Fewer berries and more pods: losers and winners of chronic disturbance in an Ecuadorian tropical dry forest

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Here, we evaluated the effects of chronic disturbance on the functional diversity of a seasonally dry tropical forest, and their potential effects on the frugivores guild. We characterized eight plant traits related to seed dispersal and calculated the community weighted means and functional diversities for trees and the whole woody community. We used generalized linear models to evaluate the effects of the disturbance on these functional estimates in relation with the abundance and diversity of fruits as resources for wildlife. Our results revealed that, the dominance of plants with costly fruiting species was reduced with disturbance. Functional richness and divergence were reduced with the disturbance, mainly in the qualitative traits. Finally, the availability of resources was slightly different between groups of dispersers, observing a general pattern of reduction in the availability and richness of fruits with disturbance. Our results suggest that the changes in species richness and abundance are not random but the result of filtering on traits related to dispersal costs and their subsequent ability to withstand environmental stress. The observed changes in vegetation have a direct effect on the availability of resources for frugivorous species, which in the medium term can affect the woody species persistence and catalyze the woody species loss. drylands functional diversity frugivory seed dispersal dispersal syndrome Figures Figure 1 Figure 2 Figure 3 Figure 4 Figure 5 Figure 6 Figure 7 Introduction Understanding how anthropogenic disturbance affects biodiversity of tropical forests is a critical demand due to the dramatic deforestation and degradation rates (Vitousek 1994 ; Portillo-Quintero and Smith 2018 ; Ribeiro et al. 2019 ). Human-driven disturbance generates a sharp decline and homogenization of biodiversity (Mckinney and Lockwood 1999 ; Olden et al. 2004 ; Lôbo et al. 2011 ; Tabarelli et al. 2012 ). This homogenization results from a reduction in the suitability of the habitat for certain species -losers- and a parallel increase in the abundance of others -winners- (Smart et al. 2006 ; Tabarelli et al. 2012 ), depending on their environmental tolerances and requirements (Cadotte et al. 2011 ). Although the underlining paradigm is a taxonomic homogenization after degradation (Olden et al. 2006 ; Lôbo et al. 2011 ), some authors suggested that it could also imply a functional simplification and convergence (Smart et al. 2006 ), increasing the vulnerability of entire species groups with particular functional traits (Cadotte et al. 2011 ; López-Martínez et al. 2013 ; Pessoa et al. 2017 ). Evidence also shows that certain critical dimensions of the plant trait architecture, such as those related to wood tissue (Chave et al. 2009 ) and to the leaf economic spectrum (Osnas et al. 2013 ), suffer a drastic reduction in tropical forests after anthropogenic disturbance (Nunes-Nesi et al. 2016 ; Sfair et al. 2018 ). It is also expected that a third functional dimension of plant species related to dispersal and reproduction is also deeply affected by man-driven disturbance (Pessoa et al. 2016 ; Pessoa et al. 2017 ). Even more, it is known that large-fruited and large-seeded species are especially sensitive after perturbation (Tabarelli et al. 2010 ; Magnago et al. 2014 ) which would have dramatic implications for animal-plant interactions, and community dynamics (Galetti et al. 2011 ; Pessoa et al. 2016 ; Pessoa et al. 2017 ). A considerable effort has been devoted to understanding the process of biodiversity loss after disturbance, including their functional and phylogenetic counterparts. However, most of those efforts have focused on deforestation and subsequent fragmentation as drivers of tropical forest diversity loss (Tabarelli et al. 2010 ; Lôbo et al. 2011 ; Pessoa et al. 2017 ; Zambrano et al. 2019 ). However the effect of chronic disturbance ( i.e. small scale extensive livestock farming and coppicing) are by far less known, despite their importance at a global scale (Laliberté et al. 2010 ). Chronic disturbance implies low-intensity but constant human pressures without a loss in the extent of vegetation (Singh 1998 ). Often the forest extent is maintained whereas the biomass, structure, diversity, and ecosystem services decline (Lamb et al. 2005 ; Peres et al. 2006 ). This maintenance of the forest extension makes difficult to assess chronic disturbance, a problem that can be aggravated by the interaction of different pressures acting together, as well as the differences in relation to the initial primary productivity of the forests (Smart et al. 2006 ; Sfair et al. 2018 ). One of the tropical ecosystems experiencing a higher pressure from chronic disturbance is the seasonally dry neotropical forests (SDTFs) (Ribeiro-Neto et al. 2016 ; Ribeiro-Neto et al. 2016 ; Arnan et al. 2018 ; Jara-Guerrero et al. 2021 ). Chronic disturbance in SDTFs usually combines livestock grazing and small-scale timber extraction (Jara-Guerrero et al. 2019 ), which intensify stress through increased solar radiation and ground-level temperature and reduced soil content of water and nutrients (Khurana and Singh 2001 ; Lebrija-Trejos et al. 2011 ; Maza-Villalobos et al. 2022 ). Previous studies suggest that the stress induced in SDTFs by chronic disturbance is driving a loss of plant taxonomic diversity (Ribeiro-Neto et al. 2016 ; Silva et al. 2020 ; Jara-Guerrero et al. 2021 ), with the exclusion of species with particular ecological functions (Sfair et al. 2018 ). However, the chronic disturbance could drive different changes at the community level, depending on the type of pressure exerted and consequences on the environment. For instance, it is expected that the establishment of species in these disturbed forests will be defined by functional traits related to stress tolerance, mainly due to increased drought (Balvanera et al. 2011 ; Fauset et al. 2012 ). On the other hand, Silva et al. ( 2020 ) reported that the richness of species with fleshy fruits, and those with zoochoric dispersal were affected negatively by an increase in aridity but positively by the wood extraction or livestock grazing in SDTFs of the Caatinga region. Recent research at SDTFs in southwestern Ecuador showed that free-foraging goats in the forest disperse mainly legume seeds, particularly those of species with dry pods (Espinosa et al. 2021 ); therefore, in chronically disturbed areas, where wild dispersers are almost excluded, those species with specialized traits for genuine dispersal by animals – i.e., fleshy fruits – may be adversely affected. On the other hand, Maza-Villalobos et al. ( 2022 ) reported for SDTFs of Mexico that the presence of cattle negatively affected the size and weight of fruits, and the seed number per fruit, while the weight and size of seeds were positively affected. Considered collectively, this evidence suggests that chronic disturbance and aridity interact in complex ways, including synergistically (Arnan et al. 2018 ), making predictions very difficult. Therefore, it seems necessary to clarify to what extent some functional traits are driving this plant diversity loss and functional homogenization because of chronic disturbance, and their effects at local scales. SDTFs in Ecuador show a significant loss of tree diversity associated with chronic disturbance (Cueva Ortiz et al. 2019 ; Jara-Guerrero et al. 2021 ). Thus, we are interested in assessing whether these changes in plant diversity generate a loss of functional diversity associated with seed dispersal, and the potential effects on the resource availability for wildlife. With this in mind, we addressed the following specific questions; i) how does the abundance of species with particular dispersal traits change with chronic disturbance? ii) Are these changes in abundance the outcome of an environmental filtering on species with particular functional traits? iii) What is the impact of those changes in the abundance and diversity of functional traits on the access to resources by wildlife? We hypothesized that chronic disturbance limits the establishment of plants with fleshy fruits, large seeds, and dispersed by animals, because of their short period of seed viability, high water and nutrient requirements, and limitation of seed dispersers to forage in disturbed areas (Ribeiro et al. 2015 ). Consequently, we expected that the variety and distribution of functional trait values, i.e. the functional diversity of traits of fruits and seeds, will be negatively affected by chronic disturbance. Because trees show a higher loss of species richness than shrub species (Jara-Guerrero et al. 2021 ), these effects should be stronger in the case of trees than when the entire plant community, including trees and shrubs, is evaluated. Although the effects of chronic disturbance on shrubs are less understood, this group may be favored by low and medium levels of chronic disturbance (Jara-Guerrero et al. 2021 ) because of the different and ampler requirements of water and light compared to trees (Niinemets 1996 ). Finally, in SDTFs, where more than half of woody species depends on animals for the seed dispersal service (Jara-Guerrero et al. 2011 ), the changes in functional diversity of the dispersal and reproductive traits have implications for the dynamics of the entire ecosystem triggering cascade effects (Cadotte et al. 2011 ; López-Martínez et al. 2013 ; Pessoa et al. 2017 ). Materials and Methods Study area Our study was conducted in Southwestern Ecuador (Loja province, Zapotillo, Macará and Celica counties; between latitudes 4°19'39 " and 4°01'40" S and between longitudes 80°19'00 " and 79°41'40" W). This is part of the Tumbesian region and comprises some of the largest and best-preserved remnants of SDTFs. The altitude ranges from 120 to 1100 m a.s.l. The annual mean temperature is between 20° and 26° C, and the annual mean precipitation ranges from 300 to 700 mm (Cueva Ortiz et al. 2019 ). There is a dry season from May to November and a rainy season from December to April. Dominant tree species were Cochlospermum vitifolium (Cochlospermaceae); Handroanthus chrysanthus and H. bilbergii (Bignoniacea); Ceiba trichystandra , Eriotheca ruizii (Bombacaceae); Guazuma ulmifolia (Malvaceae) and Muntingia calabura (Muntingiaceae) (Cueva Ortiz et al. 2019 ). These forest remnants are mainly used for grazing of goats and cattle and sporadic wood extraction (Jara-Guerrero et al. 2019 ; Cueva-Ortiz et al. 2020 ; Jara-Guerrero et al. 2021 ; Patiño et al. 2021 ; Espinosa et al. 2021 ). Although the animal community of seed dispersers has not been extensively studied, this area hosts some potential seed dispersers (Valle et al. 2021 ) such as at least two frugivorous bat species ( Artibeus fraterculus, Sturnira bakeri ) and other two omnivorous bats ( Lophostoma occidentalis, Phyllostomus discolor ) (Tirira et al. 2011 ). Two deer species that inhabit this SDTFs have also been reported feeding fruits, Odocoileus virginianus (Tirira et al. 2011 ; Jara-Guerrero et al. 2018 ) and Mazama americana (Boada and Roman 2005 ; Tirira et al. 2011 ). Other omnivores feeding on fruits are fox Lycalopex sechurae , Pecari tajacu and some rodents (e.g. Sciurus spp. and Proechimys decumanus ) (Boada and Roman 2005 ). Moreover, this area is widely recognized by the diversity of bird species, some of which are well-known for their potential as seed dispersers (Ordóñez-Delgado et al. 2016 ). Data sampling Within an area of 1800 Km 2 , we randomly selected 24 locations covering a wide gradient of chronic disturbance resulting from grazing and logging of SDTF over different periods and intensities of use (Jara-Guerrero et al. 2019 ). In each locality, we placed an L-shape cluster of three plots of 60 x 60 m separated 200 m from each other. In these plots we recorded all trees with a diameter at breast height (DBH) ≥ 10 cm. Shrubs with DBH ≥ 5 cm were also registered in a sub-plot of 20 x 20 m established in one corner of each plot (see Cueva et al. 2019 for details). Plots covered an altitudinal range from 234 to 1037 m asl. Morphology and dispersal traits Between January and June 2017, we collected fruits and seeds directly from fruiting trees. With these samples, we made a morphological characterization recording weight, length and width of fruits and seeds, number of seeds per fruit, and three qualitative traits: fruit type, fruit color and dispersal syndrome. We measured a minimum of 10 fruits and 50 seeds per species from at least five healthy individuals. We calculated the area of fruits and seeds as the area of an ellipse, i.e. the product of Pi by the radius of the length and radius of the width. For those woody species that did not produce fruits during the study time traits were obtained from bibliographic information or collections of seeds stored in the germplasm bank of Universidad Técnica Particular de Loja. We assigned a color to fruits of each species taking as reference Wheelwright & Janson ( 1985 ) and Galetti et al. ( 2011 ), which consider nine colors according to human perception: black (including dark red), red (including pink), yellow, orange, brown, gray, green, white and blue (including purple). Following Van der Pijl ( 1969 ), we categorized all the species in three primary dispersal syndromes: anemochory (wind), zoochory (animals) and autochory (explosion or gravity) (see Table S1 for the dispersal assignation). Lately and based on bibliographic information and personal observations we assigned each of these zoochorous species to a group of dispersers: birds, bats, non-ungulate mammals, ungulate mammals and reptiles (Table S2 ). Data analysis Chronic disturbance was defined based on three variables known to be a surrogate of anthropogenic perturbation: (1) distance to the nearest human settlements, which vary from hamlets to villages. Considering that the free foraging activities of the goats intensify in the surroundings of the human settlements, the increase in the distance implies less disturbance (Martorell and Peters 2005 ; Cueva Ortiz et al. 2019 ). (2) Biomass of goats feces in the plot (Martorell and Peters 2005 ; Cueva Ortiz et al. 2019 ), and (3) number of tree individuals with DBH > 20 cm, because a decrease of big trees is indicative of high disturbance (Méndez-Toribio et al. 2016 ). These predictors of chronic anthropogenic disturbance were used to adjust a principal component analysis (PCA). For the rest of analyses, we selected the first axis of the PCA as a chronic disturbance index. To evaluate the effects of chronic disturbance on the abundance of species with particular dispersal traits, we calculated the community weighted mean (CWM) (Garnier et al., 2004) by using the density of individuals for each species. For the qualitative traits, the CWM was calculated as the proportion of each trait’s level in the plot. To evaluate the changes of functional diversity with the chronic disturbance, we calculated three measures of functional diversity; functional richness (FRic), functional evenness (FEve) and functional divergence (FDis) (Villéger et al. 2008 ). These measures were calculated by using the density of each species and were estimated both for the trees and also for the entire community, i.e. trees and shrubs. Because the trees and shrubs were measured in a different sized area, we calculated the density per hectare for shrubs and trees separately and then pooled the data. We built generalized linear models for each trait by using the CWM and functional diversity as response variables, and the chronic disturbance index (CDI), elevation as a proxy of climate variation, and the interaction between chronic disturbance and elevation (CDI:E) as explanatory variables. We included the elevation as a covariate in our models to control the effects of climate on the plant community. We used elevation as a proxy of climate because it can provide a more accurate indication of local climatic variations than available climate grids (see Franklin et al. 2019 ). Additionally, the correlation between changes in the plant community and elevation has been extensively acknowledged (Gallardo-Cruz et al. 2009 ; Balvanera et al. 2011 ; Espinosa et al. 2011 ). For the analysis of qualitative traits, we adjusted Generalized Linear Models (GLMs) using a binomial error distribution. For quantitative variables, we tested the model fit using Gamma and Gaussian error distributions, as not all variables showed a normal distribution. When using Gamma error distribution, we employed three link functions: square root, logarithmic, and inverse. We adjusted three models for each measured trait: i) complete model; it is a model with CDI, elevation and CDI:E, ii) model without interaction; CDI and elevation, and iii) reduced model; only CDI. For each model we used four error distribution structures; gamma error distribution with three link functions and the gaussian error distribution. We used the AIC statistic to detect the best adjustment among the 12 models. To evaluate the effects of chronic disturbance on the availability of fruits for wildlife, we applied generalized linear models by using the basal area and species richness of plants associated with different disperser groups as response variables. In order to standardize the variables for each disperser group, we divided the basal area of resources by the highest value of the plot. We followed the same procedure used to evaluate the best model in the dispersal trait analysis (see above) but using the quasipoisson error family for count data. All of the analyses were implemented in the R environment (R Core Team 2019 ). We used the “rda” function from the “vegan” package (Oksanen et al. 2018 ) to adjust the PCA. The functional diversity measures were calculated through the “dbFD” of the “FD” package (Laliberté and Legendre 2010 ). Results From the 100 woody species recorded in the plots, we obtained data for the 72 species distributed in 33 families and 59 genera. These species represented 74% of the total abundance and 64% of the basal area of woody species in the study area. The families that presented the highest number of species and genera were: Fabaceae (22 species, 17 genera) and Malvaceae (6 species, 4 genera). Dry fruits represented the 64% (46 species), and fleshy fruits represented the other 36% (26 species). We distinguished seven types of fruits, the most common were pods (n = 18, 25%) and capsules (n = 15, 21%) related to autochory and anemochory. Other types of fruits were berries (n = 11, 15%), drupes (n = 13, 17%), samara (n = 8, 11%), in a smaller proportion achene (n = 5, 7%) and, syconium (n = 2, 3%). In addition, eight colors were recognized among fruits, being brown fruits the most common among the species (n = 36, 50%), followed by the yellow ones (n = 10, 14%), and green (n = 9, 14%). The dominant dispersal syndrome was zoochory (n = 33, 45%), followed by anemochory (n = 23, 31%) and autochory in smaller proportion (n = 16, 22%). From the autochory group, 5 species have been reported to be secondarily dispersed by ungulates (see Table S2 ). Most of the zoochorous species showed traits related to dispersal by birds (22 species) and non-ungulate mammals (17 species). Other zoochorous species presented traits related to dispersal by reptiles (13 species), micromammals (11 species) and ungulates (10 species, including those primarily autochorous) (see Table S2 ). The first PCA axis of the chronic disturbance variables explained the 54% of the variation, and was positively associated with the number of goat feces, and negatively with the distance to human settlements and density of large trees (Table S3 ). Functional traits related to seed dispersal The proportion of fruit types was affected by chronic disturbance in different ways. Within trees, only achene was not affected by CDI, while pods increased and the rest reduced (Fig. 1 , Table S4 ). Moreover, our models showed that those negative effects of CDI on the proportion of berries, capsules, samaras, and syconium were reduced as elevation increased (CDI:E positive effect). On the contrary, for pods, elevation reduced the positive effect of CDI (CDI:E negative effect). When we analyzed both trees and shrubs, the only change regarding trees was observed in berries and drupes, which did not show an effect of CDI on their proportions (Fig. 1 ). Regarding the fruit color, the proportion of tree species with red, white, and yellow fruits was negatively affected by CDI, an effect that increased with elevation (CDI:E positive effect, Fig. 2 , Table S4 ). The proportion of species with brown fruits was positively affected by CDI, although reduced with elevation. When we analyzed trees and shrubs, the pattern on brown fruits was the opposite. For black and green fruits, the effect of CDI changed from non-significant for trees to significant for shrubs and trees, being negative for black and positive for green ones. Additionally, orange fruits were positively affected by CDI (Fig. 2 ). We found that CDI affected significantly and positively the proportion of autochorous trees, and negatively that of zoochorous species, while anemochorous tree species showed no effects (Fig. 3 a, Table S4 ). At higher elevation the positive effect of chronic disturbance on the proportion of autochorous trees increased (CDI:E positive effect). The CDI did not affect autochorous species when combining tree and shrub species, while the negative effect on zoochorous species found for trees turned positive. Positive effect on zoochory was reduced with elevation (CDI:E negative effect, Fig. 3 a). We observed a significant and negative effect of chronic disturbance on fruit weight and seeds per fruit, both for trees and shrub and trees together. The negative effect of chronic disturbance reduced with elevation, except for fruit weight of trees (Fig. 3 b). Seed area of shrubs and trees was significant and negatively affected by chronic disturbance, with a weaker effect with elevation (CDI:E positive effect, Fig. 3 c). Changes in dispersal functional diversity Chronic disturbance significantly affected functional diversity in its different components. FRic and FEve of fruit color, and FDis of fruit type were affected significantly and negatively by chronic disturbance (Fig. 4 a, Table S4 ), being these effects stronger at low elevations (CDI:E positive effect). The CDI also affected positively the FEve of fruit type and dispersal syndrome (Fig. 4 a, Table S4 ). When analyzing trees and shrubs together, the positive effect of CDI changed to negative for FEve of fruit type and dispersal syndrome. Models for quantitative fruit and seed traits (Fig. 5 , Table S4 ) showed that chronic disturbance negatively affected the FRic of fruit area, as well as FEve and FDis of seed number per fruit and seed weight. The FDis of seed area also showed a negative effect of CDI. These effects of CDI were similar when analysing the trees and shrubs together, except for FEve of seed area and FDis for seed weight, with a significant and negative effect on seed area and no significant effect on seed weight. Changes in fruit availability for frugivorous groups Chronic disturbance negatively affected the species richness of tree species dispersed by birds, reptiles, and non-ungulate mammals (Fig. 6 , Table S5 ). Those effects were stronger at lower elevations. When considering tree and shrubs together, these effects remained for species dispersed by birds and non-ungulate mammals, while the effects on species dispersed by reptiles disappeared. On the contrary, the richness of species dispersed by micromammals increased with the disturbance. Chronic disturbance negatively affected the abundance of trees dispersed by birds, non-ungulate mammals, and ungulates. For species dispersed by non-ungulates mammals, this effect was stronger at lower elevations. When analyzing trees and shrubs together, the negative effect of chronic disturbance on the abundance of species dispersed by birds remained, although it was stronger at lower elevations (CDI:E positive effect). On the contrary, the negative effect on trees dispersed by ungulates and non-ungulate mammals was diluted. On the other hand, the effect of chronic disturbance on species dispersed by micromammals and reptiles became significant and negative (Fig. 7 ). Discussion Seasonal tropical dry forests are highly endangered due to chronic anthropogenic disturbance (Singh 1998 ; Miles et al. 2006 ; Oliveira et al. 2017 ). Although the reach and spatial extension of this chronic disturbance are not easy to assess, it is known that forests suffering this pressure support lower species richness than less disturbed forests (Ribeiro et al. 2015 ; Ribeiro-Neto et al. 2016 ; Sfair et al. 2018 ; Cueva Ortiz et al. 2019 ; Jara-Guerrero et al. 2021 ). Our results revealed that a reduction in the presence and abundance of species with particular seed dispersal traits accompanies this loss of woody richness. This is especially true in the tree assemblage, while shrubs show little or no effect on the variety and abundance of seed dispersal traits. In this way, the shrubs could temporally soften the chronic disturbance effects on the availability and diversity of resources for wildlife that depend on them for their food. Additionally, those areas with lower water availability (i.e. located at lower elevations), support the strongest effects of chronic disturbance on the abundance and diversity of functional traits. Previous studies indicated that the loss of forest species generated by chronic disturbance is initially defined by the loss of species with vegetative traits that allow the avoidance of water loss, such as hard and small leaves (Sfair et al. 2018 ; Ribeiro et al. 2019 ). Additionally, there is pressure from livestock, especially goats, a generalist herbivore, that controls the recruitment of new plants (Weng et al. 2017 ). As hypothesized, chronic disturbance also affects the structure and composition of the vegetation by filtering certain traits associated with dispersal, limiting the establishment of species with more expensive fruits, associated with dispersion by animals. In this way, the pressures that generate the disturbance would be limiting the species regeneration through different paths, with the zoochorous species with fleshy fruits being the major losers. Although there is not microenvironmental information for our forests, some studies in SDTFs have reported that the loss of forest density associated with chronic disturbance increases stress due to greater exposure of the soil to radiation, which, together with greater evaporation, generates an increase in water stress (Galicia et al. 1999 ; Balvanera et al. 2002 ; Sfair et al. 2018 ). Furthermore, there is evidence that these changes in microenvironmental conditions are related to the loss of most tree forest species (Jara-Guerrero et al. 2021 ), changes in plant-animal interactions (Câmara et al. 2018 ; Melo et al. 2023 ) and in species composition (Shahabuddin and Kumar 2006 ), as well as with increases in genotoxic damage in birds (Cevallos-Solorzano et al. 2023 ). Similarly, micro-environmental changes behind chronic disturbance can limit plant access to essential resources required for producing expensive fruits, thereby reducing their persistence in disturbed areas. In this line, more studies are needed to evaluate the impact of chronic disturbance on fruit production and clarify the process behind, either the abundance of individuals bearing fruits or the per capita fruit production (Pessoa et al. 2016 ). On the other hand, autochorous woody species were the winners. This result is not a surprise since autochorous species have been shown to be opportunistic pioneers and, consequently, more common in disturbed habitats (Hilje et al. 2015 ), but also some of them are secondarily dispersed by goats (Espinosa et al. 2021 ). In our study area, most of autochorous species are legumes with seeds covered by hard coats (Jara-Guerrero et al. 2011 ; Jara-Guerrero et al. 2020 ) that led them to tolerate drought and survive not only the dry season but even larger periods waiting for adequate germination windows. Contrary to what we expected, chronic disturbance did not cause a generalized loss of functional richness; however, we found important changes in the functional configuration of the woody community related to shifts in functional evenness and divergence. Two important patterns emerge from these changes in the dominance of certain functional traits: on the one hand, an increase in functional evenness, with a reduction in functional dispersion. This pattern suggests that the negative effects observed occur on dominant characters such as capsules and samaras, which generally have anemochorous dispersion. Anemochorous species dominate SDTF, representing 52% of the abundance of woody plants (Jara-Guerrero et al. 2011 ). On the other hand, chronic disturbance reduces functional evenness for some traits such as the color or size of fruits and seeds. In this case, the disturbance reduced fruit colors such as red, white, and yellow, frequently low-abundant and associated with zoochorous species, that in these forests represent 35% of the abundance of individuals (Jara-Guerrero et al. 2011 ). According to Silva et al. ( 2020 ), chronic disturbance has resulted in changes in the functional structure of the Caatinga dry forests, leading to a reduction in the FDis of reproductive functional groups. Our results support this finding and suggest that chronic disturbance may similarly modify the functional structure of the woody plant community. However, it is worth noting that our study area represents an intermediate of the disturbance gradient, which is quite far from severely degraded areas in which trees are really scarce (Jara-Guerrero et al. 2019 ). It is possible that in those areas with higher level of disturbance the filtering processes implies an even higher loss of functional richness. Shrubs play an interesting role by blurring the negative effects of chronic disturbance on the proportions of dispersal syndromes and fruit types, although the negative effect on fruit color remains. According to Jara-Guerrero et al. ( 2021 ), the openness of canopy in these forest leads to an increase in the density of shrubs which find an opportunity for actively recruit new individuals under more sunny conditions. Thus, to some extent, shrubs can help maintain a certain offer of dispersal traits in degraded forests. Another valuable finding is that the environmental filtering generated by chronic disturbance was stronger at lower elevation. In STDFs, lower elevations support the lower precipitation rates and higher mean temperatures (Cueva Ortiz et al. 2019 ), being under higher risk in the face of climate change (Manchego et al. 2017 ). Thus, those species with capsules, samaras and fleshy fruits, particularly those with red, yellow and white fruits can be lost with the chronic disturbance. Additionally, the availability of fruits associated to frugivorous species is also strongly affected at lower elevations. Since a high diversity of functional fruit traits can sustain a larger community of frugivores (Galetti et al. 2011 ; Morante-Filho et al. 2018 ), the observed changes in the functional traits of the woody community have direct effects on the availability of resources for frugivorous species (Aizen and Feinsinger 1994 ; Morante-Filho et al. 2018 ) and represented a potential cascading effect on the whole ecosystem (Ribeiro-Neto et al. 2016 ). This is especially significant for those species with red, white and yellow fruits, which are related to consumption by birds and mammals. Thus, the loss of these resources can explain the reduction of richness and abundance reported for some groups such as bats (Valle et al. 2021 ) and birds (Almazán-Núñez et al. 2015 ) in these forests. On the other hand, we found a low effect of disturbance on the abundance and diversity of resources for ungulates. One of the main ungulates is the deer ( Odocoileus virginianus ) which is known as a disperser of several species with pods that were thought to be only dispersed via autochory (Jara-Guerrero et al. 2018 ). Thus, the abundance of pods in degraded areas can explain why the richness of species dispersed by ungulates were not affected by the chronic disturbance. In conclusion, species were filtered based on traits related to