Losing our palms: The influence of landscape-scale deforestation on Arecaceae diversity in the Atlantic forest

Losing our palms: The influence of landscape-scale deforestation on Arecaceae diversity in the Atlantic forest

Forest Ecology and Management xxx (2016) xxx–xxx Contents lists available at ScienceDirect Forest Ecology and Management journal homepage: www.elsev...

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Forest Ecology and Management xxx (2016) xxx–xxx

Contents lists available at ScienceDirect

Forest Ecology and Management journal homepage: www.elsevier.com/locate/foreco

Losing our palms: The influence of landscape-scale deforestation on Arecaceae diversity in the Atlantic forest Maíra Benchimol a,⇑, Daniela C. Talora a, Eduardo Mariano-Neto a,b, Tamiris L.S. Oliveira a, Adrielle Leal a, Marcelo S. Mielke a, Deborah Faria a a PPG Ecologia e Conservação da Biodiversidade, Laboratório de Ecologia Aplicada à Conservação, Universidade Estadual de Santa Cruz, Rodovia Jorge Amado km 16, 45662-900 Ilhéus, BA, Brazil b Departamento de Botânica, Instituto de Biologia, Universidade Federal da Bahia, Rua Barão de Geremoabo, 147, Campus Universitário de Ondina, 40170-290 Salvador, BA, Brazil

a r t i c l e

i n f o

Article history: Received 4 August 2016 Received in revised form 8 November 2016 Accepted 9 November 2016 Available online xxxx Keywords: Deforestation Forest cover Habitat loss

a b s t r a c t Understanding the effects of habitat loss on biodiversity has gained pronounced importance to inform conservation planning. Palms are a characteristic, important component of forest structure and the functionality of tropical forests, yet fragmentation-related studies have been poorly investigated in deforested landscapes. Here, we examine the influence of forest loss at the landscape scale on the entire palm community by evaluating species turnover at nine 16 km2 landscapes in the Brazilian Atlantic Forest with 9– 71% forest cover. Additionally, we examine the influence of canopy openness at the local scale. We identified all live palms at the species level within 50  100 m forest plots at each site and classified species into categories based on their habitat occurrence (‘‘forest-interior” and ‘‘open-area” species). The number of Arecaceae species and stems greatly declined with lower amounts of forest cover at the landscape scale, with the power-law model best explaining these relationships. The community composition was also affected by forest cover, in which higher species dissimilarity was observed among severely deforested landscapes. Additionally, our results showed that palm assemblages have been shaped by nonrandom processes, with forest-interior species being negatively affected by reduced forest cover at the landscape scale. Landscapes embedded within less than 40% forest cover harbored fewer than 10 palm species, mainly consisting of open-area forest species. Our study therefore demonstrates the pervasive influence of habitat loss on palm diversity in severely deforested landscapes in the Brazilian Atlantic Forest hotspot. Extensive management actions, including forest restoration and the reintroduction of animal dispersers, are urgent and serve as important tools to permit the successful recruitment, reproduction and establishment of palm species in the unique Atlantic Forest biome. Ó 2016 Elsevier B.V. All rights reserved.

1. Introduction Anthropogenic activities have modified tropical forest landscapes over centuries, leading to a cascade of species extinctions mostly driven by habitat loss at the landscape scale (Wright, 2010; Arroyo-Rodríguez et al., 2013). Along the eastern Brazilian coast, the Atlantic Forest is one of 35 global biodiversity hotspots, harboring a large number of endemic species that are threatened by forest loss (Martini et al., 2007; Myers et al., 2000). The Atlantic Forest was colonized as long ago as the 1500s, and it has been drastically transformed by the impact of human colonization. Cur-

⇑ Corresponding author at: PPG Ecologia e Conservação da Biodiversidade, Laboratório de Ecologia Aplicada à Conservação, Universidade Estadual de Santa Cruz, Rodovia Jorge Amado km 16, 45662-900 Ilhéus, BA, Brazil. E-mail address: [email protected] (M. Benchimol).

rently, only 12% of the original forest cover remains intact in a mosaic of old growth and secondary forest stands (Ribeiro et al., 2009). Habitat loss and fragmentation has led to several changes in landscape structure and configuration, greatly affecting population and community dynamics (Fahrig, 2003). For instance, forest loss alone has proven to drive plant and animal species extinctions at the landscape scale in tropical forests (Banks-Leite et al., 2012; Lima and Mariano-Neto, 2014; Morante-Filho et al., 2015). Additionally, the remaining patches are prone to decrease over time, as they are more isolated and very close to the forest edge and therefore susceptible to forest fragmentation effects; indeed, recent analyses have shown that 70% of remaining forest worldwide is within 1 km of a forest boundary (Haddad et al., 2015). However, empirical studies have demonstrated that habitat loss leads to more pervasive effects on forest biodiversity than habitat

http://dx.doi.org/10.1016/j.foreco.2016.11.014 0378-1127/Ó 2016 Elsevier B.V. All rights reserved.

Please cite this article in press as: Benchimol, M., et al. Losing our palms: The influence of landscape-scale deforestation on Arecaceae diversity in the Atlantic forest. Forest Ecol. Manage. (2016), http://dx.doi.org/10.1016/j.foreco.2016.11.014

