Climate niche mismatch and the collapse of primate seed dispersal services in the Amazon
Graphical abstract
Introduction
Climate is changing at accelerated rates, threatening not only biodiversity but the ecosystem services that species are involved with. The magnitude of observed and forecasted changes is comparable to the most expressive global transformations in the past 65 million years (Diffenbaugh and Field, 2013; Kemp et al., 2015). As novel climates arise, species will either be extinct, adapt, or migrate towards newly suitable environments (Urban, 2015). Species ranges move once populations at leading edges colonize environments as they become suitable, while those at the rear edge fail to persist (Hampe, 2011). However, colonization of suitable environment depends on species dispersal abilities (Schloss et al., 2012) and the existence of permeable dispersal routes across landscapes (Lawler et al., 2013). Yet, many of these passageways have already or are projected to be disrupted by land use change (Sales et al., 2019). The relocation of species ranges can form novel biotic communities, allowing new interactions to arise (Post, 2013), but disrupting key relationships among species (Thomas and Ohlemüller, 2010).
Seed dispersal is an essential animal-plant interaction, especially in the Neotropics, where at least 75% of plants disperse their seeds via frugivore consumption (Howe and Smallwood, 1982). Frugivore-based seed dispersal is a dynamic interaction between plants and animals, usually with benefits for both groups: plants get their offspring dispersed, often increasing seedling establishment and viability, while animals obtain food (Chapman, 1995; Howe and Smallwood, 1982; Jordano, 2000). Climate-induced changes in the distribution and abundance of animal seed-dispersers may reduce the seed dispersal services they provide (Mokany et al., 2014) and are likely to weaken existing mutualisms involving plants (Tylianakis et al., 2008). In addition, plants are sessile organisms, for which seed dispersal may be the only mechanism to track their suitable habitats on changing climates (Hampe, 2011). In this way, niche tracking via animal-mediated dispersal may be necessary for plants to colonize novel suitable environments otherwise inaccessible (González-Varo et al., 2017).
Primates are remarkable seed dispersers, comprising up to 40% of frugivore biomass in tropical forests (Chapman, 1995). Primate seed dispersal affects plant population genetics, demography and community assembly in forested ecosystems (Andresen et al., 2018). In the Amazon, for example, defaunation of large-bodied primates reduces tree species richness by 55% (Nuñez-Iturri and Howe, 2007), due to a dispersal vacuum in the seedling recruitment of primate-dispersed trees (Levi and Peres, 2013). Yet, primates are especially vulnerable to climate change for inhabiting environmental conditions close to the upper thermal physiological limits (Dillon et al., 2010; Huey et al., 2012). Adaptive evolution towards warmer climates does not happen often among lineages (Araújo et al., 2013), so that small temperature increases can pose deleterious stress on primate populations (Clee et al., 2015). Furthermore, the Neotropical platyrrhine primates are mostly dependent on closed-canopy forests to feed, reproduce and to move (Mittermeier et al., 2013), so their ability to disperse across open habitat is limited (Schloss et al., 2012), reducing their potential to track suitable habitats in fragmented and human-dominated landscapes (Sales et al., 2019).
In this work, we project the synergistic effects of climate change, deforestation and dispersal limitation on the seed-dispersal services provided by Amazon primates. To do so, we combined ecological niche models with dispersal simulations accounting for natural and anthropogenic geographical barriers that might constrain primate movement. Then, we assessed the magnitude of changes in the potential amount of seeds dispersed by primates. We consider forecasts of shifts on distribution and co-occurrence between a plant and its frugivore primate community, in addition to values of potential per-capita seed dispersal (from Levi and Peres, 2013). This integrative approach rendered conservative but alarming projections showing that the ecosystem function of seed dispersal is threatened by disruption of biotic interactions, due to climate change and deforestation.