dispersal costs and their subsequent ability to withstand the environmental stress induced by the disturbance. The observed changes in vegetation have a direct effect on the availability of resources for frugivorous species, which in the medium term can generate a cascading effect on the whole forest ecosystem. Although zoochory and plant regeneration dynamics are recognized as key processes to ecosystem functionality, there is need to aid them in the development of a risk assessment approach for the ecosystem (Escribano-Avila et al. 2017 ). Our work shows that disturbance is not only reducing biodiversity, but also the key processes are being modified. The knowledge of those processes would contribute to the application of effective management actions for the conservation of the SDTFs and their ecosystem services. Declarations Conflict of interest: We declare that we have no conflict of interest. Ethics approval: Not applicable. Consent to participate : Not applicable. Consent for publication: Not applicable. Author contribution statement CE and AJ-G conceived and designed the research and analyzed the data. JC-E and JC collected the data. AJ-G, CE, AE and JC-E wrote the original draft. All co-authors discussed the results and commented and approved the final manuscript. Financial interests The authors declare they have no financial interests. Funding: This work was supported by Universidad Técnica Particular de Loja (PROY_CCNN_1054), Secretaría de Educación Superior, Ciencia, Tecnología e Innovación (PIC-13-ETAPA-004, PIC-13-ETAPA-005), German Research Foundation DFG (project PAK 824/B3), and QuerPin (PID2021-126927NB-I00). Acknowledgments The Ministerio del Ambiente y Agua del Ecuador provided us the research permit N° 002-2017-IC-FLO-NUTR-VS-UPN-DPAL-MAE for the collection of fruits and seeds in the study area. Availability of data and material: The datasets analyzed during the current study are available as supplementary material. Code availability: The codes used during the current study are available from the corresponding author on reasonable request. References Aizen MA, Feinsinger P (1994) Forest fragmentation, pollination, and plant reproduction in a chaco dry forest, Argentina. Ecology 75:330–351. https://doi.org/10.2307/1939538 Almazán-Núñez RC, Arizmendi MDC, Eguiarte LE, Corcuera P (2015) Distribution of the community of frugivorous birds along a successional gradient in a tropical dry forest in south-western Mexico. J Trop Ecol 31:57–68. https://doi.org/10.1017/S0266467414000601 Arnan X, Arcoverde GB, Pie MR, Ribeiro-Neto JD, Leal IR (2018) Increased anthropogenic disturbance and aridity reduce phylogenetic and functional diversity of ant communities in Caatinga dry forest. Sci Total Environ 631–632:429–438. https://doi.org/10.1016/j.scitotenv.2018.03.037 Balvanera P, Lott E, Segura G, Siebe C, Islas A (2002) Patterns of β-diversity in a Mexican tropical dry forest. J Veg Sci 13:145–158. https://doi.org/10.1111/j.1654-1103.2002.tb02034.x Balvanera P, Quijas S, Pérez-Jiménez A (2011) Distribution patterns of tropical dry forest trees along a mesoscale water availability gradient. Biotropica 43:414–422. https://doi.org/10.1111/j.1744-7429.2010.00712.x Boada C, Roman H (2005) Evaluación ecológica rápida de la mastofauna en dos localidades de bosque seco en el occidente de la provincia de Loja. In: Vázquez MA, Freire JF, Suárez L (eds) Biodiversidad en los bosques secos de la zona de Cerro Negro-Cazaderos, occidente de la provincia de Loja: un reporte de las evaluaciones ecológicas y socioeconómicas rápidas. EcoCiencia, MAE y Proyecto Bosque Seco, Quito, pp 73–90 Cadotte MW, Carscadden K, Mirotchnick N (2011) Beyond species: Functional diversity and the maintenance of ecological processes and services. J Appl Ecol 48:1079–1087. https://doi.org/10.1111/j.1365-2664.2011.02048.x Câmara T, Leal IR, Blüthgen N, Oliveira FMP, Queiroz RT de, Arnan X (2018) Effects of chronic anthropogenic disturbance and rainfall on the specialization of ant–plant mutualistic networks in the Caatinga, a Brazilian dry forest. J Anim Ecol 87:1022–1033. https://doi.org/10.1111/1365-2656.12820 Cevallos‐Solorzano G, Bailon‐Moscoso N, Ordóñez‐Delgado L, Jara P, Tomás G, Espinosa CI (2023) Chronic Degradation of Seasonally Dry Tropical Forests Increases the Incidence of Genotoxicity in Birds. GeoHealth 7:e2022GH000774. https://doi.org/10.1029/2022GH000774 Chave J, Coomes D, Jansen S, Lewis SL, Swenson NG, Zanne AE (2009) Towards a worldwide wood economics spectrum. Ecol Lett 12:351–366. https://doi.org/10.1111/j.1461-0248.2009.01285.x Cueva Ortiz J, Espinosa CI, Quiroz Dahik C, Aguirre Mendoza Z, Cueva Ortiz E, Gusman E, Weber M, Hildebrandt P (2019) Influence of anthropogenic factors on the diversity and structure of a dry forest in the central part of the Tumbesian region (Ecuador-Perú). Forests 10:1–22. https://doi.org/10.3390/f10010031 Cueva-Ortiz J, Espinosa CI, Aguirre-Mendoza Z, Gusmán-Montalván E, Weber M, Hildebrandt P (2020) Natural regeneration in the Tumbesian dry forest: identification of the drivers affecting abundance and diversity. Sci Rep 10:9786. https://doi.org/10.1038/s41598-020-66743-x Escribano-Avila G, Cervera L, Ordóñez-Delgado L, Jara-Guerrero A, Amador L, Paladines B, Briceño J, Parés-Jiménez V, Lizcano DJ, Duncan DH, Espinosa CI (2017) Biodiversity patterns and ecological processes in Neotropical dry forest: the need to connect research and management for long-term conservation. Neotrop Biodivers 3:107–116. https://doi.org/10.1080/23766808.2017.1298495 Espinosa CI, Cabrera O, Luzuriaga A, Escudero A (2011) What factors affect diversity and species composition of endangered tumbesian dry forests in southern Ecuador? Biotropica 43:15–22. https://doi.org/10.1111/j.1744-7429.2010.00665.x Espinosa CI, Reyes C, Jara-Guerrero A (2021) Las cabras como dispersores de semillas: aportes y limitaciones para la regeneración del bosque tropical estacionalmente seco de Ecuador. Rev Biol Trop 69:557–572. https://doi.org/10.15517/rbt.v69i2.45046 Fauset S, Baker TR, Lewis SL, Feldpausch TR, Affum-Baffoe K, Foli EG, Hamer KC, Swaine MD (2012) Drought-induced shifts in the floristic and functional composition of tropical forests in Ghana. Ecol Lett 15:1120–1129. https://doi.org/10.1111/j.1461-0248.2012.01834.x Franklin J, Majure LC, Encarnación Y, Clase T, Almonte‐Espinosa H, Landestoy M, Kratter AW, Oswald JA, Soltis DE, Terrill RS, Steadman DW (2019) Changing ecological communities along an elevation gradient in seasonally dry tropical forest on Hispaniola (Sierra Martín García, Dominican Republic). Biotropica 51:802–816. https://doi.org/10.1111/btp.12707 Galetti M, Pizo MA, Morellato LPC (2011) Diversity of functional traits of fleshy fruits in a species-rich Atlantic rain forest. Biota Neotropica 11:181–193. https://doi.org/10.1590/s1676-06032011000100019 Galicia L, Lopez-Blanco J, Zarco-Arista A, Filips V, García-Oliva F (1999) The relationship between solar radiation interception and soil content in a tropical deciduous forest in Mexico. Catena 36:153–164. https://doi.org/10.1016/S0341-8162(98)00121-0 Gallardo-Cruz JA, Pérez-García EA, Meave JA (2009) β-Diversity and vegetation structure as influenced by slope aspect and altitude in a seasonally dry tropical landscape. Landsc Ecol 24:473–482. https://doi.org/10.1007/s10980-009-9332-1 Hilje B, Calvo-Alvarado J, Jiménez-Rodríguez C, Sánchez-Azofeifa A (2015) Tree species composition, breeding systems, and pollination and dispersal syndromes in three forest successional stages in a tropical dry forest in Mesoamerica. Trop Conserv Sci 8:76–94. https://doi.org/10.1177/194008291500800109 Jara-Guerrero A, De la Cruz M, Méndez M (2011) Seed dispersal spectrum of woody species in South Ecuadorian dry forests: environmental correlates and the effect of considering species abundance. Biotropica 43:722–730. https://doi.org/10.1111/j.1744-7429.2011.00754.x Jara-Guerrero A, Escribano-Avila G, Espinosa CI, De la Cruz M, Méndez M (2018) White-tailed deer as the last megafauna dispersing seeds in Neotropical dry forests: the role of fruit and seed traits. Biotropica 50:169–177. https://doi.org/10.1111/btp.12507 Jara-Guerrero A, Espinosa CI, Méndez M, De la Cruz M, Escudero A (2020) Dispersal syndrome influences the match between seed rain and soil seed bank of woody species in a Neotropical dry forest. J Veg Sci 31:995–1005. https://doi.org/10.1111/jvs.12894 Jara-Guerrero A, González-Sánchez D, Escudero A, Espinosa CI (2021) Chronic disturbance in a tropical dry forest: Disentangling direct and indirect pathways behind the loss of plant richness. Front For Glob Change 4:723985. https://doi.org/10.3389/ffgc.2021.723985 Jara-Guerrero A, Maldonado-Riofrío D, Espinosa CI, Duncan DH (2019) Beyond the blame game: a restoration pathway reconciles ecologists’ and local leaders’ divergent models of seasonally dry tropical forest degradation. Ecol Soc 24:22. https://doi.org/10.5751/ES-11142-240422 Khurana E, Singh JS (2001) Ecology of seed and seedling growth for conservation and restoration of tropical dry forest : A review. Environ Conserv 28:39–52. https://doi.org/10.1017/S0376892901000042 Laliberté E, Legendre P (2010) A distance-based framework for measuring functional diversity from multiple traits. Ecology 91:299–305. https://doi.org/10.1890/08-2244.1 Laliberté E, Wells JA, Declerck F, Metcalfe DJ, Catterall CP, Queiroz C, Aubin I, Bonser SP, Ding Y, Fraterrigo JM, McNamara S, Morgan JW, Merlos DS, Vesk PA, Mayfield MM (2010) Land-use intensification reduces functional redundancy and response diversity in plant communities. Ecol Lett 13:76–86. https://doi.org/10.1111/j.1461-0248.2009.01403.x Lamb D, Erskine PD, Parrotta JA (2005) Restoration of Degraded Tropical Forest Landscapes. Science 310:1628–1632. https://doi.org/10.1126/science.1111773 Lebrija-Trejos E, Pérez-García EA, Meave JA, Poorter L, Bongers F (2011) Environmental changes during secondary succession in a tropical dry forest in Mexico. J Trop Ecol 27:477–489. https://doi.org/10.1017/S0266467411000253 Lôbo D, Leão T, Melo FPL, Santos AMM, Tabarelli M (2011) Forest fragmentation drives Atlantic forest of northeastern Brazil to biotic homogenization. Diversity and Distributions 17:287–296. https://doi.org/10.1111/j.1472-4642.2010.00739.x López-Martínez JO, Sanaphre-Villanueva L, Dupuy JM, Hernández-Stefanoni JL, Meave JA, Gallardo-Cruz JA (2013) β-Diversity of functional groups of woody plants in a tropical dry forest in Yucatan. PloS one 8:e73660. https://doi.org/10.1371/journal.pone.0073660 Magnago LFS, Edwards DP, Edwards FA, Magrach A, Martins SV, Laurance WF (2014) Functional attributes change but functional richness is unchanged after fragmentation of Brazilian Atlantic forests. J Ecol 102:475–485. https://doi.org/10.1111/1365-2745.12206 Manchego CE, Hildebrandt P, Cueva J, Espinosa CI, Stimm B, Günter S (2017) Climate change versus deforestation: Implications for tree species distribution in the dry forests of southern Ecuador. PLoS ONE 12:1–19. https://doi.org/10.1371/journal.pone.0190092 Martorell C, Peters EM (2005) The measurement of chronic disturbance and its effects on the threatened cactus Mammillaria pectinifera. Biol Conserv 124:199–207. https://doi.org/10.1016/j.biocon.2005.01.025 Maza-Villalobos S, García-Ramírez P, Endress BA, Lopez-Toledo L (2022) Plant functional traits under cattle grazing and fallow age scenarios in a tropical dry forest of Northwestern Mexico. Basic Appl Ecol. https://doi.org/10.1016/j.baae.2022.06.006 Mckinney ML, Lockwood JL (1999) Biotic homogenization: a few winners replacing many losers in the next mass extinction. Trends Ecol Evol 14:450–453. https://doi.org/10.1016/S0169-5347(99)01679-1 Melo DHA, Freitas AVL, Tabarelli M, Filgueiras BKC, Leal IR (2023) Aridity and chronic anthropogenic disturbance as organizing forces of fruit-feeding butterfly assemblages in a Caatinga dry forest. Biotropica 55:173–184. https://doi.org/10.1111/btp.13173 Méndez-Toribio M, Meave JA, Zermeño-Hernández I, Ibarra-Manríquez G (2016) Effects of slope aspect and topographic position on environmental variables, disturbance regime and tree community attributes in a seasonal tropical dry forest. J Veg Sci 27:1094–1103. https://doi.org/10.1111/jvs.12455 Miles L, Newton AC, DeFries RS, Ravilious C, May I, Blyth S, Kapos V, Gordon JE (2006) A global overview of the conservation status of tropical dry forests. J Biogeogr 33:491–505. https://doi.org/10.1111/j.1365-2699.2005.01424.x Morante-Filho JC, Arroyo-Rodríguez V, Pessoa M de S, Cazetta E, Faria D (2018) Direct and cascading effects of landscape structure on tropical forest and non-forest frugivorous birds. Ecol Appl 28:2024–2032. https://doi.org/10.1002/eap.1791 Niinemets Ü (1996) Plant growth-form alters the relationship between foliar morphology and species shade-tolerance ranking in temperate woody taxa. Vegetatio 124:145–153. https://doi.org/10.1007/BF00045490 Nunes-Nesi A, Nascimento VDL, De Oliveira Silva FM, Zsögön A, Araújo WL, Sulpice R (2016) Natural genetic variation for morphological and molecular determinants of plant growth and yield. J Exp Bot 67:2989–3001. https://doi.org/10.1093/jxb/erw124 Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens HH, Wagner H, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2018) vegan: community ecology package Olden JD, Poff NL, Douglas MR, Douglas ME, Fausch KD (2004) Ecological and evolutionary consequences of biotic homogenization. 19:18–24. https://doi.org/10.1016/j.tree.2003.09.010 Olden JD, Poff NL, McKinney ML (2006) Forecasting faunal and floral homogenization associated with human population geography in North America. Biol Conserv 127:261–271. https://doi.org/10.1016/j.biocon.2005.04.027 Oliveira F, Ribeiro-Neto JD, Andersen AN, Leal IR (2017) Chronic anthropogenic disturbance as a secondary driver of ant community structure: Interactions with soil type in Brazilian Caatinga. Environ Conserv 44:115–123. https://doi.org/10.1017/S0376892916000291 Ordóñez-Delgado L, Tomás G, Armijos-Ojeda D, Jara-Guerrero A, Cisneros R, Espinosa CI (2016) New contributions to the knowledge of birds in Tumbesian region; conservation implications of the Dry Forest Biosphere Reserve, Zapotillo, Ecuador. Ecosistemas 25. https://doi.org/10.7818/ECOS.2016.25-2.03 Osnas JLD, Lichstein JW, Reich PB, Pacala SW (2013) Global leaf trait relationships: Mass, area, and the leaf economics spectrum. Science 340:741–744. https://doi.org/10.1126/science.1231574 Patiño J, Ramón P, Gusmán-Montalván E, Escudero A, de la Cruz M (2021) Fencing promotes fast recovery of demographic processes after grazing-driven collapse in Bursera graveolens forests. For Ecol Manage 499:119592. https://doi.org/10.1016/j.foreco.2021.119592 Peres CA, Barlow J, Laurance WF (2006) Detecting anthropogenic disturbance in tropical forests. Trends Ecol Evol 21:227–229. https://doi.org/10.1016/j.tree.2006.03.007 Pessoa MS, Hambuckers A, Benchimol M, Rocha-Santos L, Bomfim JA, Faria D, Cazetta E (2017) Deforestation drives functional diversity and fruit quality changes in a tropical tree assemblage. Perspect Plant Ecol Evol Syst 28:78–86. https://doi.org/10.1016/j.ppees.2017.09.001 Pessoa MS, Rocha-Santos L, Talora DC, Faria D, Mariano-Neto E, Hambuckers A, Cazetta E (2016) Fruit biomass availability along a forest cover gradient. Biotropica 49:45–55. https://doi.org/10.1111/btp.12359 Portillo-Quintero C, Smith V (2018) Emerging trends of tropical dry forests loss in North & Central America during 2001–2013: The role of contextual and underlying drivers. Appl Geogr 94:58–70. https://doi.org/10.1016/j.apgeog.2018.03.011 R Core Team (2019) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria Ribeiro EMS, Arroyo-Rodríguez V, Santos BA, Tabarelli M, Leal IR (2015) Chronic anthropogenic disturbance drives the biological impoverishment of the Brazilian Caatinga vegetation. J Appl Ecol 52:611–620. https://doi.org/10.1111/1365-2664.12420 Ribeiro EMS, Lohbeck M, Santos BA, Arroyo‐Rodríguez V, Tabarelli M, Leal IR (2019) Functional diversity and composition of Caatinga woody flora are negatively impacted by chronic anthropogenic disturbance. J Ecol 107:2291–2302. https://doi.org/10.1111/1365-2745.13177 Ribeiro-Neto JD, Arnan X, Tabarelli M, Leal IR (2016) Chronic anthropogenic disturbance causes homogenization of plant and ant