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fragmentation per se (see Fahrig, 2003). Forest cover at the landscape scale can thus be considered a proxy for habitat loss, with non-linear relationships usually observed between the amount of habitat and diversity metrics for different forest biota (Pardini et al., 2010; Estavillo et al., 2013; Ochoa-Quintero et al., 2015). Species richness and compositional similarity in several tropical plant families have been strongly and positively related to forest cover, with forest sites surrounded by a greater amount of forest cover exhibiting a higher number of species and greater similarity than severely deforested landscapes (Lima and Mariano-Neto, 2014; Andrade et al., 2015). Additionally, forest loss is expected to cause alterations to local forest structure, leading forest patches to retain early successional local attributes, including a reduction in the overall basal area and increasing canopy openness (Rocha-Santos et al., 2016). Arecaceae is an essential botanical family for tropical frugivorous animals because it provides a high abundance of fleshy fruits and seeds (Zona and Henderson, 1989; Galetti et al., 2013). Additionally, palms are key components of the forest structure, and many species have been extensively harvested by humans in the tropics (Scariot, 1999). This family is widespread in both intact and fragmented tropical forests and includes species welladapted to a wide range of environmental conditions (Uhl and Dransfiled, 1987). South America is center of endemism for Arecaceae (Pintaud et al., 2008), with studies revealing that environmental factors such as humidity, temperature and soil fertility strongly control species distributions and are therefore likely to affect family richness and composition (Bjorholm et al., 2005, 2006; Salm et al., 2007). Most Arecaceae forest species cope well with moderate levels of anthropogenic disturbance (Scariot, 2001; Bjorholm et al., 2005, 2006), yet alterations including reduced seedling recruitment, competition with alien species, and disruptions to mutualistic relationships with fauna can modify population dynamics and community composition (Scariot, 1999; Wright and Duber, 2001; Fleury and Galetti, 2004). Specifically, in the Brazilian Atlantic Forest, although some species can be found in disturbed areas (e.g., Bactris spp.; Silva and Tabarelli, 2001), others are extremely sensitive to forest disturbance (e.g., Geonoma spp.) and usually exhibit reduced rates of population growth in altered environments (Svenning, 2001). As a result, habitat loss, fragmentation and palm harvesting have been considered the main threats to palms (Scariot, 1999; Tabarelli et al., 2004; Galetti et al., 2006). However, no study has investigated the community and species-specific responses to habitat loss until recently. Here, we investigated the responses of the Arecaceae family to habitat loss at the landscape scale by evaluating species turnover in nine 16 km2 landscapes ranging from 9% to 71% forest cover in the Brazilian Atlantic Forest. Additionally, we examined the influence of canopy openness on local diversity patterns. We specifically evaluated the overall species richness, composition and abundance of palms to both a forest cover gradient at the landscape scale and canopy openness at the local scale. We also classified palm species based on their habitat type and occurrence preferences to assess the responses of both groups to a reduction in forest cover. We hypothesized that palm assemblages will become heavily affected by reduced forest cover and canopy openness, with contrasting groups (‘‘open-area” and ‘‘forest-interior” species) responding oppositely depending on the forest cover gradient. We predicted that (i) species richness and composition similarity will increase in landscapes surrounded by a higher amount of forest cover, following similar responses from other floristic groups (Rigueira et al., 2013; Lima and Mariano-Neto, 2014; Andrade et al., 2015); (ii) the overall abundance will not be affected by forest cover, given that certain ecological groups will be favored by disturbance and consequently compensate for the reduction in others (Scariot, 1999; Andreazzi et al., 2012); (iii) spe-

cies richness will also increase in areas exhibiting lower canopy openness, as these areas exhibit a better-structured canopy (Hilário and Toledo, 2016; Rocha-Santos et al., 2016); and (iv) palm species will exhibit different levels of vulnerability to habitat loss, with forest-interior species and stems greatly increasing in more forested landscapes, whereas open-area species and stems will decline in landscapes containing higher amounts of forest cover. 2. Materials and methods 2.1. Study area This study is part of the REDE SISBIOTA, a research network designed to investigate how landscape-scale forest loss affects patterns of regional biodiversity and processes in anthropogenic landscapes. In this context, Landsat TM images of southern Bahia from 2011 (orbits 215/70 and 215/71) were first digitalized and used to select landscapes. The obtained map was then divided into cells of 4  4 km (16 km2) to estimate the percentage of forest cover based on the sum of old growth and secondary forests at different successional stages. From the wide number of selected landscapes, all indigenous lands, mountainous areas and sites with limited accessibility were excluded, the calculated amount of forest cover was then intensively validated in field expeditions, and each landscape was subsequently grouped into forest cover classes (in percentages). For further details regarding the study area, see Andrade et al. (2015). We performed stratified sampling from the pre-categorized groups and randomly selected nine 16 km2 areas to subsequently perform Arecaceae surveys, which were immersed in landscapes ranging from 9 to 71% forest cover (Fig. 1). We established that each surveyed site needed to be spaced at least 1 km from the other sites to avoid overlapping. The minimum and maximum distances between plots were 6.3 km and 75.1 km, respectively. The surveyed forest sites were located within the municipalities of Belmonte, Mascote and Una (center coordinates: 15°280 S and 39°150 W). Una is situated in the northern area and exhibits large tracts of continuous forest protected by the Una Biological Reserve and Una Wildlife Refuge, two forest reserves encompassing 34,804 ha. All surveyed sites comprised a mixture of mature and secondary forests embedded within a matrix of pastures and shade cacao and/or rubber plantations sharing the same phytophysiognomy and similar soil and topography (Thomas, 2003; Faria et al., 2006). The vegetation is classified as tropical evergreen forest, exhibiting a great abundance of epiphytes, ferns, bromeliads and lianas (Thomas et al., 1998). The climate is warm and humid with annual precipitation over 1300 mm, which is typical of tropical forests. 2.2. Arecaceae sampling In each selected landscape, we identified all old growth and late secondary forest fragments and randomly chose one fragment to establish a 50  100 m (0.5 ha) forest plot. The location of each plot was also randomly selected, maintaining a minimum distance of 50 m from the nearest forest border to minimize edge effects. All live adult individuals from the Arecaceae family in each forest plot were marked and samples were collected based on different criteria due to the morphological and demographic diversity of Arecaceae: [1] among arborescent species presenting underground stems (e.g., Attalea humilis), individuals exhibiting an external and visible stipe; [2] among arborescent species whose stem grows externally in diameter (e.g., Euterpe edulis), individuals with a diameter at breast height (DBH) P 5 cm; and [3] among understory species and shrubs (e.g., from the genera Desmoncus, Geo-

Please cite this article in press as: Benchimol, M., et al. Losing our palms: The influence of landscape-scale deforestation on Arecaceae diversity in the Atlantic forest. Forest Ecol. Manage. (2016), http://dx.doi.org/10.1016/j.foreco.2016.11.014

M. Benchimol et al. / Forest Ecology and Management xxx (2016) xxx–xxx

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Fig. 1. Spatial distribution of the nine forest plots surveyed in southern Bahia, Brazil. Plots located in the municipalities of Belmonte and Mascote are shown in (a), whereas those located in Una are shown in (b).

