Phylogenetic dimension of tree communities reveals

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Phylogenetic dimension of tree communities reveals high conservation value of .... share particular physiological, ecological and life-history traits (Arroyo-Rodríguez, Pineda, .... three sites within the Montes Azules Biosphere Reserve, and 26 forest ...... Graham, C.H., & Fine, P.V.A. (2008) Phylogenetic beta diversity: Linking ...
1 Diversity and Distributions (in press) Phylogenetic dimension of tree communities reveals high conservation value of disturbed tropical rainforests Edgar E. Santo-Silva1, 2,*, Bráulio A. Santos3, Víctor Arroyo-Rodríguez4, Felipe P. L. Melo1, Deborah Faria5, Eliana Cazetta5, Eduardo Mariano-Neto6, Manuel A. Hernández-Ruedas4, Marcelo Tabarelli1 1

Departamento de Botânica, Universidade Federal de Pernambuco, Recife, Pernambuco 50670-901, Brazil. 2 Unidade Acadêmica de Serra Talhada, Universidade Federal Rural de Pernambuco, Serra Talhada, Pernambuco 56909-535, Brazil. 3 Departamento de Sistemática e Ecologia, Universidade Federal da Paraíba, João Pessoa, Paraíba 58051-900, Brazil. 4 Instituto de Investigaciones en Ecosistemas y Sustentabilidad, Universidad Nacional Autónoma de México, 58190 Morelia, Michoacán, Mexico. 5Laboratório de Ecologia Aplicada à Conservação, Universidade Estadual de Santa Cruz, Ilhéus, Bahia 45662-900, Brazil. 6Departamento de Botânica, Instituto de Biologia, Universidade Federal da Bahia, Salvador, Bahia 40170-290, Brazil. * E-mail:[email protected] ABSTRACT Aim: The conversion of old-growth tropical forests into human-modified landscapes threatens biodiversity worldwide, but its impact on the phylogenetic dimension of remaining communities is still poorly known. Negative and neutral responses of tree phylogenetic diversity to land use change have been reported at local and landscape scales. Here, we hypothesized that such variable responses to disturbance depend on the regional context, being stronger in more degraded rainforest regions with a longer history of land use. Location: Six regions in Mexico and Brazil. Methods: We used a large vegetation database (6923 trees from 686 species) recorded in 98 50-ha landscapes distributed across two Brazilian and four Mexican regions, which exhibit different degrees of disturbance. In each region, we assessed whether phylogenetic alpha and beta diversities were related to landscape-scale forest loss, the percentage of shade-intolerant species (a proxy of local disturbance) and/or the relatedness of decreasing (losers) and increasing (winners) taxa. Results: Contrary to our expectations, the percentage of forest cover and shade-intolerant species were weakly related to phylogenetic alpha and beta diversities in all but one region. Loser species were generally as dispersed across the phylogeny as winner species, allowing more degraded, deforested and species-poorer forests to sustain relatively high levels of evolutionary (phylogenetic) diversity. Main conclusion: Our findings support previous evidence indicating that traits related to high susceptibility to forest disturbances are convergent or have low phylogenetic signal. More importantly, they reveal that the evolutionary value of disturbed forests is (at least in a phylogenetic sense) much greater than previously thought. Keywords: Brazil, evolutionary diversity, habitat fragmentation, Mexico, phylogenetic diversity, phylogenetic structure