communities in the Brazilian Caatinga. Biodivers Conserv 25:943–956. https://doi.org/10.1007/s10531-016-1099-5 Sfair JC, De Bello F, De Frana TQ, Baldauf C, Tabarelli M (2018) Chronic human disturbance affects plant trait distribution in a seasonally dry tropical forest. Environ Res Lett 13. https://doi.org/10.1088/1748-9326/aa9f5e Shahabuddin G, Kumar R (2006) Influence of anthropogenic disturbance on bird communities in a tropical dry forest: role of vegetation structure. Anim Conserv 9:404–413. https://doi.org/10.1111/j.1469-1795.2006.00051.x Silva JLS, Cruz-Neto O, Rito KF, Arnan X, Leal IR, Peres CA, Tabarelli M, Valentina Lopes A (2020) Divergent responses of plant reproductive strategies to chronic anthropogenic disturbance and aridity in the Caatinga dry forest. Sci Total Environ 704:135240. https://doi.org/10.1016/j.scitotenv.2019.135240 Singh SP (1998) Chronic disturbance, a principal cause of environmental degradation in developing countries. Envir Conserv 25:1–2. https://doi.org/10.1017/S0376892998000010 Smart SM, Thompson K, Marrs RH, Le Duc MG, Maskell LC, Firbank LG (2006) Biotic homogenization and changes in species diversity across human-modified ecosystems. Proc R Soc B 273:2659–2665. https://doi.org/10.1098/rspb.2006.3630 Tabarelli M, Aguiar AV, Girão LC, Peres CA, Lopes AV (2010) Effects of pioneer tree species hyperabundance on forest fragments in Northeastern Brazil. Conserv Biol 24:1654–1663. https://doi.org/10.1111/j.1523-1739.2010.01529.x Tabarelli M, Peres CA, Melo FPL (2012) The “few winners and many losers” paradigm revisited: Emerging prospects for tropical forest biodiversity. Biol Conserv 155:136–140. https://doi.org/10.1016/j.biocon.2012.06.020 Tirira DG, Burneo SF, Boada CE, Lobos SE (2011) Mammalia, Chiroptera, Phyllostomidae, Lonchophylla hesperia G. M. Allen, 1908: second record of the Western Nectar Bat in Ecuador after 70 years. Check List 7:315. https://doi.org/10.15560/7.3.315 Valle D, Griffith DM, Jara-Guerrero A, Armijos-Ojeda D, Espinosa CI (2021) A multifaceted approach to understanding bat community response to disturbance in a seasonally dry tropical forest. Sci Rep 11:5667. https://doi.org/10.1038/s41598-021-85066-z Van Der Pijl L (1969) Principles of dispersal in higher plants. Springer-Verlag Berlin Heidelberg, New York Villéger S, Mason NWH, Mouillot D (2008) New multidimensional functional diversity indices for a multifaceted framework in functional ecology. Ecology 89:2290–2301. https://doi.org/10.1890/07-1206.1 Vitousek P (1994) Beyond global warming: ecology and global change. Ecology 75:1861–1876 Weng C-Y, Hsieh C, Su M-H (2017) Recruitment dynamics mediated by ungulate herbivory can affect species coexistence for tree seedling assemblages. TAIWANIA 62:283–293. https://doi.org/10.6165/tai.2017.62.283 Wheelwright NT, Janson CH (1985) Colors of fruit displays of bird-dispersed plants. Am Nat 126:777–799 Zambrano J, Garzon-Lopez CX, Yeager L, Fortunel C, Cordeiro NJ, Beckman NG (2019) The effects of habitat loss and fragmentation on plant functional traits and functional diversity: what do we know so far? Oecologia 191:505–518. https://doi.org/10.1007/s00442-019-04505-x Supplementary Files TableS1.pdf TableS2.pdf TableS3.pdf TableS4.pdf TableS5.pdf Cite Share Download PDF Status: Posted Version 1 posted You are reading this latest preprint version Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. 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The dots in the plot represent the estimate for each variable, while the lines represent the standard deviation. Variables with significant effects are shown with colored lines, while variables with non-significant effects are shown with grey lines. Each plot includes only the variables considered in the best model.\u003c/p\u003e","description":"","filename":"Figure1.png","url":"https://assets-eu.researchsquare.com/files/rs-4469206/v1/14063a15286ca4532760ad75.png"},{"id":58189011,"identity":"4c472d84-2e14-4ff3-b9e4-acbf2bfc3f80","added_by":"auto","created_at":"2024-06-12 08:06:36","extension":"png","order_by":2,"title":"Figure 2","display":"","copyAsset":false,"role":"figure","size":274821,"visible":true,"origin":"","legend":"\u003cp\u003eGeneralized linear model estimates of the proportion of fruit color for trees (left), and trees and shrubs (right). The dots in the plot represent the estimate for each variable, while the lines represent the standard deviation. Variables with significant effects are shown with colored lines, while variables with non-significant effects are shown with grey lines. Each plot includes only the variables considered in the best model.\u003c/p\u003e","description":"","filename":"Figure2.png","url":"https://assets-eu.researchsquare.com/files/rs-4469206/v1/3bc3c6d1b8e5e67865e2c438.png"},{"id":58188992,"identity":"bd501c04-1fe0-4c83-8633-3ebd984889aa","added_by":"auto","created_at":"2024-06-12 08:06:35","extension":"png","order_by":3,"title":"Figure 3","display":"","copyAsset":false,"role":"figure","size":352808,"visible":true,"origin":"","legend":"\u003cp\u003eGeneralized linear model estimates of the proportion of dispersal syndromes, fruit and seed traits for trees (left), and trees and shrubs (right). The dots in the plot represent the estimate for each variable, while the lines represent the standard deviation. Variables with significant effects are shown with colored lines, while variables with non-significant effects are shown with grey lines. Each plot includes only the variables considered in the best model.\u003c/p\u003e","description":"","filename":"Figure3.png","url":"https://assets-eu.researchsquare.com/files/rs-4469206/v1/c92ae546137f623f2659ead5.png"},{"id":58189002,"identity":"73bec45a-5e5c-4a85-b240-a52ea58807aa","added_by":"auto","created_at":"2024-06-12 08:06:36","extension":"png","order_by":4,"title":"Figure 4","display":"","copyAsset":false,"role":"figure","size":315742,"visible":true,"origin":"","legend":"\u003cp\u003eGeneralized linear model estimates of functional diversity of qualitative traits for trees (top) and trees and shrubs (bottom). The dots in the plot represent the estimate for each variable, while the lines represent the standard deviation. Variables with significant effects are shown with colored lines, while variables with non-significant effects are shown with grey lines. Each plot includes only the variables considered in the best model.\u003c/p\u003e","description":"","filename":"Figure4.png","url":"https://assets-eu.researchsquare.com/files/rs-4469206/v1/88de5da843a8b837dce580fe.png"},{"id":58189015,"identity":"690e1396-c420-4056-8202-df1a24d59e58","added_by":"auto","created_at":"2024-06-12 08:06:37","extension":"png","order_by":5,"title":"Figure 5","display":"","copyAsset":false,"role":"figure","size":462924,"visible":true,"origin":"","legend":"\u003cp\u003eGeneralized linear model estimates of the functional diversity of quantitative fruit and seed traits for trees (top) and trees and shrubs (bottom). The dots in the plot represent the estimate for each variable, while the lines represent the standard deviation. Variables with significant effects are shown with colored lines, while variables with non-significant effects are shown with grey lines. Each plot includes only the variables considered in the best model.\u003c/p\u003e","description":"","filename":"Figure5.png","url":"https://assets-eu.researchsquare.com/files/rs-4469206/v1/9c8985bd2973b02e667b9fd4.png"},{"id":58189010,"identity":"12d52219-65ed-4c7c-b867-19c68eb41441","added_by":"auto","created_at":"2024-06-12 08:06:36","extension":"png","order_by":6,"title":"Figure 6","display":"","copyAsset":false,"role":"figure","size":493117,"visible":true,"origin":"","legend":"\u003cp\u003eGeneralized linear model estimates of the resources richness for trees (left), and trees and shrubs (right). The dots in the plot represent the estimate for each variable, while the lines represent the standard deviation. Variables with significant effects are shown with colored lines, while variables with non-significant effects are shown with grey lines. Each plot includes only the variables considered in the best model.\u003c/p\u003e","description":"","filename":"Figure6.png","url":"https://assets-eu.researchsquare.com/files/rs-4469206/v1/344e407af1c8005da9d823f3.png"},{"id":58189003,"identity":"18e0f039-1816-4b76-b7c7-a4cada1a3270","added_by":"auto","created_at":"2024-06-12 08:06:36","extension":"png","order_by":7,"title":"Figure 7","display":"","copyAsset":false,"role":"figure","size":502133,"visible":true,"origin":"","legend":"\u003cp\u003eGeneralized linear model estimates of the resources abundance for trees (left), and trees and shrubs (right). The dots in the plot represent the estimate for each variable, while the lines represent the standard deviation. Variables with significant effects are shown with colored lines, while variables with non-significant effects are shown with grey lines. Each plot includes only the variables considered in the best model.\u003c/p\u003e","description":"","filename":"Figure7.png","url":"https://assets-eu.researchsquare.com/files/rs-4469206/v1/ae468e91aeca7ef70ebc59b1.png"},{"id":63707137,"identity":"6efdf1f3-46bf-4bcc-b4fa-765ed2b2b779","added_by":"auto","created_at":"2024-08-31 20:43:41","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":3307369,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-4469206/v1/bb3fd387-653a-4600-ae88-18f9c9cd9b48.pdf"},{"id":58188999,"identity":"006ab377-f812-45cb-baf9-e9879e9d5721","added_by":"auto","created_at":"2024-06-12 08:06:36","extension":"pdf","order_by":11,"title":"","display":"","copyAsset":false,"role":"supplement","size":221103,"visible":true,"origin":"","legend":"","description":"","filename":"TableS1.pdf","url":"https://assets-eu.researchsquare.com/files/rs-4469206/v1/d00d339c2d924204552b9ec8.pdf"},{"id":58189001,"identity":"a129e8d2-86cc-4d00-b8bd-614b31a12d93","added_by":"auto","created_at":"2024-06-12 08:06:36","extension":"pdf","order_by":12,"title":"","display":"","copyAsset":false,"role":"supplement","size":122246,"visible":true,"origin":"","legend":"","description":"","filename":"TableS2.pdf","url":"https://assets-eu.researchsquare.com/files/rs-4469206/v1/8cafeb1cdb39f4ae16bae5d3.pdf"},{"id":58189007,"identity":"90a3b929-f441-4d9f-8b6f-de7bb7a4bacc","added_by":"auto","created_at":"2024-06-12 08:06:36","extension":"pdf","order_by":13,"title":"","display":"","copyAsset":false,"role":"supplement","size":35936,"visible":true,"origin":"","legend":"","description":"","filename":"TableS3.pdf","url":"https://assets-eu.researchsquare.com/files/rs-4469206/v1/428f314b4f64e53f87fcdb40.pdf"},{"id":58189013,"identity":"10ee354f-30e2-43ae-a6b7-74175cabf81f","added_by":"auto","created_at":"2024-06-12 08:06:36","extension":"pdf","order_by":14,"title":"","display":"","copyAsset":false,"role":"supplement","size":186794,"visible":true,"origin":"","legend":"","description":"","filename":"TableS4.pdf","url":"https://assets-eu.researchsquare.com/files/rs-4469206/v1/d8c74bc068562de031f490f1.pdf"},{"id":58189005,"identity":"950ce3f4-dae1-420e-9c19-b3dc774091ed","added_by":"auto","created_at":"2024-06-12 08:06:36","extension":"pdf","order_by":15,"title":"","display":"","copyAsset":false,"role":"supplement","size":66344,"visible":true,"origin":"","legend":"","description":"","filename":"TableS5.pdf","url":"https://assets-eu.researchsquare.com/files/rs-4469206/v1/34e62fd7dcd1415ca7098b99.pdf"}],"financialInterests":"","formattedTitle":"Fewer berries and more pods: losers and winners of chronic disturbance in an Ecuadorian tropical dry forest","fulltext":[{"header":"Introduction","content":"\u003cp\u003eUnderstanding how anthropogenic disturbance affects biodiversity of tropical forests is a critical demand due to the dramatic deforestation and degradation rates (Vitousek \u003cspan citationid=\"CR71\" class=\"CitationRef\"\u003e1994\u003c/span\u003e; Portillo-Quintero and Smith \u003cspan citationid=\"CR55\" class=\"CitationRef\"\u003e2018\u003c/span\u003e; Ribeiro et al. \u003cspan citationid=\"CR58\" class=\"CitationRef\"\u003e2019\u003c/span\u003e). Human-driven disturbance generates a sharp decline and homogenization of biodiversity (Mckinney and Lockwood \u003cspan citationid=\"CR38\" class=\"CitationRef\"\u003e1999\u003c/span\u003e; Olden et al. \u003cspan citationid=\"CR46\" class=\"CitationRef\"\u003e2004\u003c/span\u003e; L\u0026ocirc;bo et al. \u003cspan citationid=\"CR32\" class=\"CitationRef\"\u003e2011\u003c/span\u003e; Tabarelli et al. \u003cspan citationid=\"CR66\" class=\"CitationRef\"\u003e2012\u003c/span\u003e). This homogenization results from a reduction in the suitability of the habitat for certain species -losers- and a parallel increase in the abundance of others -winners- (Smart et al. \u003cspan citationid=\"CR64\" class=\"CitationRef\"\u003e2006\u003c/span\u003e; Tabarelli et al. \u003cspan citationid=\"CR66\" class=\"CitationRef\"\u003e2012\u003c/span\u003e), depending on their environmental tolerances and requirements (Cadotte et al. \u003cspan citationid=\"CR7\" class=\"CitationRef\"\u003e2011\u003c/span\u003e). Although the underlining paradigm is a taxonomic homogenization after degradation (Olden et al. \u003cspan citationid=\"CR47\" class=\"CitationRef\"\u003e2006\u003c/span\u003e; L\u0026ocirc;bo et al. \u003cspan citationid=\"CR32\" class=\"CitationRef\"\u003e2011\u003c/span\u003e), some authors suggested that it could also imply a functional simplification and convergence (Smart et al. \u003cspan citationid=\"CR64\" class=\"CitationRef\"\u003e2006\u003c/span\u003e), increasing the vulnerability of entire species groups with particular functional traits (Cadotte et al. \u003cspan citationid=\"CR7\" class=\"CitationRef\"\u003e2011\u003c/span\u003e; L\u0026oacute;pez-Mart\u0026iacute;nez et al. \u003cspan citationid=\"CR33\" class=\"CitationRef\"\u003e2013\u003c/span\u003e; Pessoa et al. \u003cspan citationid=\"CR53\" class=\"CitationRef\"\u003e2017\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eEvidence also shows that certain critical dimensions of the plant trait architecture, such as those related to wood tissue (Chave et al. \u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e2009\u003c/span\u003e) and to the leaf economic spectrum (Osnas et al. \u003cspan citationid=\"CR50\" class=\"CitationRef\"\u003e2013\u003c/span\u003e), suffer a drastic reduction in tropical forests after anthropogenic disturbance (Nunes-Nesi et al. \u003cspan citationid=\"CR44\" class=\"CitationRef\"\u003e2016\u003c/span\u003e; Sfair et al. \u003cspan citationid=\"CR60\" class=\"CitationRef\"\u003e2018\u003c/span\u003e). It is also expected that a third functional dimension of plant species related to dispersal and reproduction is also deeply affected by man-driven disturbance (Pessoa et al. \u003cspan citationid=\"CR54\" class=\"CitationRef\"\u003e2016\u003c/span\u003e; Pessoa et al. \u003cspan citationid=\"CR53\" class=\"CitationRef\"\u003e2017\u003c/span\u003e). Even more, it is known that large-fruited and large-seeded species are especially sensitive after perturbation (Tabarelli et al. \u003cspan citationid=\"CR65\" class=\"CitationRef\"\u003e2010\u003c/span\u003e; Magnago et al. \u003cspan citationid=\"CR34\" class=\"CitationRef\"\u003e2014\u003c/span\u003e) which would have dramatic implications for animal-plant interactions, and community dynamics (Galetti et al. \u003cspan citationid=\"CR18\" class=\"CitationRef\"\u003e2011\u003c/span\u003e; Pessoa et al. \u003cspan citationid=\"CR54\" class=\"CitationRef\"\u003e2016\u003c/span\u003e; Pessoa et al. \u003cspan citationid=\"CR53\" class=\"CitationRef\"\u003e2017\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eA considerable effort has been devoted to understanding the process of biodiversity loss after disturbance, including their functional and phylogenetic counterparts. However, most of those efforts have focused on deforestation and subsequent fragmentation as drivers of tropical forest diversity loss (Tabarelli et al. \u003cspan citationid=\"CR65\" class=\"CitationRef\"\u003e2010\u003c/span\u003e; L\u0026ocirc;bo et al. \u003cspan citationid=\"CR32\" class=\"CitationRef\"\u003e2011\u003c/span\u003e; Pessoa et al. \u003cspan citationid=\"CR53\" class=\"CitationRef\"\u003e2017\u003c/span\u003e; Zambrano et al. \u003cspan citationid=\"CR74\" class=\"CitationRef\"\u003e2019\u003c/span\u003e). However the effect of chronic disturbance (\u003cem\u003ei.e.