noma and Bactris), individuals showing reproductive signs (Salm et al., 2011). Species were identified by consulting the herbarium of the Universidade Estadual de Santa Cruz (HUESC) and the literature (Lorenzi et al., 2010; Henderson, 2011). Arecaceae experts were also consulted to confirm the identifications. When possible, botanical vouchers were stored at the HUESC. We further classified each species recorded at least once according to its occurrence and habitat type, i.e., either preferentially occurring in dense-canopy forests (hereafter, ‘‘forest-interior species”) or mostly inhabiting open areas or sparsely dense forests (‘‘open-area species”). This classification was based on a comprehensive literature review, specialist consultations and our own knowledge from observations at other forest sites. We also considered the previous classification from Pires (2006), in which palm species were classified into (1) those favoring forest interior, (2) those favoring open areas, or (3) habitat generalists. Accordingly, we used the two former categories to classify species within two different ecological groups, ‘‘forest-interior” and ‘‘open-area” species. This classification considers that palm species respond

differently to increasing light intensity (i.e., the fundamental source of energy for carbon assimilation), with some species responding positively whereas others react negatively to light intensification (Barot et al., 2005). We excluded Euterpe edulis from this specific analysis due to its generalist response regarding light behavior, which could lead to biases in abundance patterns. 2.3. Canopy openness To assess the canopy openness of each forest plot, we took 10 hemispheric photographs using a 180° (fisheye) lens only on cloudy days to avoid sun reflection by the leaves of the vegetation (Whitmore et al., 1993). Each plot was subdivided into 10 adjacent and circular sub-plots of 20 m2, within which one photo was taken at the central point. The photos were subsequently analyzed in Gap Light Analyzer (GLA version 2.0), which converts each color photograph into a black and white image and calculates the canopy openness by relating the sum of white pixels (light that comes from overstory gaps) and black pixels, which is equivalent to

Please cite this article in press as: Benchimol, M., et al. Losing our palms: The influence of landscape-scale deforestation on Arecaceae diversity in the Atlantic forest. Forest Ecol. Manage. (2016), http://dx.doi.org/10.1016/j.foreco.2016.11.014

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branches and leaves (Frazer et al., 1999). We used the mean of all hemispheric photos taken per plot for data analysis. 2.4. Data analysis We first generated a semivariogram to evaluate potential spatial dependence in the data, considering both the richness and abundance of Arecaceae. This analysis revealed spatial trends, with correlations between the values of a variable decreasing with distance. We thus needed to include spatial covariates in the statistical models by performing 1000 Monte Carlo simulations to construct a confidence envelope based on a complete spatial random distribution of the data to infer the existence and type of spatial trend. The semivariograms were created using the ‘‘geoR” package (Ribeiro and Diggle, 2016) in the R environment (R Core Team, 2016). We thus investigated the patterns of overall richness, abundance and species composition of Arecaceae in response to the percentage of forest cover at the landscape level using a model selection approach. We first performed detrended correspondence analysis (DCA) ordinations on the quantitative species composition using abundance data and used the first axis as a compound variable representing Arecaceae composition. For each response variable, we compared five models that are widely used to examine the effects of habitat loss on forest biota (Banks-Leite et al., 2014; Lima and Mariano-Neto, 2014): (i) a generalized linear model (GLM), (ii) a logistic model (Pinheiro and Bates, 2000); (iii) the power-law model (Crawley, 2007); (iv); the piecewise model (Francesco Ficetola and Denoel, 2009) and (v) the null model. When logistic or piecewise models were selected, we also performed the Davies’ test, which tests for a non-zero difference-inslope parameter for a segmented relationship (Francesco Ficetola and Denoel, 2009) to find possible break points. We used the Akaike information criterion (AICc) and Akaike information weights corrected for small samples (AICw) to select the most plausible model (Anderson, 2008). The best model was the one with the lowest AICc value, exhibiting a difference of at least 2.00 compared to the second model, and a weight of at least two times the weight of the second best model. Otherwise, all models exhibiting low AICc values were considered equivalent, and decisions about the best model were made based on analyses of the residuals and model simplicity (i.e., inexistence of a trend in the residuals and a low number of parameters or linearity). We built routines to adjust nonlinear model parameters with Poisson error, minimizing the model log-likelihood using numerical optimization (Bolker, 2007), and to calculate the AICc, AICw and confidence intervals of the parameters in all models. Additionally, we performed nonmetric dimensional scaling (NMDS) to evaluate the compositional similarities among the forest-interior and openarea forest palm species based on the abundance data. We also intended to investigate the combined influence of forest cover and canopy openness on forest-interior and open-area species abundance using multiple linear regression. However, we first tested for collinearity by performing a Pearson correlation analysis between forest cover and canopy openness, obtaining high levels of correlation (r = 0.91). We were therefore unable to perform any subsequent analyses using both variables and opted to forest cover for three main reasons: (i) it slightly better explained the abundance patterns of palm assemblages (R2 = 0.45, whereas R2 = 0.43 for canopy openness); (ii) it is considered a good proxy for habitat loss (Fahrig, 2003), which was our main focus in this study; and (iii) it is a more practical tool for conservation management actions. We further evaluated the abundance response of forest-interior and open-area ecological groups by performing the same model selection approach as previously described. In addition, we specif-

ically scrutinized the abundance patterns of two genera containing a great number of species, Geonoma and Bactris, as well as the abundance of G. pohliana, a forest interior specialist that has been widely and abundantly recorded at our study sites. All analyses were implemented in the R environment (R Core Team, 2016).