2 INTRODUCTION Land use change for agricultural production has led to tropical forest loss worldwide, creating landscapes with lower forest cover composed of small, isolated and degraded forest remnants (Malhi, Gardner, Goldsmith, Silman, & Zelazowski, 2014). Biodiversity is usually threatened by these changes, but a group of native disturbance-adapted species thrive in human-modified tropical landscapes (HMTLs) (Tabarelli, Peres, & Melo, 2012), triggering a timely debate on the ability of HMTLs to retain biodiversity (Arroyo-Rodríguez et al., 2017; Melo, Arroyo-Rodríguez, Fahrig, Martínez-Ramos, & Tabarelli, 2013). Quantifying such ability is amongst the biggest challenges for today’s tropical ecologists, as it requires a multiscale assessment of different dimensions of biological diversity, including the way diversity is distributed across the landscape (Sfair, Arroyo-Rodríguez, Santos, & Tabarelli, 2016). The phylogenetic dimension of species diversity is increasingly being assessed in HMTLs, providing an evolutionary basis for their conservation value (Cavender-Bares, Kozak, Fine, & Kembel, 2009; Moreno et al., 2017; Pausas & Verdú, 2010; Tucker et al., 2017). Yet, the available studies are not conclusive, as negative (Munguía-Rosas et al., 2014; Ribeiro et al., 2016; Santos et al., 2014) and neutral responses (Arroyo-Rodríguez et al., 2012; Matos et al., 2017; Santos, Arroyo-Rodríguez, Moreno, & Tabarelli, 2010) of phylogenetic diversity to anthropogenic disturbances have been reported. Also, most studies focus on local (alpha) changes in phylogenetic diversity, overlooking the patterns of phylogenetic differentiation (beta-diversity) among localities (but see Andrade et al., 2015). Evaluating the beta component of phylogenetic diversity is of key relevance to connect local to regional processes in HMTLs (Graham & Fine, 2008; Moreno et al., 2017; Swenson, 2011; Tucker et al., 2017). Tropical tree communities often respond to human disturbance by losing species that share particular physiological, ecological and life-history traits (Arroyo-Rodríguez, Pineda, Escobar, & Benítez-Malvido, 2009; Laurance, Nascimento, Laurance, Andrade, Ribeiro, et al., 2006; Santos et al., 2008; Santo-Silva, Almeida, Melo, Zickel, & Tabarelli, 2013). Species with high wood density, high shade-tolerance, and particularly those occupying the emergent strata of the forest or requiring specialized biotic agents for pollination and seed dispersal, are known to be more susceptible to forest disturbance (Laurance, Nascimento, Laurance, Andrade, Fearnside, et al., 2006; Lopes, Girão, Santos, Peres, & Tabarelli, 2009; Melo, Martínez-Salas, Benítez-Malvido, & Ceballos, 2010; Michalski, Nishi, & Peres, 2007; Oliveira, Santos, & Tabarelli, 2008; but see Kunstler et al 2016). This trait-based vulnerability to disturbance may favour the co-occurrence of close relatives if vulnerable traits are conserved along the phylogeny, but may also favour the co-occurrence of distant relatives if vulnerable traits are phylogenetically convergent or evenly distributed across the phylogeny. Though scarce, the taxonomic and phylogenetic evidence available so far suggest that vulnerable traits are not conserved (Arroyo-Rodríguez et al., 2012; Lopes et al., 2009; Santos et al., 2010), allowing highly disturbed, species-poor forests to retain similar levels of phylogenetic spread as low disturbed, species-rich forests (but see opposite patterns in tropical dry forests; Munguía-Rosas et al., 2014; Ribeiro et al., 2016). Because species represent multiple traits (vulnerable or not) and multiple trait combinations, linking the phylogenetic distribution of particular vulnerable traits to the overall changes in phylogenetic dimension of tree communities is not straightforward. A more comprehensive approach can be looking at the relatedness of those taxa that are favored by human disturbance and compare it with the relatedness of disfavored taxa (winners and losers, respectively, sensu Tabarelli et al., 2012). If winners are more related than losers, we may expect loss of phylogenetic spread following disturbance. This has been described for the fragmented forests of Central Amazonia, where the phylogenetic impoverishment of tree communities over time was attributed to the gradual replacement of 31 less related tree genera