\u003c/em\u003e small scale extensive livestock farming and coppicing) are by far less known, despite their importance at a global scale (Lalibert\u0026eacute; et al. \u003cspan citationid=\"CR29\" class=\"CitationRef\"\u003e2010\u003c/span\u003e). Chronic disturbance implies low-intensity but constant human pressures without a loss in the extent of vegetation (Singh \u003cspan citationid=\"CR63\" class=\"CitationRef\"\u003e1998\u003c/span\u003e). Often the forest extent is maintained whereas the biomass, structure, diversity, and ecosystem services decline (Lamb et al. \u003cspan citationid=\"CR30\" class=\"CitationRef\"\u003e2005\u003c/span\u003e; Peres et al. \u003cspan citationid=\"CR52\" class=\"CitationRef\"\u003e2006\u003c/span\u003e). This maintenance of the forest extension makes difficult to assess chronic disturbance, a problem that can be aggravated by the interaction of different pressures acting together, as well as the differences in relation to the initial primary productivity of the forests (Smart et al. \u003cspan citationid=\"CR64\" class=\"CitationRef\"\u003e2006\u003c/span\u003e; Sfair et al. \u003cspan citationid=\"CR60\" class=\"CitationRef\"\u003e2018\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eOne of the tropical ecosystems experiencing a higher pressure from chronic disturbance is the seasonally dry neotropical forests (SDTFs) (Ribeiro-Neto et al. \u003cspan citationid=\"CR59\" class=\"CitationRef\"\u003e2016\u003c/span\u003e; Ribeiro-Neto et al. \u003cspan citationid=\"CR59\" class=\"CitationRef\"\u003e2016\u003c/span\u003e; Arnan et al. \u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e2018\u003c/span\u003e; Jara-Guerrero et al. \u003cspan citationid=\"CR25\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). Chronic disturbance in SDTFs usually combines livestock grazing and small-scale timber extraction (Jara-Guerrero et al. \u003cspan citationid=\"CR26\" class=\"CitationRef\"\u003e2019\u003c/span\u003e), which intensify stress through increased solar radiation and ground-level temperature and reduced soil content of water and nutrients (Khurana and Singh \u003cspan citationid=\"CR27\" class=\"CitationRef\"\u003e2001\u003c/span\u003e; Lebrija-Trejos et al. \u003cspan citationid=\"CR31\" class=\"CitationRef\"\u003e2011\u003c/span\u003e; Maza-Villalobos et al. \u003cspan citationid=\"CR37\" class=\"CitationRef\"\u003e2022\u003c/span\u003e). Previous studies suggest that the stress induced in SDTFs by chronic disturbance is driving a loss of plant taxonomic diversity (Ribeiro-Neto et al. \u003cspan citationid=\"CR59\" class=\"CitationRef\"\u003e2016\u003c/span\u003e; Silva et al. \u003cspan citationid=\"CR62\" class=\"CitationRef\"\u003e2020\u003c/span\u003e; Jara-Guerrero et al. \u003cspan citationid=\"CR25\" class=\"CitationRef\"\u003e2021\u003c/span\u003e), with the exclusion of species with particular ecological functions (Sfair et al. \u003cspan citationid=\"CR60\" class=\"CitationRef\"\u003e2018\u003c/span\u003e). However, the chronic disturbance could drive different changes at the community level, depending on the type of pressure exerted and consequences on the environment. For instance, it is expected that the establishment of species in these disturbed forests will be defined by functional traits related to stress tolerance, mainly due to increased drought (Balvanera et al. \u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e2011\u003c/span\u003e; Fauset et al. \u003cspan citationid=\"CR16\" class=\"CitationRef\"\u003e2012\u003c/span\u003e). On the other hand, Silva et al. (\u003cspan citationid=\"CR62\" class=\"CitationRef\"\u003e2020\u003c/span\u003e) reported that the richness of species with fleshy fruits, and those with zoochoric dispersal were affected negatively by an increase in aridity but positively by the wood extraction or livestock grazing in SDTFs of the Caatinga region. Recent research at SDTFs in southwestern Ecuador showed that free-foraging goats in the forest disperse mainly legume seeds, particularly those of species with dry pods (Espinosa et al. \u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e2021\u003c/span\u003e); therefore, in chronically disturbed areas, where wild dispersers are almost excluded, those species with specialized traits for genuine dispersal by animals \u0026ndash; i.e., fleshy fruits \u0026ndash; may be adversely affected. On the other hand, Maza-Villalobos et al. (\u003cspan citationid=\"CR37\" class=\"CitationRef\"\u003e2022\u003c/span\u003e) reported for SDTFs of Mexico that the presence of cattle negatively affected the size and weight of fruits, and the seed number per fruit, while the weight and size of seeds were positively affected. Considered collectively, this evidence suggests that chronic disturbance and aridity interact in complex ways, including synergistically (Arnan et al. \u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e2018\u003c/span\u003e), making predictions very difficult. Therefore, it seems necessary to clarify to what extent some functional traits are driving this plant diversity loss and functional homogenization because of chronic disturbance, and their effects at local scales.\u003c/p\u003e \u003cp\u003eSDTFs in Ecuador show a significant loss of tree diversity associated with chronic disturbance (Cueva Ortiz et al. \u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e2019\u003c/span\u003e; Jara-Guerrero et al. \u003cspan citationid=\"CR25\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). Thus, we are interested in assessing whether these changes in plant diversity generate a loss of functional diversity associated with seed dispersal, and the potential effects on the resource availability for wildlife. With this in mind, we addressed the following specific questions; i) how does the abundance of species with particular dispersal traits change with chronic disturbance? ii) Are these changes in abundance the outcome of an environmental filtering on species with particular functional traits? iii) What is the impact of those changes in the abundance and diversity of functional traits on the access to resources by wildlife? We hypothesized that chronic disturbance limits the establishment of plants with fleshy fruits, large seeds, and dispersed by animals, because of their short period of seed viability, high water and nutrient requirements, and limitation of seed dispersers to forage in disturbed areas (Ribeiro et al. \u003cspan citationid=\"CR57\" class=\"CitationRef\"\u003e2015\u003c/span\u003e). Consequently, we expected that the variety and distribution of functional trait values, \u003cem\u003ei.e.\u003c/em\u003e the functional diversity of traits of fruits and seeds, will be negatively affected by chronic disturbance. Because trees show a higher loss of species richness than shrub species (Jara-Guerrero et al. \u003cspan citationid=\"CR25\" class=\"CitationRef\"\u003e2021\u003c/span\u003e), these effects should be stronger in the case of trees than when the entire plant community, including trees and shrubs, is evaluated. Although the effects of chronic disturbance on shrubs are less understood, this group may be favored by low and medium levels of chronic disturbance (Jara-Guerrero et al. \u003cspan citationid=\"CR25\" class=\"CitationRef\"\u003e2021\u003c/span\u003e) because of the different and ampler requirements of water and light compared to trees (Niinemets \u003cspan citationid=\"CR43\" class=\"CitationRef\"\u003e1996\u003c/span\u003e). Finally, in SDTFs, where more than half of woody species depends on animals for the seed dispersal service (Jara-Guerrero et al. \u003cspan citationid=\"CR22\" class=\"CitationRef\"\u003e2011\u003c/span\u003e), the changes in functional diversity of the dispersal and reproductive traits have implications for the dynamics of the entire ecosystem triggering cascade effects (Cadotte et al. \u003cspan citationid=\"CR7\" class=\"CitationRef\"\u003e2011\u003c/span\u003e; L\u0026oacute;pez-Mart\u0026iacute;nez et al. \u003cspan citationid=\"CR33\" class=\"CitationRef\"\u003e2013\u003c/span\u003e; Pessoa et al. \u003cspan citationid=\"CR53\" class=\"CitationRef\"\u003e2017\u003c/span\u003e).\u003c/p\u003e"},{"header":"Materials and Methods","content":"\u003cdiv id=\"Sec3\" class=\"Section2\"\u003e \u003ch2\u003eStudy area\u003c/h2\u003e \u003cp\u003eOur study was conducted in Southwestern Ecuador (Loja province, Zapotillo, Macar\u0026aacute; and Celica counties; between latitudes 4\u0026deg;19'39 \" and 4\u0026deg;01'40\" S and between longitudes 80\u0026deg;19'00 \" and 79\u0026deg;41'40\" W). This is part of the Tumbesian region and comprises some of the largest and best-preserved remnants of SDTFs. The altitude ranges from 120 to 1100 m a.s.l. The annual mean temperature is between 20\u0026deg; and 26\u0026deg; C, and the annual mean precipitation ranges from 300 to 700 mm (Cueva Ortiz et al. \u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e2019\u003c/span\u003e). There is a dry season from May to November and a rainy season from December to April. Dominant tree species were \u003cem\u003eCochlospermum vitifolium\u003c/em\u003e (Cochlospermaceae); \u003cem\u003eHandroanthus chrysanthus\u003c/em\u003e and \u003cem\u003eH. bilbergii\u003c/em\u003e (Bignoniacea); \u003cem\u003eCeiba trichystandra\u003c/em\u003e, \u003cem\u003eEriotheca ruizii\u003c/em\u003e (Bombacaceae); \u003cem\u003eGuazuma ulmifolia\u003c/em\u003e (Malvaceae) and \u003cem\u003eMuntingia calabura\u003c/em\u003e (Muntingiaceae) (Cueva Ortiz et al. \u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e2019\u003c/span\u003e). These forest remnants are mainly used for grazing of goats and cattle and sporadic wood extraction (Jara-Guerrero et al. \u003cspan citationid=\"CR26\" class=\"CitationRef\"\u003e2019\u003c/span\u003e; Cueva-Ortiz et al. \u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e2020\u003c/span\u003e; Jara-Guerrero et al. \u003cspan citationid=\"CR25\" class=\"CitationRef\"\u003e2021\u003c/span\u003e; Pati\u0026ntilde;o et al. \u003cspan citationid=\"CR51\" class=\"CitationRef\"\u003e2021\u003c/span\u003e; Espinosa et al. \u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e2021\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eAlthough the animal community of seed dispersers has not been extensively studied, this area hosts some potential seed dispersers (Valle et al. \u003cspan citationid=\"CR68\" class=\"CitationRef\"\u003e2021\u003c/span\u003e) such as at least two frugivorous bat species (\u003cem\u003eArtibeus fraterculus, Sturnira bakeri\u003c/em\u003e) and other two omnivorous bats (\u003cem\u003eLophostoma occidentalis, Phyllostomus discolor\u003c/em\u003e) (Tirira et al. \u003cspan citationid=\"CR67\" class=\"CitationRef\"\u003e2011\u003c/span\u003e). Two deer species that inhabit this SDTFs have also been reported feeding fruits, \u003cem\u003eOdocoileus virginianus\u003c/em\u003e (Tirira et al. \u003cspan citationid=\"CR67\" class=\"CitationRef\"\u003e2011\u003c/span\u003e; Jara-Guerrero et al. \u003cspan citationid=\"CR23\" class=\"CitationRef\"\u003e2018\u003c/span\u003e) and \u003cem\u003eMazama americana\u003c/em\u003e (Boada and Roman \u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e2005\u003c/span\u003e; Tirira et al. \u003cspan citationid=\"CR67\" class=\"CitationRef\"\u003e2011\u003c/span\u003e). Other omnivores feeding on fruits are fox \u003cem\u003eLycalopex sechurae\u003c/em\u003e, \u003cem\u003ePecari tajacu\u003c/em\u003e and some rodents (e.g. \u003cem\u003eSciurus\u003c/em\u003e spp. and \u003cem\u003eProechimys decumanus\u003c/em\u003e) (Boada and Roman \u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e2005\u003c/span\u003e). Moreover, this area is widely recognized by the diversity of bird species, some of which are well-known for their potential as seed dispersers (Ord\u0026oacute;\u0026ntilde;ez-Delgado et al. \u003cspan citationid=\"CR49\" class=\"CitationRef\"\u003e2016\u003c/span\u003e).\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec4\" class=\"Section2\"\u003e \u003ch2\u003eData sampling\u003c/h2\u003e \u003cp\u003eWithin an area of 1800 Km\u003csup\u003e2\u003c/sup\u003e, we randomly selected 24 locations covering a wide gradient of chronic disturbance resulting from grazing and logging of SDTF over different periods and intensities of use (Jara-Guerrero et al. \u003cspan citationid=\"CR26\" class=\"CitationRef\"\u003e2019\u003c/span\u003e). In each locality, we placed an L-shape cluster of three plots of 60 x 60 m separated 200 m from each other. In these plots we recorded all trees with a diameter at breast height (DBH)\u0026thinsp;\u0026ge;\u0026thinsp;10 cm. Shrubs with DBH\u0026thinsp;\u0026ge;\u0026thinsp;5 cm were also registered in a sub-plot of 20 x 20 m established in one corner of each plot (see Cueva et al. 2019 for details). Plots covered an altitudinal range from 234 to 1037 m asl.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec5\" class=\"Section2\"\u003e \u003ch2\u003eMorphology and dispersal traits\u003c/h2\u003e \u003cp\u003eBetween January and June 2017, we collected fruits and seeds directly from fruiting trees. With these samples, we made a morphological characterization recording weight, length and width of fruits and seeds, number of seeds per fruit, and three qualitative traits: fruit type, fruit color and dispersal syndrome. We measured a minimum of 10 fruits and 50 seeds per species from at least five healthy individuals. We calculated the area of fruits and seeds as the area of an ellipse, \u003cem\u003ei.e.\u003c/em\u003e the product of \u003cem\u003ePi\u003c/em\u003e by the radius of the length and radius of the width. For those woody species that did not produce fruits during the study time traits were obtained from bibliographic information or collections of seeds stored in the germplasm bank of Universidad T\u0026eacute;cnica Particular de Loja. We assigned a color to fruits of each species taking as reference Wheelwright \u0026amp; Janson (\u003cspan citationid=\"CR73\" class=\"CitationRef\"\u003e1985\u003c/span\u003e) and Galetti et al. (\u003cspan citationid=\"CR18\" class=\"CitationRef\"\u003e2011\u003c/span\u003e), which consider nine colors according to human perception: black (including dark red), red (including pink), yellow, orange, brown, gray, green, white and blue (including purple). Following Van der Pijl (\u003cspan citationid=\"CR69\" class=\"CitationRef\"\u003e1969\u003c/span\u003e), we categorized all the species in three primary dispersal syndromes: anemochory (wind), zoochory (animals) and autochory (explosion or gravity) (see Table \u003cspan refid=\"MOESM1\" class=\"InternalRef\"\u003eS1\u003c/span\u003e for the dispersal assignation). Lately and based on bibliographic information and personal observations we assigned each of these zoochorous species to a group of dispersers: birds, bats, non-ungulate mammals, ungulate mammals and reptiles (Table \u003cspan refid=\"MOESM2\" class=\"InternalRef\"\u003eS2\u003c/span\u003e).\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec6\" class=\"Section2\"\u003e \u003ch2\u003eData analysis\u003c/h2\u003e \u003cp\u003eChronic disturbance was defined based on three variables known to be a surrogate of anthropogenic perturbation: (1) distance to the nearest human settlements, which vary from hamlets to villages. Considering that the free foraging activities of the goats intensify in the surroundings of the human settlements, the increase in the distance implies less disturbance (Martorell and Peters \u003cspan citationid=\"CR36\" class=\"CitationRef\"\u003e2005\u003c/span\u003e; Cueva Ortiz et al. \u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e2019\u003c/span\u003e). (2) Biomass of goats feces in the plot (Martorell and Peters \u003cspan citationid=\"CR36\" class=\"CitationRef\"\u003e2005\u003c/span\u003e; Cueva Ortiz et al. \u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e2019\u003c/span\u003e), and (3) number of tree individuals with DBH\u0026thinsp;\u0026gt;\u0026thinsp;20 cm, because a decrease of big trees is indicative of high disturbance (M\u0026eacute;ndez-Toribio et al. \u003cspan citationid=\"CR40\" class=\"CitationRef\"\u003e2016\u003c/span\u003e). These predictors of chronic anthropogenic disturbance were used to adjust a principal component analysis (PCA). For the rest of analyses, we selected the first axis of the PCA as a chronic disturbance index.