3. Results We sampled 1472 adult individuals belonging to 18 species and 7 genera within 4.5 ha of forest sampled across all nine plots (Table S1). Each plot contained between 5 and 16 species (mean ± SD = 9.6 ± 1.8). The most frequent species among all surveyed landscapes was Bactris hirta (N = 8 plots), whereas Euterpe edulis was the most abundant, with 323 individuals distributed in six areas. Some species of Bactris and all species of Geonoma were more frequently recorded in landscapes exhibiting more forest cover, especially B. glassmanii and G. pauciflora, which occurred only in landscapes with at least 50% forest cover. Conversely, Allagoptera caudescens, Desmoncus orthacanthos and Syagrus botryophora were more frequent in landscapes with under 50% forest cover (Table S1). We determined the habitat classification for all species, of which nine were classified as forest-interior species, whereas the others were categorized as open-area species (Table S1). Canopy openness presented values ranging between 4.9% and 11.6% (mean ± SD = 8.2% ± 2.3), with the study site embedded within the lowest percentage of forest cover (9%) presenting 11% canopy openness and the site showing the greatest forest cover (71%) exhibiting 5.8% canopy openness. All semivariograms showed random patterns of variance associated with distance, failing to exhibit spatial patterns for either Arecaceae richness or abundance. Therefore, given that no trend associated with spatial distributions of the landscapes was observed, we did not include spatial covariates in our models investigating the palm responses to the amount of forest cover. The number of Arecaceae species and stems declined with lower amounts of forest cover at the landscape scale (Fig. 2), with the power-law model best explaining these relationships (Table 1). Additionally, both GLMs and the null models appeared among the best models explaining the richness patterns, but because a significant trend in the residuals of the null model was observed, we did not consider it as a plausible model. The Arecaceae community structure was compared among the surveyed landscapes, with forest cover significantly affecting the first DCA axis and showing more similarity among landscapes embedded within more forest cover than those sites surrounded by lower percentages of coverage (Fig. 3). Both the power-law model and the GLM were parsimonious models for explaining the community composition (Table 1). The composition was considerably distinguishable between openarea and forest-interior species, with the former group exhibiting higher similarity among all nine species than ‘‘forest-interior” species (Fig. 4). Forest cover also explained patterns of both forest-interior and open-area species abundance, mostly explained by the piecewise model (Table 1). We detected a higher number of open-area stems within more deforested landscapes, with a breakpoint of 39.2% (±4.2; P < 0.001) forest cover (Fig. 5). Conversely, a lower number of forest-interior stems were recorded in landscapes with lower forest cover, exhibiting a threshold at 39.6% (±2.2; P < 0.001) forest cover (Fig. 5). Similarly, the piecewise model was the most plausible model explaining patterns of Geonoma spp. abundance, which was greatly reduced in more deforested landscapes (Table 1 and Fig. 6). Conversely, the logistic model best explained the abundance patterns of Bactris spp. and Geonoma pohliana, which presented a lower number of stems in landscapes harboring a lower percentage of forest cover (Table 1 and Fig. 6).

Please cite this article in press as: Benchimol, M., et al. Losing our palms: The influence of landscape-scale deforestation on Arecaceae diversity in the Atlantic forest. Forest Ecol. Manage. (2016), http://dx.doi.org/10.1016/j.foreco.2016.11.014

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Fig. 2. The relationship between forest cover at the landscape scale and (A) the overall palm species richness and (B) abundance at nine surveyed forest sites in southern Bahia, Brazil.

Table 1 Ranking of the best models explaining the Arecaceae patterns investigated in this study. All parsimonious models are highlighted in bold. NC = Parameters did not converge. Model

wAICc

Model

dAICc

wAICc

0.0 0.3 1.3 11.8 NC

0.42 0.37 0.22 0.00

Overall abundance Power-law GLM Null Logistic Piecewise

0.0 3.4 215.7 NC NC

0.84 0.16 <0.001

Composition GLM Power-law Null Logistic Piecewise

0.0 0.9 9.6 26.6 NC

0.61 0.39 0.00 <0.001

Geonoma pohliana abundance Logistic Piecewise GLM Null Power-law

0.0 75.1 116.8 335.9 NC

1.00 <0.001 <0.001 <0.001

Geonoma spp. abundance Piecewise Logistic GLM Null Power-law

0.0 18.6 38.2 536.7 NC

1.00 <0.001 <0.001 <0.001 <0.001

Bactris spp. abundance Logistic Piecewise GLM Null Power-law

0.0 25.3 27.9 59.0 NC

1.00 <0.001 <0.001 <0.001

‘Open-area’ abundance Piecewise GLM Null Power-law Logistic

0.0 60.7 204.5 NC NC

1.00 <0.001 <0.001

‘Forest-interior’ abundance Piecewise Logistic Power-law GLM Null

0.0 13.1 14.2 38.8 513.1

0.99 0.00 <0.001 <0.001 <0.001

Overall richness Power-law GLM Null Piecewise Logistic

dAICc

4. Discussion Our study clearly demonstrates the erosion of Arecaceae richness, composition and abundance associated to reduced forest cover within landscapes of the threatened Brazilian Atlantic Forest. To the best of our knowledge, this is the first study to document the influence of reduced forest cover on an entire palm assemblage, a key ecological group characterizing the structure and composition of tropical forest (Scariot, 1999). Habitat loss has strongly influenced the structure of palm assemblages in a non-linear pattern, with a greater number of species and stems recorded in more forested landscapes. The more deforested landscapes have also more open canopies, indicating a strong correlation between landscape-scale deforestation and important structural local modifications that ultimately could serve as more proximal mechanisms helping explaining the observed compositional changes. Additionally, our results showed that palm assemblages have been under non-random transitions, with open-area species being favored by reduced forest cover at the landscape scale. However, the increase in open-area stems did not compensate for the decline in the abundance of forest-interior species. Unless management

actions are conducted, fragmented forest landscapes are expected to experience a predictable pattern in terms of Arecaceae assemblages, with fragments embedded within less than 40% forest cover locally showing fewer than 10 palm species, mainly consisting of open-area forest species. 4.1. Effects on overall palm assemblages We observed a substantial loss of palm stems in response to reduced forest cover at the landscape scale, following a nonlinear pattern. Studies within the same Atlantic Forest landscapes have also shown a positive trend in the relationship between forest cover and the richness and abundance of other full tree assemblages and particular floristic groups, including Sapotaceae (Lima and Mariano-Neto, 2014), Myrtaceae (Rigueira et al., 2013) and Rubiaceae (Andrade et al., 2015). We have now provided additional evidence for the drastic consequences of reductions in forest cover on floristic assemblages in the unique Atlantic Forest hotspot, showing that a minimum of 40% forest cover is required to ensure that more than half of the total palm species recorded in our study site remain—similar values have been recorded for other floristic

Please cite this article in press as: Benchimol, M., et al. Losing our palms: The influence of landscape-scale deforestation on Arecaceae diversity in the Atlantic forest. Forest Ecol. Manage. (2016), http://dx.doi.org/10.1016/j.foreco.2016.11.014

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Fig. 3. Detrended correspondence analysis (DCA) ordinations of the quantitative species composition of palm species (A) and (B) the relationship between the strongest DCA axis and forest cover at the landscape scale at nine forest sites in southern Bahia, Brazil.