3 (losers) by a group of 28 more related genera (winners) (Santos et al., 2014). Similarly, plant communities in Costa Rica become more phylogenetically even as succession unfolds owing to the replacement of individuals belonging to closely related early-successional species by late-successional individuals belonging to a wider diversity of lineages (Norden, Letcher, Boukili, Swenson, & Chazdon, 2012). Although landscape-scale forest loss is considered a key driver of biological impoverishment in HMTLs (Fahrig, 2003, 2013), its impact on phylogenetic diversity and structure of communities is still poorly understood, as all studies on the topic have focused on the effect of patch-scale predictors (but see Matos et al., 2017). For example, Munguía-Rosas et al. (2014) compare plant phylogenetic diversity between forest fragments and continuous forest plots and find that it is 19% greater in continuous than in fragmented forests. Santos et al. (2010) report a decrease in tree phylogenetic diversity along forest edges, but this and other studies (Arroyo-Rodríguez et al., 2012; Santos et al., 2014) did not find a significant effect of fragment size on tree phylogenetic diversity and structure. Further studies are therefore needed to assess the effect of landscape forest loss on tree communities, especially because there is evidence that this factor can increase the susceptibility of tree species to local disturbances (Arroyo-Rodríguez et al., 2009, Arroyo-Rodríguez, Rös, et al., 2013). Also, comparing the response of tree communities to forest loss across regions with different disturbance regime and land use history is urgently needed, as such response may depend on (i) the level of disturbance regime at the regional scale (see the “fragmentation threshold hypothesis”; Villard & Metzger, 2014), and (ii) on the amount of time the remaining communities have been exposed to disturbance, especially when considering long-lived organisms such as trees (Metzger et al., 2009). Here we analysed tree communities in 98 50-ha landscapes distributed across six fragmented rainforest regions with different disturbance regime and land use history from Mexico and Brazil. We tested the hypothesis that the impact of landscape-scale forest loss and local disturbance on tree evolutionary diversity is more evident in regions with a higher disturbance degree and a longer history of land use. In each region we assessed patterns of within-landscape (alpha) and between-landscape (beta) phylogenetic diversities. If the taxa that are favored by disturbance are more phylogenetically related than those that are disadvantaged, we expect a loss of phylogenetic alpha diversity with increasing landscape forest loss and local disturbance. Under this scenario, phylogenetic beta diversity should rise with the increasing differences in forest cover and local disturbance between landscapes, particularly between those immersed in highly disturbed regions with older land use history (see the “landscape divergence hypothesis”; Arroyo-Rodríguez, Rös, et al., 2013; Laurance et al., 2007), within which dispersal limitation would be higher (Arroyo-Rodríguez, Rös, et al., 2013; Socolar, Gilroy, Kunin, & Edwards, 2016). Nonetheless, if losers are as phylogenetically diverse as winners, we would expect a weak effect of local and landscape disturbances on phylogenetic alpha and beta diversities.

METHODS Study regions We assessed six Neotropical rainforest regions, four from Mexico (Los Tuxtlas and Lacandona) and two from Brazil (Serra Grande and Una), which exhibit different degrees of disturbance (Table 1). Within the Los Tuxtlas region, we studied three subregions (hereafter regions) with different deforestation levels (LDL = low deforestation level, 24% of remaining forest cover; IDL = intermediate deforestation level, 11%; HDL = high deforestation level,

4 4%). We made this distinction because previous taxonomic assessments have demonstrated striking differences among the subregions, which also showed notable differences in land use history (Table 1). We have studied each of the six regions for almost a decade (Los Tuxtlas: Arroyo-Rodríguez et al., 2009, 2012; Arroyo-Rodríguez, Rös, et al. 2013; Lacandona: Hernández-Ruedas et al., 2014; Serra Grande: Santos et al., 2008; Una: Pardini et al., 2009). Based on our personal knowledge and published reports on the land use history and matrix composition, we classified the regions into three classes of disturbance regime: (i) low disturbance – Lacandona and Una; (ii) intermediate disturbance – Los Tuxtlas LDL and IDL; and (iii) high disturbance – Los Tuxtlas HDL and Serra Grande (Table 1). All study areas are located in lowland forest areas (