\u003c/p\u003e \u003cp\u003eTo evaluate the effects of chronic disturbance on the abundance of species with particular dispersal traits, we calculated the community weighted mean (CWM) (Garnier et al., 2004) by using the density of individuals for each species. For the qualitative traits, the CWM was calculated as the proportion of each trait\u0026rsquo;s level in the plot. To evaluate the changes of functional diversity with the chronic disturbance, we calculated three measures of functional diversity; functional richness (FRic), functional evenness (FEve) and functional divergence (FDis) (Vill\u0026eacute;ger et al. \u003cspan citationid=\"CR70\" class=\"CitationRef\"\u003e2008\u003c/span\u003e). These measures were calculated by using the density of each species and were estimated both for the trees and also for the entire community, \u003cem\u003ei.e.\u003c/em\u003e trees and shrubs. Because the trees and shrubs were measured in a different sized area, we calculated the density per hectare for shrubs and trees separately and then pooled the data.\u003c/p\u003e \u003cp\u003eWe built generalized linear models for each trait by using the CWM and functional diversity as response variables, and the chronic disturbance index (CDI), elevation as a proxy of climate variation, and the interaction between chronic disturbance and elevation (CDI:E) as explanatory variables. We included the elevation as a covariate in our models to control the effects of climate on the plant community. We used elevation as a proxy of climate because it can provide a more accurate indication of local climatic variations than available climate grids (see Franklin et al. \u003cspan citationid=\"CR17\" class=\"CitationRef\"\u003e2019\u003c/span\u003e). Additionally, the correlation between changes in the plant community and elevation has been extensively acknowledged (Gallardo-Cruz et al. \u003cspan citationid=\"CR20\" class=\"CitationRef\"\u003e2009\u003c/span\u003e; Balvanera et al. \u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e2011\u003c/span\u003e; Espinosa et al. \u003cspan citationid=\"CR14\" class=\"CitationRef\"\u003e2011\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eFor the analysis of qualitative traits, we adjusted Generalized Linear Models (GLMs) using a binomial error distribution. For quantitative variables, we tested the model fit using Gamma and Gaussian error distributions, as not all variables showed a normal distribution. When using Gamma error distribution, we employed three link functions: square root, logarithmic, and inverse. We adjusted three models for each measured trait: i) complete model; it is a model with CDI, elevation and CDI:E, ii) model without interaction; CDI and elevation, and iii) reduced model; only CDI. For each model we used four error distribution structures; gamma error distribution with three link functions and the gaussian error distribution. We used the AIC statistic to detect the best adjustment among the 12 models.\u003c/p\u003e \u003cp\u003eTo evaluate the effects of chronic disturbance on the availability of fruits for wildlife, we applied generalized linear models by using the basal area and species richness of plants associated with different disperser groups as response variables. In order to standardize the variables for each disperser group, we divided the basal area of resources by the highest value of the plot. We followed the same procedure used to evaluate the best model in the dispersal trait analysis (see above) but using the quasipoisson error family for count data.\u003c/p\u003e \u003cp\u003eAll of the analyses were implemented in the R environment (R Core Team \u003cspan citationid=\"CR56\" class=\"CitationRef\"\u003e2019\u003c/span\u003e). We used the \u0026ldquo;rda\u0026rdquo; function from the \u0026ldquo;vegan\u0026rdquo; package (Oksanen et al. \u003cspan citationid=\"CR45\" class=\"CitationRef\"\u003e2018\u003c/span\u003e) to adjust the PCA. The functional diversity measures were calculated through the \u0026ldquo;dbFD\u0026rdquo; of the \u0026ldquo;FD\u0026rdquo; package (Lalibert\u0026eacute; and Legendre \u003cspan citationid=\"CR28\" class=\"CitationRef\"\u003e2010\u003c/span\u003e).\u003c/p\u003e \u003c/div\u003e"},{"header":"Results","content":"\u003cp\u003eFrom the 100 woody species recorded in the plots, we obtained data for the 72 species distributed in 33 families and 59 genera. These species represented 74% of the total abundance and 64% of the basal area of woody species in the study area. The families that presented the highest number of species and genera were: Fabaceae (22 species, 17 genera) and Malvaceae (6 species, 4 genera). Dry fruits represented the 64% (46 species), and fleshy fruits represented the other 36% (26 species). We distinguished seven types of fruits, the most common were pods (n\u0026thinsp;=\u0026thinsp;18, 25%) and capsules (n\u0026thinsp;=\u0026thinsp;15, 21%) related to autochory and anemochory. Other types of fruits were berries (n\u0026thinsp;=\u0026thinsp;11, 15%), drupes (n\u0026thinsp;=\u0026thinsp;13, 17%), samara (n\u0026thinsp;=\u0026thinsp;8, 11%), in a smaller proportion achene (n\u0026thinsp;=\u0026thinsp;5, 7%) and, syconium (n\u0026thinsp;=\u0026thinsp;2, 3%). In addition, eight colors were recognized among fruits, being brown fruits the most common among the species (n\u0026thinsp;=\u0026thinsp;36, 50%), followed by the yellow ones (n\u0026thinsp;=\u0026thinsp;10, 14%), and green (n\u0026thinsp;=\u0026thinsp;9, 14%). The dominant dispersal syndrome was zoochory (n\u0026thinsp;=\u0026thinsp;33, 45%), followed by anemochory (n\u0026thinsp;=\u0026thinsp;23, 31%) and autochory in smaller proportion (n\u0026thinsp;=\u0026thinsp;16, 22%). From the autochory group, 5 species have been reported to be secondarily dispersed by ungulates (see Table \u003cspan refid=\"MOESM2\" class=\"InternalRef\"\u003eS2\u003c/span\u003e). Most of the zoochorous species showed traits related to dispersal by birds (22 species) and non-ungulate mammals (17 species). Other zoochorous species presented traits related to dispersal by reptiles (13 species), micromammals (11 species) and ungulates (10 species, including those primarily autochorous) (see Table \u003cspan refid=\"MOESM2\" class=\"InternalRef\"\u003eS2\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eThe first PCA axis of the chronic disturbance variables explained the 54% of the variation, and was positively associated with the number of goat feces, and negatively with the distance to human settlements and density of large trees (Table \u003cspan refid=\"MOESM3\" class=\"InternalRef\"\u003eS3\u003c/span\u003e).\u003c/p\u003e \u003cdiv id=\"Sec8\" class=\"Section2\"\u003e \u003ch2\u003eFunctional traits related to seed dispersal\u003c/h2\u003e \u003cp\u003eThe proportion of fruit types was affected by chronic disturbance in different ways. Within trees, only achene was not affected by CDI, while pods increased and the rest reduced (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003e, Table \u003cspan refid=\"MOESM4\" class=\"InternalRef\"\u003eS4\u003c/span\u003e). Moreover, our models showed that those negative effects of CDI on the proportion of berries, capsules, samaras, and syconium were reduced as elevation increased (CDI:E positive effect). On the contrary, for pods, elevation reduced the positive effect of CDI (CDI:E negative effect). When we analyzed both trees and shrubs, the only change regarding trees was observed in berries and drupes, which did not show an effect of CDI on their proportions (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003e).\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cp\u003eRegarding the fruit color, the proportion of tree species with red, white, and yellow fruits was negatively affected by CDI, an effect that increased with elevation (CDI:E positive effect, Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e2\u003c/span\u003e, Table \u003cspan refid=\"MOESM4\" class=\"InternalRef\"\u003eS4\u003c/span\u003e). The proportion of species with brown fruits was positively affected by CDI, although reduced with elevation. When we analyzed trees and shrubs, the pattern on brown fruits was the opposite. For black and green fruits, the effect of CDI changed from non-significant for trees to significant for shrubs and trees, being negative for black and positive for green ones. Additionally, orange fruits were positively affected by CDI (Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e2\u003c/span\u003e).\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cp\u003eWe found that CDI affected significantly and positively the proportion of autochorous trees, and negatively that of zoochorous species, while anemochorous tree species showed no effects (Fig.\u0026nbsp;\u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e3\u003c/span\u003ea, Table \u003cspan refid=\"MOESM4\" class=\"InternalRef\"\u003eS4\u003c/span\u003e). At higher elevation the positive effect of chronic disturbance on the proportion of autochorous trees increased (CDI:E positive effect). The CDI did not affect autochorous species when combining tree and shrub species, while the negative effect on zoochorous species found for trees turned positive. Positive effect on zoochory was reduced with elevation (CDI:E negative effect, Fig.\u0026nbsp;\u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e3\u003c/span\u003ea).\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cp\u003eWe observed a significant and negative effect of chronic disturbance on fruit weight and seeds per fruit, both for trees and shrub and trees together. The negative effect of chronic disturbance reduced with elevation, except for fruit weight of trees (Fig.\u0026nbsp;\u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e3\u003c/span\u003eb). Seed area of shrubs and trees was significant and negatively affected by chronic disturbance, with a weaker effect with elevation (CDI:E positive effect, Fig.\u0026nbsp;\u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e3\u003c/span\u003ec).\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec9\" class=\"Section2\"\u003e \u003ch2\u003eChanges in dispersal functional diversity\u003c/h2\u003e \u003cp\u003eChronic disturbance significantly affected functional diversity in its different components. FRic and FEve of fruit color, and FDis of fruit type were affected significantly and negatively by chronic disturbance (Fig.\u0026nbsp;\u003cspan refid=\"Fig4\" class=\"InternalRef\"\u003e4\u003c/span\u003ea, Table \u003cspan refid=\"MOESM4\" class=\"InternalRef\"\u003eS4\u003c/span\u003e), being these effects stronger at low elevations (CDI:E positive effect). The CDI also affected positively the FEve of fruit type and dispersal syndrome (Fig.\u0026nbsp;\u003cspan refid=\"Fig4\" class=\"InternalRef\"\u003e4\u003c/span\u003ea, Table \u003cspan refid=\"MOESM4\" class=\"InternalRef\"\u003eS4\u003c/span\u003e). When analyzing trees and shrubs together, the positive effect of CDI changed to negative for FEve of fruit type and dispersal syndrome.\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cp\u003eModels for quantitative fruit and seed traits (Fig.\u0026nbsp;\u003cspan refid=\"Fig5\" class=\"InternalRef\"\u003e5\u003c/span\u003e, Table \u003cspan refid=\"MOESM4\" class=\"InternalRef\"\u003eS4\u003c/span\u003e) showed that chronic disturbance negatively affected the FRic of fruit area, as well as FEve and FDis of seed number per fruit and seed weight. The FDis of seed area also showed a negative effect of CDI. These effects of CDI were similar when analysing the trees and shrubs together, except for FEve of seed area and FDis for seed weight, with a significant and negative effect on seed area and no significant effect on seed weight.\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec10\" class=\"Section2\"\u003e \u003ch2\u003eChanges in fruit availability for frugivorous groups\u003c/h2\u003e \u003cp\u003eChronic disturbance negatively affected the species richness of tree species dispersed by birds, reptiles, and non-ungulate mammals (Fig.\u0026nbsp;\u003cspan refid=\"Fig6\" class=\"InternalRef\"\u003e6\u003c/span\u003e, Table \u003cspan refid=\"MOESM5\" class=\"InternalRef\"\u003eS5\u003c/span\u003e). Those effects were stronger at lower elevations. When considering tree and shrubs together, these effects remained for species dispersed by birds and non-ungulate mammals, while the effects on species dispersed by reptiles disappeared. On the contrary, the richness of species dispersed by micromammals increased with the disturbance.\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cp\u003eChronic disturbance negatively affected the abundance of trees dispersed by birds, non-ungulate mammals, and ungulates. For species dispersed by non-ungulates mammals, this effect was stronger at lower elevations. When analyzing trees and shrubs together, the negative effect of chronic disturbance on the abundance of species dispersed by birds remained, although it was stronger at lower elevations (CDI:E positive effect). On the contrary, the negative effect on trees dispersed by ungulates and non-ungulate mammals was diluted. On the other hand, the effect of chronic disturbance on species dispersed by micromammals and reptiles became significant and negative (Fig.\u0026nbsp;\u003cspan refid=\"Fig7\" class=\"InternalRef\"\u003e7\u003c/span\u003e).\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003c/div\u003e"},{"header":"Discussion","content":"\u003cp\u003eSeasonal tropical dry forests are highly endangered due to chronic anthropogenic disturbance (Singh \u003cspan citationid=\"CR63\" class=\"CitationRef\"\u003e1998\u003c/span\u003e; Miles et al. \u003cspan citationid=\"CR41\" class=\"CitationRef\"\u003e2006\u003c/span\u003e; Oliveira et al. \u003cspan citationid=\"CR48\" class=\"CitationRef\"\u003e2017\u003c/span\u003e). Although the reach and spatial extension of this chronic disturbance are not easy to assess, it is known that forests suffering this pressure support lower species richness than less disturbed forests (Ribeiro et al. \u003cspan citationid=\"CR57\" class=\"CitationRef\"\u003e2015\u003c/span\u003e; Ribeiro-Neto et al. \u003cspan citationid=\"CR59\" class=\"CitationRef\"\u003e2016\u003c/span\u003e; Sfair et al. \u003cspan citationid=\"CR60\" class=\"CitationRef\"\u003e2018\u003c/span\u003e; Cueva Ortiz et al. \u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e2019\u003c/span\u003e; Jara-Guerrero et al. \u003cspan citationid=\"CR25\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). Our results revealed that a reduction in the presence and abundance of species with particular seed dispersal traits accompanies this loss of woody richness. This is especially true in the tree assemblage, while shrubs show little or no effect on the variety and abundance of seed dispersal traits. In this way, the shrubs could temporally soften the chronic disturbance effects on the availability and diversity of resources for wildlife that depend on them for their food. Additionally, those areas with lower water availability (i.e. located at lower elevations), support the strongest effects of chronic disturbance on the abundance and diversity of functional traits. Previous studies indicated that the loss of forest species generated by chronic disturbance is initially defined by the loss of species with vegetative traits that allow the avoidance of water loss, such as hard and small leaves (Sfair et al. \u003cspan citationid=\"CR60\" class=\"CitationRef\"\u003e2018\u003c/span\u003e; Ribeiro et al. \u003cspan citationid=\"CR58\" class=\"CitationRef\"\u003e2019\u003c/span\u003e). Additionally, there is pressure from livestock, especially goats, a generalist herbivore, that controls the recruitment of new plants (Weng et al. \u003cspan citationid=\"CR72\" class=\"CitationRef\"\u003e2017\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eAs hypothesized, chronic disturbance also affects the structure and composition of