Fig. 4. Nonmetric dimensional scaling (NMDS) for the quantitative species composition among forest-interior and open-area palm species surveyed at nine forest sites in southern Bahia, Brazil.

groups. Although we predicted that forest cover would not affect patterns of abundance, a loss of individuals was clearly observed with a decline in forest cover, demonstrating, therefore, the strong influence of habitat loss on the overall structure of Arecaceae assemblages. In fact, in a recent study conducted in northern Bahia, researchers recorded a higher abundance of palms in forest patches presenting taller, larger trees, and a greater proportion of closed canopy (Hilário and Toledo, 2016), common characteristics of patches with higher amounts of forest cover. The overall density of tree species was also greatly reduced in landscapes embedded within a lower amount of forest cover based on a total of twenty sampling sites at our same study site (Rocha-Santos et al., 2016), indicating a general shrinkage in both the local forest structure and abundance in severely deforested landscapes. Likewise, palm assemblages followed this pattern of decline, suggesting that Arecaceae is a very sensitive group to forest loss. Given that palms are key components of forest structure and serve as important food resources in tropical forests (Scariot, 1999; Aguirre and Dirzo, 2008), a reduction in their richness and abundance is likely to mir-

Fig. 5. The relationships between forest cover at the landscape scale and the abundance of open-area (A) and forest-interior (B) forest species at nine surveyed forest sites in southern Bahia, Brazil.

Please cite this article in press as: Benchimol, M., et al. Losing our palms: The influence of landscape-scale deforestation on Arecaceae diversity in the Atlantic forest. Forest Ecol. Manage. (2016), http://dx.doi.org/10.1016/j.foreco.2016.11.014

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Fig. 6. The relationships between forest cover at the landscape scale and the abundance of (A) Geonoma spp., (B) Bactris spp. and only (C) Geonoma pohliana at nine surveyed forest sites in southern Bahia, Brazil.

ror the impoverishment of specialist frugivores faunal species in highly fragmented forest landscapes. Indeed, a wide range of medium- and large-bodied bird and mammal species are key agents of seed dispersal and the recruitment of palm species in the Atlantic Forest (Zona and Henderson, 1989; Fragoso and Huffman, 2000). However, southern Bahia has long been experiencing high levels of hunting pressure (Canale et al., 2012), and we are aware that several frugivorous bird and mammal species have gone extinct within our deforested landscapes (MoranteFilho et al., 2015; Benchimol, unpublished data). The synergistic effects of fragmentation and defaunation have reduced the densities of both seedling and juvenile species of a key palm species within southeastern Atlantic Forest remnants, Astrocaryum aculeatissimum (Galetti et al., 2006). We therefore presume that local extinctions of key palm dispersers may have affected the dispersal and regeneration of large-seeded palm species, such as Attalea humilis, which appeared in only two surveyed forest sites—both presenting low abundance and embedded within greater than 40% forest coverage. For these species, therefore, local diversity may be explained by the synergetic effects of habitat loss, fragmentation and widespread hunting pressure. Forest cover has also strongly influenced the species composition patterns of Arecaceae in a linear way, in which those landscapes with greater forest cover exhibited higher compositional similarity. In forest patches within the Biological Dynamics ofForest Fragments Project of Central Amazonia, palm assemblages were more similar in similar-sized patches, suggesting the differential responses of this group to habitat fragmentation (Scariot, 1999). A great dissimilarity among deforested landscapes—higher beta diversity—might have occurred due to a decrease in the likelihood of species flux, which in turn led to cumulative differences in species composition (Arroyo-Rodríguez et al., 2013). Likewise, a higher dissimilarity was observed for both adult and juvenile tree assemblages in severely deforested landscapes in our study area, another sign that forest loss has induced an unbalance in floristic diversity in Atlantic Forest landscapes. These results indicate that palm species diversity is proportionally reduced in response to reduced forest cover, as also reported for Rubiaceae species (Andrade et al., 2015). In the southeastern Brazilian Atlantic Forest, habitat loss has also significantly reduced the diversity of Arecaceae, with a significant drop in the number of seedlings in small forest patches (Pires, 2006; Galetti et al., 2006). Therefore, the maintenance of

higher amounts of forest cover at the landscape scale enables a structured palm assemblage, locally comprising a high number of widely diversified stems. 4.2. Vulnerability among species by habitat type Habitat loss did not affect palm species uniformly, with habitat type preferences greatly explaining varying degrees of sensitivity. Specifically, open-area species were favored in severely deforested landscapes, whereas forest-interior species were most extinctionprone in these landscapes. Indeed, life-history traits have been recognized to determine degrees of vulnerability of tropical plant species, with emergent species containing large seeds, exhibiting dense wood and classified as shade-tolerant showing higher sensitivity to habitat loss and fragmentation within Amazonian and Atlantic Forest landscapes (Santos et al., 2008; Magnago et al., 2014; Benchimol and Peres, 2015; Santo-Silva et al., 2015). Specifically, in our studied area, the regeneration strategy has greatly affected the abundance patterns of both young and adult tree species (Benchimol et al., unpublished data), yet the categorization into shade-tolerant and shade-intolerant group species is challenging for palm species. Nevertheless, we were able to classify all species into their preferential habitat type occurrence, i.e., ‘‘forestinterior” and ‘‘open-area” species, and unveiled the strong negative influence of more deforested landscapes on forest-interior species. Indeed, Arecaceae exhibits hyper-diverse adaptation to different environments, with many species coping well with moderate anthropogenic pressures (Svenning, 1998). As expected, the abundance of open-area species was clearly benefited by reduced forest cover and its associated effects, but the increased abundance of these species was not enough to compensate for the loss of forest-interior individuals. Additionally, the values of canopy openness varied among landscapes and were strongly correlated to forest cover, suggesting that palms are also highly sensitive to local changes. Despite the fact that canopy openness influences several processes among plants, the influences of forest cover at the landscape scale are more straightforward for use in conservation practices. It seems that open-area species have been benefiting from forest reductions, such as Allagoptera caudescens and Syagrus botryophora, which have been recorded at higher abundances in more deforested landscapes. We indeed noted a strong correlation between forest cover and canopy openness, indicating that more