Section snippets
Seed dispersal quantification
To calculate the magnitude of the effect of climate change and deforestation on the seed dispersal services provided by Amazon primates, we build upon a previous work, using a unique study system for which daily per-capita seed dispersal data is available (from Levi and Peres, 2013). The seed dispersal system, formed by the fleshy-fruited Sapotaceae tree Manilkara bidentata [hereafter referred to solely as Manilkara] and a frugivore community of sympatric primates, was extensively studied in a
Co-occurrence and niche mismatch
Using data on the daily amount of seeds dispersed per km2 by each primate from a frugivore community, plus their projected co-occurrence with the fleshy-fruited plant Manilkara bidentata, we estimated the potential amount of seeds that could be dispersed by each primate across the plant range (Table 1, Supporting Tables S1 and S2). The tufted capuchin, Sapajus apella, exhibited the largest potential range overlap with Manilkara, sharing a suitable area close to 5 × 105 km2, closely followed by
Discussion
By forecasting species distributional shifts of a uniquely well-studied seed dispersal system, we estimate the magnitude of the change in a key ecosystem function mediated by an animal-plant interaction. Seed dispersal via frugivore consumption is essential for ecosystem resilience, especially in the Tropics, where most trees rely on plant-animal interactions for dispersing their seeds (Howe and Smallwood, 1982). We found that the redistribution of Amazon primates, due to the synergism among
Author contributions
LS and MP conceived and designed this study; LS performed ecological niche modelling and seed dispersal analysis; LS, LC and MP drafted the manuscript. All authors provided input, approved the final version of this manuscript and agree to be accountable for all aspects of the work.
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001. LS is funded by the PNPD (Programa Nacional de Pós-Doutorado, in Portuguese) at the University of Campinas. MMP is funded by CAPES. LC is supported by a Young Investigator grant from FAPESP (#2014/14739-0).
References (74)
- et al.
The crucial role of the accessible area in ecological niche modeling and species distribution modeling
Ecol. Model.
(2011) Plants on the move: the role of seed dispersal and initial population establishment for climate-driven range expansions
Acta Oecol.
(2011)- et al.
Dispersal vacuum in the seedling recruitment of a primate-dispersed Amazonian tree
Biol. Conserv.
(2013) - et al.
Downsized mutualisms: consequences of seed dispersers’ body-size reduction for early plant recruitment
Perspect. Plant Ecol. Evol. Syst.
(2015) - et al.
Large vertebrates as the missing components of seed-dispersal networks
Biol. Conserv.
(2013) Summary for policymakers
R: A Language and Environment for Statistical Computing
(2019)- et al.
spThin: an R package for spatial thinning of species occurrence records for use in ecological niche models
Ecography (Cop.)
(2015) A new look at the statistical model identification
IEEE Trans. Automat. Contr.
(1974)- et al.
Primate seed dispersal: old and new challenges
Int. J. Primatol.
(2018)
Heat freezes niche evolution
Ecol. Lett.
Standards for distribution models in biodiversity assessments
Sci. Adv.
Why is a landscape perspective important in studies of primates?
Am. J. Primatol.
Assessing habitat fragmentation effects on primates: the importance of evaluating questions at the correct scale
Selecting pseudo-absences for species distribution models: how, where and how many?
Methods Ecol. Evol.
Impacts of climate change on the future of biodiversity
Ecol. Lett.
Major shifts in Amazon wildlife populations from recent intensification of floods and drought
Conserv. Biol.
Primate seed dispersal: coevolution and conservation implications
Evol. Anthropol. Issues, News, Rev.
Chimpanzee population structure in Cameroon and Nigeria is associated with habitat variation that may be lost under climate change
BMC Evol. Biol.
Changes in ecologically critical terrestrial climate conditions
Science
Global metabolic impacts of recent climate warming
Nature
Defaunation in the Anthropocene
Science (80-. )
A statistical explanation of MaxEnt for ecologists
Divers. Distrib.
Defaunation precipitates the extinction of evolutionarily distinct interactions in the Anthropocene
Sci. Adv.
The MIGCLIM R package - seamless integration of dispersal constraints into projections of species distribution models
Ecography (Cop.).
Amazon fires clearly linked to deforestation, scientists say
Science (80-. )
Impending Extinction Crisis of the World’s Primates: Why Primates Matter
Anthropogenic Range Contractions Bias Species Climate Change Forecasts
Declining body size: a third universal response to warming?
Trends Ecol. Evol.
Seed dispersers help plants to escape global warming
Oikos
Climate and land use changes will degrade the configuration of the landscape for titi monkeys in eastern Brazil
Glob. Chang. Biol.
The influence of spatial errors in species occurrence data used in distribution models
J. Appl. Ecol.
Emissions – the ‘business as usual’ story is misleading
Nature
Very high resolution interpolated climate surfaces for global land areas
Int. J. Climatol.
Ecology of seed dispersal
Annu. Rev. Ecol. Syst.
Predicting organismal vulnerability to climate warming: roles of behaviour, physiology and adaptation
Philos. Trans. R. Soc. B Biol. Sci.
Climate change 2014: impacts, adaptation, and vulnerability. Part A: global and sectoral aspects
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