the vegetation by filtering certain traits associated with dispersal, limiting the establishment of species with more expensive fruits, associated with dispersion by animals. In this way, the pressures that generate the disturbance would be limiting the species regeneration through different paths, with the zoochorous species with fleshy fruits being the major losers. Although there is not microenvironmental information for our forests, some studies in SDTFs have reported that the loss of forest density associated with chronic disturbance increases stress due to greater exposure of the soil to radiation, which, together with greater evaporation, generates an increase in water stress (Galicia et al. \u003cspan citationid=\"CR19\" class=\"CitationRef\"\u003e1999\u003c/span\u003e; Balvanera et al. \u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e2002\u003c/span\u003e; Sfair et al. \u003cspan citationid=\"CR60\" class=\"CitationRef\"\u003e2018\u003c/span\u003e). Furthermore, there is evidence that these changes in microenvironmental conditions are related to the loss of most tree forest species (Jara-Guerrero et al. \u003cspan citationid=\"CR25\" class=\"CitationRef\"\u003e2021\u003c/span\u003e), changes in plant-animal interactions (C\u0026acirc;mara et al. \u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e2018\u003c/span\u003e; Melo et al. \u003cspan citationid=\"CR39\" class=\"CitationRef\"\u003e2023\u003c/span\u003e) and in species composition (Shahabuddin and Kumar \u003cspan citationid=\"CR61\" class=\"CitationRef\"\u003e2006\u003c/span\u003e), as well as with increases in genotoxic damage in birds (Cevallos-Solorzano et al. \u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e2023\u003c/span\u003e). Similarly, micro-environmental changes behind chronic disturbance can limit plant access to essential resources required for producing expensive fruits, thereby reducing their persistence in disturbed areas. In this line, more studies are needed to evaluate the impact of chronic disturbance on fruit production and clarify the process behind, either the abundance of individuals bearing fruits or the per capita fruit production (Pessoa et al. \u003cspan citationid=\"CR54\" class=\"CitationRef\"\u003e2016\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eOn the other hand, autochorous woody species were the winners. This result is not a surprise since autochorous species have been shown to be opportunistic pioneers and, consequently, more common in disturbed habitats (Hilje et al. \u003cspan citationid=\"CR21\" class=\"CitationRef\"\u003e2015\u003c/span\u003e), but also some of them are secondarily dispersed by goats (Espinosa et al. \u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). In our study area, most of autochorous species are legumes with seeds covered by hard coats (Jara-Guerrero et al. \u003cspan citationid=\"CR22\" class=\"CitationRef\"\u003e2011\u003c/span\u003e; Jara-Guerrero et al. \u003cspan citationid=\"CR24\" class=\"CitationRef\"\u003e2020\u003c/span\u003e) that led them to tolerate drought and survive not only the dry season but even larger periods waiting for adequate germination windows.\u003c/p\u003e \u003cp\u003eContrary to what we expected, chronic disturbance did not cause a generalized loss of functional richness; however, we found important changes in the functional configuration of the woody community related to shifts in functional evenness and divergence. Two important patterns emerge from these changes in the dominance of certain functional traits: on the one hand, an increase in functional evenness, with a reduction in functional dispersion. This pattern suggests that the negative effects observed occur on dominant characters such as capsules and samaras, which generally have anemochorous dispersion. Anemochorous species dominate SDTF, representing 52% of the abundance of woody plants (Jara-Guerrero et al. \u003cspan citationid=\"CR22\" class=\"CitationRef\"\u003e2011\u003c/span\u003e). On the other hand, chronic disturbance reduces functional evenness for some traits such as the color or size of fruits and seeds. In this case, the disturbance reduced fruit colors such as red, white, and yellow, frequently low-abundant and associated with zoochorous species, that in these forests represent 35% of the abundance of individuals (Jara-Guerrero et al. \u003cspan citationid=\"CR22\" class=\"CitationRef\"\u003e2011\u003c/span\u003e). According to Silva et al. (\u003cspan citationid=\"CR62\" class=\"CitationRef\"\u003e2020\u003c/span\u003e), chronic disturbance has resulted in changes in the functional structure of the Caatinga dry forests, leading to a reduction in the FDis of reproductive functional groups. Our results support this finding and suggest that chronic disturbance may similarly modify the functional structure of the woody plant community. However, it is worth noting that our study area represents an intermediate of the disturbance gradient, which is quite far from severely degraded areas in which trees are really scarce (Jara-Guerrero et al. \u003cspan citationid=\"CR26\" class=\"CitationRef\"\u003e2019\u003c/span\u003e). It is possible that in those areas with higher level of disturbance the filtering processes implies an even higher loss of functional richness.\u003c/p\u003e \u003cp\u003eShrubs play an interesting role by blurring the negative effects of chronic disturbance on the proportions of dispersal syndromes and fruit types, although the negative effect on fruit color remains. According to Jara-Guerrero et al. (\u003cspan citationid=\"CR25\" class=\"CitationRef\"\u003e2021\u003c/span\u003e), the openness of canopy in these forest leads to an increase in the density of shrubs which find an opportunity for actively recruit new individuals under more sunny conditions. Thus, to some extent, shrubs can help maintain a certain offer of dispersal traits in degraded forests.\u003c/p\u003e \u003cp\u003eAnother valuable finding is that the environmental filtering generated by chronic disturbance was stronger at lower elevation. In STDFs, lower elevations support the lower precipitation rates and higher mean temperatures (Cueva Ortiz et al. \u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e2019\u003c/span\u003e), being under higher risk in the face of climate change (Manchego et al. \u003cspan citationid=\"CR35\" class=\"CitationRef\"\u003e2017\u003c/span\u003e). Thus, those species with capsules, samaras and fleshy fruits, particularly those with red, yellow and white fruits can be lost with the chronic disturbance. Additionally, the availability of fruits associated to frugivorous species is also strongly affected at lower elevations.\u003c/p\u003e \u003cp\u003eSince a high diversity of functional fruit traits can sustain a larger community of frugivores (Galetti et al. \u003cspan citationid=\"CR18\" class=\"CitationRef\"\u003e2011\u003c/span\u003e; Morante-Filho et al. \u003cspan citationid=\"CR42\" class=\"CitationRef\"\u003e2018\u003c/span\u003e), the observed changes in the functional traits of the woody community have direct effects on the availability of resources for frugivorous species (Aizen and Feinsinger \u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e1994\u003c/span\u003e; Morante-Filho et al. \u003cspan citationid=\"CR42\" class=\"CitationRef\"\u003e2018\u003c/span\u003e) and represented a potential cascading effect on the whole ecosystem (Ribeiro-Neto et al. \u003cspan citationid=\"CR59\" class=\"CitationRef\"\u003e2016\u003c/span\u003e). This is especially significant for those species with red, white and yellow fruits, which are related to consumption by birds and mammals. Thus, the loss of these resources can explain the reduction of richness and abundance reported for some groups such as bats (Valle et al. \u003cspan citationid=\"CR68\" class=\"CitationRef\"\u003e2021\u003c/span\u003e) and birds (Almaz\u0026aacute;n-N\u0026uacute;\u0026ntilde;ez et al. \u003cspan citationid=\"CR2\" class=\"CitationRef\"\u003e2015\u003c/span\u003e) in these forests. On the other hand, we found a low effect of disturbance on the abundance and diversity of resources for ungulates. One of the main ungulates is the deer (\u003cem\u003eOdocoileus virginianus\u003c/em\u003e) which is known as a disperser of several species with pods that were thought to be only dispersed via autochory (Jara-Guerrero et al. \u003cspan citationid=\"CR23\" class=\"CitationRef\"\u003e2018\u003c/span\u003e). Thus, the abundance of pods in degraded areas can explain why the richness of species dispersed by ungulates were not affected by the chronic disturbance.\u003c/p\u003e \u003cp\u003eIn conclusion, species were filtered based on traits related to dispersal costs and their subsequent ability to withstand the environmental stress induced by the disturbance. The observed changes in vegetation have a direct effect on the availability of resources for frugivorous species, which in the medium term can generate a cascading effect on the whole forest ecosystem. Although zoochory and plant regeneration dynamics are recognized as key processes to ecosystem functionality, there is need to aid them in the development of a risk assessment approach for the ecosystem (Escribano-Avila et al. \u003cspan citationid=\"CR13\" class=\"CitationRef\"\u003e2017\u003c/span\u003e). Our work shows that disturbance is not only reducing biodiversity, but also the key processes are being modified. The knowledge of those processes would contribute to the application of effective management actions for the conservation of the SDTFs and their ecosystem services.\u003c/p\u003e"},{"header":"Declarations","content":"\u003cp\u003e \u003ch2\u003eConflict of interest:\u003c/h2\u003e \u003cp\u003eWe declare that we have no conflict of interest.\u003c/p\u003e \u003c/p\u003e \u003cp\u003e \u003cstrong\u003eEthics approval:\u003c/strong\u003e \u003cp\u003eNot applicable.\u003c/p\u003e \u003c/p\u003e \u003cp\u003e \u003cstrong\u003e \u003cb\u003eConsent to participate\u003c/b\u003e:\u003c/strong\u003e \u003cp\u003eNot applicable.\u003c/p\u003e \u003c/p\u003e \u003cp\u003e \u003cstrong\u003eConsent for publication:\u003c/strong\u003e \u003cp\u003eNot applicable.\u003c/p\u003e \u003c/p\u003e\u003cp\u003e \u003ch2\u003eAuthor contribution statement\u003c/h2\u003e \u003cp\u003eCE and AJ-G conceived and designed the research and analyzed the data. JC-E and JC collected the data. AJ-G, CE, AE and JC-E wrote the original draft. All co-authors discussed the results and commented and approved the final manuscript.\u003c/p\u003e \u003c/p\u003e \u003cp\u003e \u003cstrong\u003eFinancial interests\u003c/strong\u003e \u003cp\u003eThe authors declare they have no financial interests.\u003c/p\u003e \u003c/p\u003e\u003ch2\u003eFunding:\u003c/h2\u003e \u003cp\u003eThis work was supported by Universidad T\u0026eacute;cnica Particular de Loja (PROY_CCNN_1054), Secretar\u0026iacute;a de Educaci\u0026oacute;n Superior, Ciencia, Tecnolog\u0026iacute;a e Innovaci\u0026oacute;n (PIC-13-ETAPA-004, PIC-13-ETAPA-005), German Research Foundation DFG (project PAK 824/B3), and QuerPin (PID2021-126927NB-I00).\u003c/p\u003e\u003ch2\u003eAcknowledgments\u003c/h2\u003e \u003cp\u003eThe Ministerio del Ambiente y Agua del Ecuador provided us the research permit N\u0026deg; 002-2017-IC-FLO-NUTR-VS-UPN-DPAL-MAE for the collection of fruits and seeds in the study area.\u003c/p\u003e\u003ch2\u003eAvailability of data and material:\u003c/h2\u003e \u003cp\u003eThe datasets analyzed during the current study are available as supplementary material.\u003c/p\u003e\u003ch2\u003eCode availability:\u003c/h2\u003e \u003cp\u003eThe codes used during the current study are available from the corresponding author on reasonable request.\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\n\u003cli\u003eAizen MA, Feinsinger P (1994) Forest fragmentation, pollination, and plant reproduction in a chaco dry forest, Argentina. Ecology 75:330\u0026ndash;351. https://doi.org/10.2307/1939538\u003c/li\u003e\n\u003cli\u003eAlmaz\u0026aacute;n-N\u0026uacute;\u0026ntilde;ez RC, Arizmendi MDC, Eguiarte LE, Corcuera P (2015) Distribution of the community of frugivorous birds along a successional gradient in a tropical dry forest in south-western Mexico. J Trop Ecol 31:57\u0026ndash;68. https://doi.org/10.1017/S0266467414000601\u003c/li\u003e\n\u003cli\u003eArnan X, Arcoverde GB, Pie MR, Ribeiro-Neto JD, Leal IR (2018) Increased anthropogenic disturbance and aridity reduce phylogenetic and functional diversity of ant communities in Caatinga dry forest. Sci Total Environ 631\u0026ndash;632:429\u0026ndash;438. https://doi.org/10.1016/j.scitotenv.2018.03.037\u003c/li\u003e\n\u003cli\u003eBalvanera P, Lott E, Segura G, Siebe C, Islas A (2002) Patterns of \u0026beta;-diversity in a Mexican tropical dry forest. J Veg Sci 13:145\u0026ndash;158. https://doi.org/10.1111/j.1654-1103.2002.tb02034.x\u003c/li\u003e\n\u003cli\u003eBalvanera P, Quijas S, P\u0026eacute;rez-Jim\u0026eacute;nez A (2011) Distribution patterns of tropical dry forest trees along a mesoscale water availability gradient. Biotropica 43:414\u0026ndash;422. https://doi.org/10.1111/j.1744-7429.2010.00712.x\u003c/li\u003e\n\u003cli\u003eBoada C, Roman H (2005) Evaluaci\u0026oacute;n ecol\u0026oacute;gica r\u0026aacute;pida de la mastofauna en dos localidades de bosque seco en el occidente de la provincia de Loja. In: V\u0026aacute;zquez MA, Freire JF, Su\u0026aacute;rez L (eds) Biodiversidad en los bosques secos de la zona de Cerro Negro-Cazaderos, occidente de la provincia de Loja: un reporte de las evaluaciones ecol\u0026oacute;gicas y socioecon\u0026oacute;micas r\u0026aacute;pidas. EcoCiencia, MAE y Proyecto Bosque Seco, Quito, pp 73\u0026ndash;90\u003c/li\u003e\n\u003cli\u003eCadotte MW, Carscadden K, Mirotchnick N (2011) Beyond species: Functional diversity and the maintenance of ecological processes and services. J Appl Ecol 48:1079\u0026ndash;1087. https://doi.org/10.1111/j.1365-2664.2011.02048.x\u003c/li\u003e\n\u003cli\u003eC\u0026acirc;mara T, Leal IR, Bl\u0026uuml;thgen N, Oliveira FMP, Queiroz RT de, Arnan X (2018) Effects of chronic anthropogenic disturbance and rainfall on the specialization of ant\u0026ndash;plant mutualistic networks in the Caatinga, a Brazilian dry forest. J Anim Ecol 87:1022\u0026ndash;1033. https://doi.org/10.1111/1365-2656.12820\u003c/li\u003e\n\u003cli\u003eCevallos‐Solorzano G, Bailon‐Moscoso N, Ord\u0026oacute;\u0026ntilde;ez‐Delgado L, Jara P, Tom\u0026aacute;s G, Espinosa CI (2023) Chronic Degradation of Seasonally Dry Tropical Forests Increases the Incidence of Genotoxicity in Birds. GeoHealth 7:e2022GH000774. https://doi.org/10.1029/2022GH000774\u003c/li\u003e\n\u003cli\u003eChave J, Coomes D, Jansen S, Lewis SL, Swenson NG, Zanne AE (2009) Towards a worldwide wood economics spectrum. Ecol Lett 12:351\u0026ndash;366. https://doi.org/10.1111/j.1461-0248.2009.01285.x\u003c/li\u003e\n\u003cli\u003eCueva Ortiz J, Espinosa CI, Quiroz Dahik C, Aguirre Mendoza Z, Cueva Ortiz E, Gusman E, Weber M, Hildebrandt P (2019) Influence of anthropogenic factors on the diversity and structure of a dry forest in the central part of the Tumbesian region (Ecuador-Per\u0026uacute;). Forests 10:1\u0026ndash;22. https://doi.org/10.3390/f10010031\u003c/li\u003e\n\u003cli\u003eCueva-Ortiz J, Espinosa CI, Aguirre-Mendoza Z, Gusm\u0026aacute;n-Montalv\u0026aacute;n E, Weber M, Hildebrandt P (2020) Natural regeneration in the Tumbesian dry forest: identification of the drivers affecting abundance and diversity. Sci Rep 10:9786. https://doi.org/10.1038/s41598-020-66743-x\u003c/li\u003e\n\u003cli\u003eEscribano-Avila G, Cervera L, Ord\u0026oacute;\u0026ntilde;ez-Delgado L, Jara-Guerrero A, Amador L, Paladines B, Brice\u0026ntilde;o J, Par\u0026eacute;s-Jim\u0026eacute;nez V, Lizcano DJ, Duncan DH, Espinosa CI (2017) Biodiversity patterns and ecological processes in Neotropical dry forest: the need to connect research and management for long-term conservation. Neotrop Biodivers 3:107\u0026ndash;116. https://doi.org/10.1080/23766808.2017.1298495\u003c/li\u003e\n\u003cli\u003eEspinosa CI, Cabrera O, Luzuriaga A, Escudero A (2011) What factors affect diversity and species composition of endangered tumbesian dry forests in southern Ecuador? Biotropica 