Please cite this article in press as: Benchimol, M., et al. Losing our palms: The influence of landscape-scale deforestation on Arecaceae diversity in the Atlantic forest. Forest Ecol. Manage. (2016), http://dx.doi.org/10.1016/j.foreco.2016.11.014

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deforested landscapes exhibit greater light exposure (see also Rocha-Santos et al., 2016) and will consequently benefit openarea species. At our study site, palms seem to be sensitive to both local and landscape changes, possibly because forest patches in more deforested landscapes are likely to be more degraded and, as a result, have higher values of canopy openness. Conversely, the number of stems of overall forest-interior species nonlinearly increased accordingly to the expansion of forest cover at the landscape scale. Additionally, dense-canopy preferential genera declined in severely deforested landscapes, including Bactris spp. and Geonoma spp., and the forest-interior Geonoma pohliana exhibited lower abundance in more deforested landscapes. As this species or the entire genus are conspicuous elements of the local forests and are found in closed and less disturbed forests, their assessment could serve as indicators of the local levels of forest degradation, particularly related to the structural shrinkage of the native forest and its increasing levels of canopy openness. 5. Conclusions Our study demonstrates the sharp collapse in palm diversity in severely deforested landscapes in the Brazilian Atlantic Forest, a key structural and functional plant component of tropical forests (Aguirre and Dirzo, 2008). Approximately 45 palm species belonging to 10 genera occur in the remaining Atlantic Forest hotspot (Lorenzi et al., 2004), with 18 recorded at our studied site in southern Bahia, including the threatened Syagrus botryophora (Noblick, 1998) and one of the most economically valuable products, Euterpe edulis (Fantini and Guries, 2007). Specifically, in landscapes embedded within less than 40% forest cover, we unveiled a strong decrease in the number of species as well as their abundance and composition, similar to patterns obtained for other floristic groups (Rigueira et al., 2013; Lima and Mariano-Neto, 2014; Andrade et al., 2015). As a result, palm-animal interactions, including pollination and dispersal, are greatly compromised over the long term (Guimarães et al., 2005; Barfod et al., 2011). We also relate that the absence of key animal dispersers coupled with low habitat availability are likely to profoundly modify the structure of Atlantic Forests, possibly causing a turnover in palm species—large-seeded and economic species have been indeed penalized whereas open-area species have thrived in severely deforested landscapes. Deforestation is also likely to be affecting the surveyed areas at the local level, with sites embedded within lower levels of forest cover at the landscape scale also exhibiting greater canopy openness. Considering the high costs of measuring the tree canopy in situ, we highlight that measuring forest cover at the landscape scale can be a more straightforward and cheaper method for forest conservation practices. Extensive management actions, including forest restoration and the reintroduction of animal dispersers, are urgently needed and serve as important tools to permit the successful recruitment, reproduction and establishment of palm species in the unique Atlantic Forest biome. Acknowledgments The present study represents publication number #22 of the REDE SISBIOTA, funded by the Brazilian National Council for Scientific and Technological Development (CNPq; 563216/2010-7) and the Universidade Estadual de Santa Cruz (Propp 00220.1100.1039 and 00220.1100.1095). We are grateful to all landowners who enabled us to work on their properties and to all field assistants, especially Rafael Chaves and Carol Cornélio. Funding for Tamiris L. S. Oliveira and Adrielle Leal during this study were provided by scholarships from CAPES (Brazilian Higher Education Council) and CNPq, respectively. We also thank Luiz Alberto Mattos Silva,

Curator of HUESC, H. Lorenzi, Gil Marcelo Reuss-Strenzel and Carlos Alex Lima Guimarães for helping us in species identification and other facilities. Eduardo Mariano-Neto, Deborah Faria (3045371/2015-2) and Marcelo S. Mielke (306531/2015-1) gratefully acknowledge CNPq for the award of fellowships of scientific productivity.

Appendix A. Supplementary material Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.foreco.2016.11. 014.

