased distance to old-growth forest, and higher levels of ongoing disturbance [13,14]. Farmed tropical landscapes often retain considerable tree cover; a recent

Disperser limitation

Seed dispersal initiates secondary forest succession in deforested tropical landscapes, with dispersers transporting seeds from sources and depositing them in areas where seed banks are depauperate [33]. Wind, frugivorous bats, and small birds are the key seed dispersers in early succession (Figure 1) because they transport many seeds to regeneration sites [1,24,31]. In degraded landscapes, wind-dispersed species tend to dominate seed rain in pastures and can be important to initiate

Establishment limitation

Seedling establishment may limit forest regeneration if the site is unsuitable for seed germination and early seedling survival [64]. Establishment is dictated by the biotic and abiotic conditions of the microsite and the seed and seedling traits of tree species [19]. For example, we see selection for fast-growing species dispersed into open pastures because they are more likely than slower-growing species to outcompete grasses and shrubs for available light [29,52]. The high light and low

Moving forward using the Source-Disperser Limitation Framework

Given that tropical forest succession hinges on overcoming limitations in seed sources and dispersers, we propose the Source-Disperser Limitation Framework (SDLF) to better understand succession in tropical agricultural landscapes. The central tenet of the SDLF is that the interaction between seed sources and dispersers controls seed movement to sites starting or undergoing regeneration (Figure 2A). Seed movement from sources to microsites by dispersers is the primary limitation, since seedling

Concluding remarks

The unification of niche differentiation and dispersal limitation can provide a mechanistic explanation of succession in the tropics. The study of seed dispersal has a long history in the context of tropical secondary forests [1,2,16,29,31]; here we are proposing an integration of seed dispersal limitation with niche differentiation to better predict tropical forest succession. Specifically, we need a mechanistic approach to understand what limits seed arrival (seed sources and dispersers) and

Acknowledgments

We thank Luke Browne, Liza Comita, Meg Crofoot, Dina Dechmann, Ana Cristina Palma, and Pablo Stevenson for comments on earlier drafts of this article. We also thank three anonymous reviewers and Andrea Stephens; their comments helped us improve the ideas proposed in this opinion article. D.D. was supported by a Resesearch Fellowship from the Alexander von Humboldt Foundation, Germany.

Declaration of interests

The authors have no interests to declare.

Glossary

Disperser limitation
insufficient numbers or types of dispersers that preclude the arrival of seeds at recruitment sites. Disperser limitation can also occur due to changes in behavior (e.g., animals actively avoid areas with low forest cover).
Endozoochory
seed dispersal via ingestion by vertebrate animals.
Extirpations
local extinctions of dispersers, potentially due to predation, hunting, or habitat loss, among other factors.
Metabarcoding
using short sequences of DNA from specified genes of

References (79)

  • M. Quesada

    Succession and management of tropical dry forests in the Americas: review and new perspectives

    For. Ecol. Manag.

    (2009)
  • H.C. Muller-Landau et al.

    Seed dispersal of woody plants in tropical forests: concepts, examples and future directions

  • H.F. Howe et al.

    Ecology of seed dispersal

    Annu. Rev. Ecol. Syst.

    (1982)
  • V. Arroyo-Rodríguez

    Multiple successional pathways in human-modified tropical landscapes: new insights from forest succession, forest fragmentation and landscape ecology research

    Biol. Rev. Camb. Philos. Soc.

    (2017)
  • F.E. Clements

    Plant Succession: An Analysis of the Development of Vegetation

    (1916)
  • D. Tilman

    Constraints and tradeoffs: toward a predictive theory of competition and succession

    Oikos

    (1990)
  • F.A. Bazzaz et al.

    Physiological ecology of tropical succession: a comparative review

    Annu. Rev. Ecol. Syst.

    (1980)
  • N. Rüger

    Demographic trade-offs predict tropical forest dynamics

    Science

    (2020)
  • M. Vellend

    The Theory of Ecological Communities

    (2016)
  • Food and Agriculture Organization. of the United Nations (FAO)

    Global Forest Resources Assessment 2015: How Are the World’s Forests Changing?

    (2015)
  • L. Parry

    Large-vertebrate assemblages of primary and secondary forests in the Brazilian Amazon

    J. Trop. Ecol.

    (2007)
  • A.C. Palma

    Dispersal and recruitment limitations in secondary forests

    J. Veg. Sci.

    (2021)
  • R.L. Chazdon

    Second Growth: The Promise of Tropical Forest Regeneration in an Age of Deforestation

    (2014)
  • L.K. Werden

    Effects of dispersal- and niche-based factors on tree recruitment in tropical wet forest restoration

    Ecol. Appl.

    (2020)
  • D.H. Dent

    Secondary forests of central Panama increase in similarity to old-growth forest over time in shade tolerance but not species composition

    J. Veg. Sci.

    (2013)
  • E.W. Schupp

    Intrinsic and extrinsic drivers of intraspecific variation in seed dispersal are diverse and pervasive

    AoB Plants

    (2019)
  • H.S. Rogers

    The total dispersal kernel: a review and future directions

    AoB Plants

    (2019)
  • R. Zwolak

    How intraspecific variation in seed-dispersing animals matters for plants

    Biol. Rev. Camb. Philos. Soc.

    (2018)
  • C.J. Clark

    Are plant populations seed limited? A critique and meta-analysis of seed addition experiments

    Am. Nat.

    (2007)
  • R.J. Zomer

    Global tree cover and biomass carbon on agricultural land: the contribution of agroforestry to global and national carbon budgets

    Sci. Rep.

    (2016)
  • C.D. Mendenhall

    Quantifying and sustaining biodiversity in tropical agricultural landscapes

    Proc. Natl. Acad. Sci. U. S. A.

    (2016)
  • J. Ghazoul

    Pollen and seed dispersal among dispersed plants

    Biol. Rev. Camb. Philos. Soc.

    (2005)
  • J. Zambrano et al.

    Forest fragmentation alters the population dynamics of a late-successional tropical tree

    Biotropica

    (2014)
  • N.R. Ingle

    Seed dispersal by wind, birds, and bats between Philippine montane rainforest and successional vegetation

    Oecologia

    (2003)
  • A. Cubiña et al.

    The effect of distance from forest edge on seed rain and soil seed bank in a tropical pasture

    Biotropica

    (2001)
  • R. Crouzeilles et al.

    Which landscape size best predicts the influence of forest cover on restoration success? A global meta-analysis on the scale of effect

    J. Appl. Ecol.

    (2016)
  • B.C. Tarbox

    Divergent rates of change between tree cover types in a tropical pastoral region

    Landsc. Ecol.

    (2018)
  • K.D. Holl

    Factors limiting tropical rain forest regeneration in abandoned pasture: seed rain, seed germination, microclimate, and soil

    Biotropica

    (1999)
  • D. Piotto

    Successional, spatial, and seasonal changes in seed rain in the Atlantic forest of southern Bahia, Brazil

    PLoS One

    (2019)

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