References Aguirre, A., Dirzo, R., 2008. Effects of fragmentation on pollinator abundance and fruit set of an abundant understory palm in a Mexican tropical forest. Biol. Conserv. 141, 375–384. Anderson, D.R., 2008. Model Based Inference in the Life Sciences: A Primer on Evidence. Springer, NY. Andrade, E.R., Jardim, J.G., Santos, B.A., Melo, F.P., Talora, D.C., Faria, D., Cazetta, E., 2015. Effects of habitat loss on taxonomic and phylogenetic diversity of understory Rubiaceae in Atlantic forest landscapes. For. Ecol. Manage. 349, 73– 84. Andreazzi, C.S., Pimenta, C.S., Pires, A.S., Fernandez, F.A.S., Oliveira-Santos, L.G., Menezes, J.F.S., 2012. Increased productivity and reduced seed predation favor a large-seeded palm in small Atlantic Forest fragments. Biotropica 44, 237–245. Arroyo-Rodríguez, V., Rös, M., Escobar, F., Melo, F.P., Santos, B.A., Tabarelli, M., Chazdon, R., 2013. Plant b-diversity in fragmented rain forests: testing floristic homogenization and differentiation hypotheses. J. Ecol. 101, 1449–1458. Banks-Leite, C., Ewers, R.M., Metzger, J.P., 2012. Unraveling the drivers of community dissimilarity and species extinction in fragmented landscapes. Ecology 93, 2560–2569. Banks-Leite, C. et al., 2014. Using ecological thresholds to evaluate the costs and benefits of set-asides in a biodiversity hotspot. Science 29, 1041–1045. Barfod, A.S., Hagen, M., Borchsenius, F., 2011. Twenty-five years of progress in understanding pollination mechanisms in palms (Arecaceae). Ann. Bot. 108, 1503–1516. Barot, S., Mitja, D., Meija, G.D., Grimaldi, M., 2005. Reproductive plasticity in an Amazonian palm. Evol. Ecol. Res. 7, 1051–1065. Benchimol, M., Peres, C.A., 2015. Edge-mediated compositional and functional decay of tree assemblages in Amazonian forest islands after 26 years of isolation. J. Ecol. 103, 408–420. Bjorholm, S., Svenning, J.C., Skov, F., Balslev, H., 2005. Environmental and spatial controls of palm (Arecaceae) species richness across the Americas. Glob. Ecol. Biogeogr. 14, 423–429. Bjorholm, S., Svenning, J.C., Baker, W.J., Skov, F., Balslev, H., 2006. Historical legacies in the geographical diversity patterns of New World palm (Arecaceae) subfamilies. Bot. J. Linn. Soc. 151, 113–125. Bolker, B.M., 2007. Ecological Models and Sats in R. Princeton University Press, New Jersey. Canale, G.R., Peres, C.A., Guidorizzi, C.E., Gatto, C.A., Kierulff, M.C., 2012. Pervasive defaunation of forest remnants in a tropical biodiversity hotspot. PLoS One 7, e41671. Crawley, M.J., 2007. The R Book. Wiley Publishing, England. Estavillo, C., Pardini, R., Rocha, P.L.B., 2013. Forest loss and the biodiversity threshold: an evaluation considering species habitat requirements and the use of matrix habitats. PLoS One 8, e82369. Fahrig, L., 2003. Effects of habitat fragmentation on biodiversity. Annu. Rev. Ecol. Evol. Syst. 34, 487–515. Fantini, A.C., Guries, R.P., 2007. Forest structure and productivity of palmiteiro (Euterpe edulis Martius) in the Brazilian Mata Atlântica. For. Ecol. Manage. 242, 185–194. Faria, D., Laps, R.R., Baumgarten, J., Cetra, M., 2006. Bat and bird assemblages from forests and shade cacao plantations in two contrasting landscapes in the Atlantic Forest of Southern Bahia, Brazil. Biodivers. Conserv. 15, 587–612. Fleury, M., Galetti, M., 2004. Effects of microhabitat on palm seed predation in two forest fragments in southeast Brazil. Acta Oecol. 26, 179–184. Fragoso, J.M.V., Huffman, J.M., 2000. Seed-dispersal and seedling recruitment patterns by the last Neotropical megafaunal element in Amazonia, the tapir. J. Trop. Ecol. 16, 369–385. Francesco Ficetola, G., Denoel, M., 2009. Ecological thresholds: an assessment of methods to identify abrupt changes in species-habitat relationships. Ecography 32, 1075–1084. Frazer, G.W., Canham, C.D., Lertzman, K.P., 1999. Gap Light Analyzer (GLA), Version 2.0: Imaging Software to Extract Canopy Structure and Gap Light Transmission Indices from True-Colour Fisheye Photographs, Users Manual and Program Documentation. Simon Fraser University, Burnaby, British Columbia, and The Institute of Ecosystem Studies, Millbrook, New York, p. 36.

Please cite this article in press as: Benchimol, M., et al. Losing our palms: The influence of landscape-scale deforestation on Arecaceae diversity in the Atlantic forest. Forest Ecol. Manage. (2016), http://dx.doi.org/10.1016/j.foreco.2016.11.014

M. Benchimol et al. / Forest Ecology and Management xxx (2016) xxx–xxx Galetti, M., Donatti, C.I., Pires, A.S., Guimarães, P.R., Jordano, P., 2006. Seed survival and dispersal of an endemic Atlantic forest palm: the combined effects of defaunation and forest fragmentation. Bot. J. Linn. Soc. 151, 141–149. Galetti, M. et al., 2013. Functional extinction of birds drives rapid evolutionary changes in seed size. Science 340, 1086–1090. Guimarães, P.R., Lopes, P.F., Lyra, M.L., Muriel, A.P., 2005. Fleshy pulp enhances the location of Syagrus romanzoffiana (Arecaceae) fruits by seed-dispersing rodents in an Atlantic forest in south-eastern Brazil. J. Trop. Ecol. 21, 109–112. Haddad, N.M. et al., 2015. Habitat fragmentation and its lasting impact on Earth’s ecosystems. Sci. Adv. 1, e1500052. Henderson, A.A., 2011. Revision of Geonoma (Arecaceae). Phytotaxa 17, 1–271. Hilário, R.R., Toledo, J.J., 2016. Effects of climate and forest structure on palms, bromeliads and bamboos in Atlantic Forest fragments of Northeastern Brazil. Brazil. J. Biol. http://dx.doi.org/10.1590/1519-6984.00815. Lima, M.M., Mariano-Neto, E., 2014. Extinction thresholds for Sapotaceae due to forest cover in Atlantic Forest landscapes. For. Ecol. Manage. 312, 260–270. Lorenzi, H., Sousa, H.M., Costa, J.T.M., Cerqueira, L.S.C., Ferreira, E., 2004. Palmeiras Brasileiras: Nativas E Exóticas Cultivadas. Instituto Plantarum, Nova Odessa, SP. Lorenzi, H., Noblick, L., Kahn, F., Ferreira, E., 2010. Flora Brasileira: Arecaceae (Palmeiras). Instituto Plantarum, Nova Odessa, SP. Magnago, L.F.S., Edwards, D.P., Edwards, F.A., Magrach, A., Martins, S.V., Laurance, W.F., 2014. Functional attributes change but functional richness is unchanged after fragmentation of Brazilian Atlantic forests. J. Ecol. 102, 475–485. Martini, A.M.Z., Fiaschi, P., Amorim, A.M., da Paixão, J.L., 2007. A hot-point within a hot-spot: a high diversity site in Brazil’s Atlantic Forest. Biodivers. Conserv. 16, 3111–3128. Morante-Filho, J.C., Faria, D., Mariano-Neto, E., Rhodes, J., 2015. Birds in anthropogenic landscapes: the responses of ecological groups to forest lossin the Brazilian Atlantic Forest. PLoS One 10, e0128923. Myers, N., Mittermeier, R.A., Mittermeier, C.G., Fonseca, G.A., daand Kent, J., 2000. Biodiversity hotspots for conservation priorities. Nature 403, 853–858. Noblick, L., 1998. Syagrus botryophora. The IUCN Red List of Threatened Species 1998 (downloaded on 21 May 2016). Ochoa-Quintero, J.M., Garder, T.A., Rosa, I., Ferraz, S.F.B., Sutherland, W.J., 2015. Thresholds of species loss in Amazonian deforestation frontier landscapes. Conserv. Biol. 29, 440–451. Pardini, R., Bueno, A.A., Gardner, T.A., Prado, P.I., Metzger, J.P., 2010. Beyond the fragmentation threshold hypothesis: regime shifts in biodiversity across fragmented landscape. PLoS One 5, 1–10. Pinheiro, J.C., Bates, D.M., 2000. Mixed-Effects Models in S and S-Plus. Springer Science and Business Media. Pintaud, J.C. et al., 2008. Las palmeras de América del Sur: diversidad, distribución e historia evolutiva. Revista peruana de biología 15, 7–30. Pires, A.S., 2006. Perda de diversidade de Arecaceae em fragmentos de Mata Atlântica: padrões e processos PhD Thesis. Universidade Estadual Paulista, Rio Claro, São Paulo. R Core Team, 2016. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria . Ribeiro, M.C., Metzger, J.P., Martensen, A.C., Ponzoni, F.J., Hirota, M.M., 2009. The Brazilian Atlantic Forest: How much is left, and how is the remaining forest distributed? Implications for conservation. Biol. Conserv. 142, 1141–1153. Ribeiro Jr, P.J., Diggle, P.J., 2016. geoR: Analysis of Geostatistical Data. R package version 1.7-5.2 .

9

Rigueira, D.M.G., Rocha, P.L.B., Mariano-Neto, E., 2013. Forest cover, extinction thresholds and time lags in woody plants (Myrtaceae) in the Brazilian Atlantic Forest: resources for conservation. Biodivers. Conserv. 22, 3141–3163. Rocha-Santos, L., Pessoa, M.S., Cassano, C.R., Talora, D.C., Orihuela, R.L.L., MarianoNeto, E., Morante-Filho, J.C., Faria, D., Cazetta, E., 2016. The shrinkage of a forest: landscape-scale deforestation leading to overall changes in local forest structure. Biol. Conserv. 196, 1–9. Salm, R., Salles, N.V.D., Alonso, W.J., Schuck-Paim, C., 2007. Cross-scale determinants of palm species distribution. Acta Amazon. 37, 17–25. Salm, R., Jardim, M.A.G., Albernaz, A.L.K.M., 2011. Abundance and diversity of palms in the Sustainable Forest District of BR-163 road, Pará, Brazil. Biota Neotrop. 11, 99–105. Santo-Silva, E.E., Withey, K.D., Almeida, W.R., Mendes, G., Lopes, A.V., Tabarelli, M., 2015. Seedling assemblages and the alternative successional pathways experienced by Atlantic forest fragments. Plant Ecol. Div. 4, 483–492. Santos, B.A., Peres, C.A., Oliveira, M.A., Grillo, A., Alves-Costa, C.P., Tabarelli, M., 2008. Drastic erosion in functional attributes of tree assemblages in Atlantic forest fragments of northeastern Brazil. Biol. Conserv. 142, 249–260. Scariot, A., 1999. Forest fragmentation effects on palm diversity in central Amazonia. J. Ecol. 87, 66–76. Scariot, A., 2001. Weedy and secundary palm species in central amazonian forest Fragments. Acta Bot. Brasil. 15, 272–280. Silva, M.G., Tabarelli, M., 2001. Seed dispersal, plant recruitment and spatial distribution of Bactris acanthocarpa Martius (Arecaceae) in a remnant of Atlantic forest in northeast Brazil. Acta Oecol. 22, 259–268. Svenning, J.C., 1998. The effect of land-use on the local distribution of palm species in an Andean rain forest fragment in northwestern Ecuador. Biodivers. Conserv. 7, 1529–1537. Svenning, J.C., 2001. On the role of microenvironmental heterogeneity in the ecology and diversification of neotropical rain-forest palms (Arecaceae). Bot. Rev. 67, 1–53. Tabarelli, M., Silva, M.J.C., Gascon, C., 2004. Forest fragmentation, synergisms and the impoverishment of neotropical forests. Biodiv. Conserv. 13, 1419–1425. Thomas, W.W., Carvalho, A.M.V., Amorim, A.M.A., Garrison, J., Arbeláez, A.L., 1998. Plant endemism in two forests in southern Bahia, Brazil. Biodiv. Conserv. 7, 311–322. Thomas, W.W. (2003) Natural vegetation types in southern Bahia. In: Prado, P.I., Landau, E.C., Moura, R.T., Pinto, L.P.S., Fonseca, G.A.B., Alger, K. (orgs.), corredor deBiodiversidade da Mata Atlântica do Sul da Bahia. Publicação em CD-ROM, Ilhéus, IESB/CI/CABS/UFMG/UNICAMP. Uhl, N.W., Dransfiled, J., 1987. Genera Palmarum. Allen Press, Kansas. 610 pp. Whitmore, T.C., Brown, N.D., Swaine, M.D., Kennedy, D., Goodwin-Bailey, C.I., Gong, W.K., 1993. Use of hemispherical photographs in forest ecology: measurement of gap size and radiation totals in a Bornean tropical rain forest. J. Trop. Ecol. 9, 131–151. Wright, S.J., Duber, H.C., 2001. Poachers and forest fragmentation alter seed dispersal, seed survival, and seedling recruitment in the palm attaleabutyraceae, with implications for tropical tree diversity 1. Biotropica 33, 583–595. Wright, S.J., 2010. The future of tropical forests. Ann. N. Y. Acad. Sci. 1195, 1–27. Zona, S., Henderson, A., 1989. A review of animal-mediated seed dispersal of palms. Selbyana, 6–21.

Please cite this article in press as: Benchimol, M., et al. Losing our palms: The influence of landscape-scale deforestation on Arecaceae diversity in the Atlantic forest. Forest Ecol. Manage. (2016), http://dx.doi.org/10.1016/j.foreco.2016.11.014