43:15\u0026ndash;22. https://doi.org/10.1111/j.1744-7429.2010.00665.x\u003c/li\u003e\n\u003cli\u003eEspinosa CI, Reyes C, Jara-Guerrero A (2021) Las cabras como dispersores de semillas: aportes y limitaciones para la regeneraci\u0026oacute;n del bosque tropical estacionalmente seco de Ecuador. Rev Biol Trop 69:557\u0026ndash;572. https://doi.org/10.15517/rbt.v69i2.45046\u003c/li\u003e\n\u003cli\u003eFauset S, Baker TR, Lewis SL, Feldpausch TR, Affum-Baffoe K, Foli EG, Hamer KC, Swaine MD (2012) Drought-induced shifts in the floristic and functional composition of tropical forests in Ghana. Ecol Lett 15:1120\u0026ndash;1129. https://doi.org/10.1111/j.1461-0248.2012.01834.x\u003c/li\u003e\n\u003cli\u003eFranklin J, Majure LC, Encarnaci\u0026oacute;n Y, Clase T, Almonte‐Espinosa H, Landestoy M, Kratter AW, Oswald JA, Soltis DE, Terrill RS, Steadman DW (2019) Changing ecological communities along an elevation gradient in seasonally dry tropical forest on Hispaniola (Sierra Mart\u0026iacute;n Garc\u0026iacute;a, Dominican Republic). Biotropica 51:802\u0026ndash;816. https://doi.org/10.1111/btp.12707\u003c/li\u003e\n\u003cli\u003eGaletti M, Pizo MA, Morellato LPC (2011) Diversity of functional traits of fleshy fruits in a species-rich Atlantic rain forest. Biota Neotropica 11:181\u0026ndash;193. https://doi.org/10.1590/s1676-06032011000100019\u003c/li\u003e\n\u003cli\u003eGalicia L, Lopez-Blanco J, Zarco-Arista A, Filips V, Garc\u0026iacute;a-Oliva F (1999) The relationship between solar radiation interception and soil content in a tropical deciduous forest in Mexico. Catena 36:153\u0026ndash;164. https://doi.org/10.1016/S0341-8162(98)00121-0\u003c/li\u003e\n\u003cli\u003eGallardo-Cruz JA, P\u0026eacute;rez-Garc\u0026iacute;a EA, Meave JA (2009) \u0026beta;-Diversity and vegetation structure as influenced by slope aspect and altitude in a seasonally dry tropical landscape. Landsc Ecol 24:473\u0026ndash;482. https://doi.org/10.1007/s10980-009-9332-1\u003c/li\u003e\n\u003cli\u003eHilje B, Calvo-Alvarado J, Jim\u0026eacute;nez-Rodr\u0026iacute;guez C, S\u0026aacute;nchez-Azofeifa A (2015) Tree species composition, breeding systems, and pollination and dispersal syndromes in three forest successional stages in a tropical dry forest in Mesoamerica. Trop Conserv Sci 8:76\u0026ndash;94. https://doi.org/10.1177/194008291500800109\u003c/li\u003e\n\u003cli\u003eJara-Guerrero A, De la Cruz M, M\u0026eacute;ndez M (2011) Seed dispersal spectrum of woody species in South Ecuadorian dry forests: environmental correlates and the effect of considering species abundance. Biotropica 43:722\u0026ndash;730. https://doi.org/10.1111/j.1744-7429.2011.00754.x\u003c/li\u003e\n\u003cli\u003eJara-Guerrero A, Escribano-Avila G, Espinosa CI, De la Cruz M, M\u0026eacute;ndez M (2018) White-tailed deer as the last megafauna dispersing seeds in Neotropical dry forests: the role of fruit and seed traits. Biotropica 50:169\u0026ndash;177. https://doi.org/10.1111/btp.12507\u003c/li\u003e\n\u003cli\u003eJara-Guerrero A, Espinosa CI, M\u0026eacute;ndez M, De la Cruz M, Escudero A (2020) Dispersal syndrome influences the match between seed rain and soil seed bank of woody species in a Neotropical dry forest. J Veg Sci 31:995\u0026ndash;1005. https://doi.org/10.1111/jvs.12894\u003c/li\u003e\n\u003cli\u003eJara-Guerrero A, Gonz\u0026aacute;lez-S\u0026aacute;nchez D, Escudero A, Espinosa CI (2021) Chronic disturbance in a tropical dry forest: Disentangling direct and indirect pathways behind the loss of plant richness. Front For Glob Change 4:723985. https://doi.org/10.3389/ffgc.2021.723985\u003c/li\u003e\n\u003cli\u003eJara-Guerrero A, Maldonado-Riofr\u0026iacute;o D, Espinosa CI, Duncan DH (2019) Beyond the blame game: a restoration pathway reconciles ecologists\u0026rsquo; and local leaders\u0026rsquo; divergent models of seasonally dry tropical forest degradation. Ecol Soc 24:22. https://doi.org/10.5751/ES-11142-240422\u003c/li\u003e\n\u003cli\u003eKhurana E, Singh JS (2001) Ecology of seed and seedling growth for conservation and restoration of tropical dry forest : A review. Environ Conserv 28:39\u0026ndash;52. https://doi.org/10.1017/S0376892901000042\u003c/li\u003e\n\u003cli\u003eLalibert\u0026eacute; E, Legendre P (2010) A distance-based framework for measuring functional diversity from multiple traits. Ecology 91:299\u0026ndash;305. https://doi.org/10.1890/08-2244.1\u003c/li\u003e\n\u003cli\u003eLalibert\u0026eacute; E, Wells JA, Declerck F, Metcalfe DJ, Catterall CP, Queiroz C, Aubin I, Bonser SP, Ding Y, Fraterrigo JM, McNamara S, Morgan JW, Merlos DS, Vesk PA, Mayfield MM (2010) Land-use intensification reduces functional redundancy and response diversity in plant communities. Ecol Lett 13:76\u0026ndash;86. https://doi.org/10.1111/j.1461-0248.2009.01403.x\u003c/li\u003e\n\u003cli\u003eLamb D, Erskine PD, Parrotta JA (2005) Restoration of Degraded Tropical Forest Landscapes. Science 310:1628\u0026ndash;1632. https://doi.org/10.1126/science.1111773\u003c/li\u003e\n\u003cli\u003eLebrija-Trejos E, P\u0026eacute;rez-Garc\u0026iacute;a EA, Meave JA, Poorter L, Bongers F (2011) Environmental changes during secondary succession in a tropical dry forest in Mexico. J Trop Ecol 27:477\u0026ndash;489. https://doi.org/10.1017/S0266467411000253\u003c/li\u003e\n\u003cli\u003eL\u0026ocirc;bo D, Le\u0026atilde;o T, Melo FPL, Santos AMM, Tabarelli M (2011) Forest fragmentation drives Atlantic forest of northeastern Brazil to biotic homogenization. Diversity and Distributions 17:287\u0026ndash;296. https://doi.org/10.1111/j.1472-4642.2010.00739.x\u003c/li\u003e\n\u003cli\u003eL\u0026oacute;pez-Mart\u0026iacute;nez JO, Sanaphre-Villanueva L, Dupuy JM, Hern\u0026aacute;ndez-Stefanoni JL, Meave JA, Gallardo-Cruz JA (2013) \u0026beta;-Diversity of functional groups of woody plants in a tropical dry forest in Yucatan. PloS one 8:e73660. https://doi.org/10.1371/journal.pone.0073660\u003c/li\u003e\n\u003cli\u003eMagnago LFS, Edwards DP, Edwards FA, Magrach A, Martins SV, Laurance WF (2014) Functional attributes change but functional richness is unchanged after fragmentation of Brazilian Atlantic forests. J Ecol 102:475\u0026ndash;485. https://doi.org/10.1111/1365-2745.12206\u003c/li\u003e\n\u003cli\u003eManchego CE, Hildebrandt P, Cueva J, Espinosa CI, Stimm B, G\u0026uuml;nter S (2017) Climate change versus deforestation: Implications for tree species distribution in the dry forests of southern Ecuador. PLoS ONE 12:1\u0026ndash;19. https://doi.org/10.1371/journal.pone.0190092\u003c/li\u003e\n\u003cli\u003eMartorell C, Peters EM (2005) The measurement of chronic disturbance and its effects on the threatened cactus Mammillaria pectinifera. Biol Conserv 124:199\u0026ndash;207. https://doi.org/10.1016/j.biocon.2005.01.025\u003c/li\u003e\n\u003cli\u003eMaza-Villalobos S, Garc\u0026iacute;a-Ram\u0026iacute;rez P, Endress BA, Lopez-Toledo L (2022) Plant functional traits under cattle grazing and fallow age scenarios in a tropical dry forest of Northwestern Mexico. Basic Appl Ecol. https://doi.org/10.1016/j.baae.2022.06.006\u003c/li\u003e\n\u003cli\u003eMckinney ML, Lockwood JL (1999) Biotic homogenization: a few winners replacing many losers in the next mass extinction. Trends Ecol Evol 14:450\u0026ndash;453. https://doi.org/10.1016/S0169-5347(99)01679-1\u003c/li\u003e\n\u003cli\u003eMelo DHA, Freitas AVL, Tabarelli M, Filgueiras BKC, Leal IR (2023) Aridity and chronic anthropogenic disturbance as organizing forces of fruit-feeding butterfly assemblages in a Caatinga dry forest. Biotropica 55:173\u0026ndash;184. https://doi.org/10.1111/btp.13173\u003c/li\u003e\n\u003cli\u003eM\u0026eacute;ndez-Toribio M, Meave JA, Zerme\u0026ntilde;o-Hern\u0026aacute;ndez I, Ibarra-Manr\u0026iacute;quez G (2016) Effects of slope aspect and topographic position on environmental variables, disturbance regime and tree community attributes in a seasonal tropical dry forest. J Veg Sci 27:1094\u0026ndash;1103. https://doi.org/10.1111/jvs.12455\u003c/li\u003e\n\u003cli\u003eMiles L, Newton AC, DeFries RS, Ravilious C, May I, Blyth S, Kapos V, Gordon JE (2006) A global overview of the conservation status of tropical dry forests. J Biogeogr 33:491\u0026ndash;505. https://doi.org/10.1111/j.1365-2699.2005.01424.x\u003c/li\u003e\n\u003cli\u003eMorante-Filho JC, Arroyo-Rodr\u0026iacute;guez V, Pessoa M de S, Cazetta E, Faria D (2018) Direct and cascading effects of landscape structure on tropical forest and non-forest frugivorous birds. Ecol Appl 28:2024\u0026ndash;2032. https://doi.org/10.1002/eap.1791\u003c/li\u003e\n\u003cli\u003eNiinemets \u0026Uuml; (1996) Plant growth-form alters the relationship between foliar morphology and species shade-tolerance ranking in temperate woody taxa. Vegetatio 124:145\u0026ndash;153. https://doi.org/10.1007/BF00045490\u003c/li\u003e\n\u003cli\u003eNunes-Nesi A, Nascimento VDL, De Oliveira Silva FM, Zs\u0026ouml;g\u0026ouml;n A, Ara\u0026uacute;jo WL, Sulpice R (2016) Natural genetic variation for morphological and molecular determinants of plant growth and yield. J Exp Bot 67:2989\u0026ndash;3001. https://doi.org/10.1093/jxb/erw124\u003c/li\u003e\n\u003cli\u003eOksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O\u0026rsquo;Hara RB, Simpson GL, Solymos P, Stevens HH, Wagner H, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O\u0026rsquo;Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2018) vegan: community ecology package\u003c/li\u003e\n\u003cli\u003eOlden JD, Poff NL, Douglas MR, Douglas ME, Fausch KD (2004) Ecological and evolutionary consequences of biotic homogenization. 19:18\u0026ndash;24. https://doi.org/10.1016/j.tree.2003.09.010\u003c/li\u003e\n\u003cli\u003eOlden JD, Poff NL, McKinney ML (2006) Forecasting faunal and floral homogenization associated with human population geography in North America. Biol Conserv 127:261\u0026ndash;271. https://doi.org/10.1016/j.biocon.2005.04.027\u003c/li\u003e\n\u003cli\u003eOliveira F, Ribeiro-Neto JD, Andersen AN, Leal IR (2017) Chronic anthropogenic disturbance as a secondary driver of ant community structure: Interactions with soil type in Brazilian Caatinga. Environ Conserv 44:115\u0026ndash;123. https://doi.org/10.1017/S0376892916000291\u003c/li\u003e\n\u003cli\u003eOrd\u0026oacute;\u0026ntilde;ez-Delgado L, Tom\u0026aacute;s G, Armijos-Ojeda D, Jara-Guerrero A, Cisneros R, Espinosa CI (2016) New contributions to the knowledge of birds in Tumbesian region; conservation implications of the Dry Forest Biosphere Reserve, Zapotillo, Ecuador. Ecosistemas 25. https://doi.org/10.7818/ECOS.2016.25-2.03\u003c/li\u003e\n\u003cli\u003eOsnas JLD, Lichstein JW, Reich PB, Pacala SW (2013) Global leaf trait relationships: Mass, area, and the leaf economics spectrum. Science 340:741\u0026ndash;744. https://doi.org/10.1126/science.1231574\u003c/li\u003e\n\u003cli\u003ePati\u0026ntilde;o J, Ram\u0026oacute;n P, Gusm\u0026aacute;n-Montalv\u0026aacute;n E, Escudero A, de la Cruz M (2021) Fencing promotes fast recovery of demographic processes after grazing-driven collapse in Bursera graveolens forests. For Ecol Manage 499:119592. https://doi.org/10.1016/j.foreco.2021.119592\u003c/li\u003e\n\u003cli\u003ePeres CA, Barlow J, Laurance WF (2006) Detecting anthropogenic disturbance in tropical forests. Trends Ecol Evol 21:227\u0026ndash;229. https://doi.org/10.1016/j.tree.2006.03.007\u003c/li\u003e\n\u003cli\u003ePessoa MS, Hambuckers A, Benchimol M, Rocha-Santos L, Bomfim JA, Faria D, Cazetta E (2017) Deforestation drives functional diversity and fruit quality changes in a tropical tree assemblage. Perspect Plant Ecol Evol Syst 28:78\u0026ndash;86. https://doi.org/10.1016/j.ppees.2017.09.001\u003c/li\u003e\n\u003cli\u003ePessoa MS, Rocha-Santos L, Talora DC, Faria D, Mariano-Neto E, Hambuckers A, Cazetta E (2016) Fruit biomass availability along a forest cover gradient. Biotropica 49:45\u0026ndash;55. https://doi.org/10.1111/btp.12359\u003c/li\u003e\n\u003cli\u003ePortillo-Quintero C, Smith V (2018) Emerging trends of tropical dry forests loss in North \u0026amp; Central America during 2001\u0026ndash;2013: The role of contextual and underlying drivers. Appl Geogr 94:58\u0026ndash;70. https://doi.org/10.1016/j.apgeog.2018.03.011\u003c/li\u003e\n\u003cli\u003eR Core Team (2019) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria\u003c/li\u003e\n\u003cli\u003eRibeiro EMS, Arroyo-Rodr\u0026iacute;guez V, Santos BA, Tabarelli M, Leal IR (2015) Chronic anthropogenic disturbance drives the biological impoverishment of the Brazilian Caatinga vegetation. J Appl Ecol 52:611\u0026ndash;620. https://doi.org/10.1111/1365-2664.12420\u003c/li\u003e\n\u003cli\u003eRibeiro EMS, Lohbeck M, Santos BA, Arroyo‐Rodr\u0026iacute;guez V, Tabarelli M, Leal IR (2019) Functional diversity and composition of Caatinga woody flora are negatively impacted by chronic anthropogenic disturbance. J Ecol 107:2291\u0026ndash;2302. https://doi.org/10.1111/1365-2745.13177\u003c/li\u003e\n\u003cli\u003eRibeiro-Neto JD, Arnan X, Tabarelli M, Leal IR (2016) Chronic anthropogenic disturbance causes homogenization of plant and ant communities in the Brazilian Caatinga. Biodivers Conserv 25:943\u0026ndash;956. https://doi.org/10.1007/s10531-016-1099-5\u003c/li\u003e\n\u003cli\u003eSfair JC, De Bello F, De Frana TQ, Baldauf C, Tabarelli M (2018) Chronic human disturbance affects plant trait distribution in a seasonally dry tropical forest. Environ Res Lett 13. https://doi.org/10.1088/1748-9326/aa9f5e\u003c/li\u003e\n\u003cli\u003eShahabuddin G, Kumar R (2006) Influence of anthropogenic disturbance on bird communities in a tropical dry forest: role of vegetation structure. Anim Conserv 9:404\u0026ndash;413. https://doi.org/10.1111/j.1469-1795.2006.00051.x\u003c/li\u003e\n\u003cli\u003eSilva JLS, Cruz-Neto O, Rito KF, Arnan X, Leal IR, Peres CA, Tabarelli M, Valentina Lopes A (2020) Divergent responses of plant reproductive strategies to chronic anthropogenic disturbance and aridity in the Caatinga dry forest. Sci Total Environ 704:135240. https://doi.org/10.1016/j.scitotenv.2019.135240\u003c/li\u003e\n\u003cli\u003eSingh SP (1998) Chronic disturbance, a principal cause of environmental degradation in developing countries. Envir Conserv 25:1\u0026ndash;2. https://doi.org/10.1017/S0376892998000010\u003c/li\u003e\n\u003cli\u003eSmart SM, Thompson K, Marrs RH, Le Duc MG, Maskell LC, Firbank LG (2006) Biotic homogenization and changes in species diversity across human-modified ecosystems. Proc R Soc B 273:2659\u0026ndash;2665. https://doi.org/10.1098/rspb.2006.3630\u003c/li\u003e\n\u003cli\u003eTabarelli M, Aguiar AV, Gir\u0026atilde;o LC, Peres CA, Lopes AV (2010) Effects of pioneer tree species hyperabundance on forest fragments in Northeastern Brazil. Conserv Biol 24:1654\u0026ndash;1663. https://doi.org/10.1111/j.1523-1739.2010.01529.x\u003c/li\u003e\n\u003cli\u003eTabarelli M, Peres CA, Melo FPL (2012) The \u0026ldquo;few winners and many losers\u0026rdquo; paradigm revisited: Emerging prospects for tropical forest biodiversity. Biol Conserv 155:136\u0026ndash;140. https://doi.org/10.1016/j.biocon.2012.06.020\u003c/li\u003e\n\u003cli\u003eTirira DG, Burneo SF, Boada CE, Lobos SE (2011) Mammalia, Chiroptera, Phyllostomidae, Lonchophylla hesperia G. M. Allen, 1908: second record of the Western Nectar Bat in Ecuador after 70 years. Check List 7:315. https://doi.org/10.15560/7.3.315\u003c/li\u003e\n\u003cli\u003eValle D, Griffith DM, Jara-Guerrero A, Armijos-Ojeda D, Espinosa CI (2021) A multifaceted approach to understanding bat community response to disturbance in a seasonally dry tropical forest. Sci Rep 11:5667. https://doi.org/10.1038/s41598-021-85066-z\u003c/li\u003e\n\u003cli\u003eVan Der Pijl L (1969) Principles of dispersal in higher plants. Springer-Verlag Berlin Heidelberg, New York\u003c/li\u003e\n\u003cli\u003eVill\u0026eacute;ger S, Mason NWH, Mouillot D (2008) New multidimensional functional diversity indices for a multifaceted framework in functional ecology. Ecology 89:2290\u0026ndash;2301. https://doi.org/10.1890/07-1206.1\u003c/li\u003e\n\u003cli\u003eVitousek P (1994) Beyond global warming: ecology and global change. Ecology 75:1861\u0026ndash;1876\u003c/li\u003e\n\u003cli\u003eWeng C-Y, Hsieh C, Su M-H (2017) Recruitment dynamics mediated by ungulate herbivory can affect species coexistence for tree seedling assemblages. TAIWANIA 62:283\u0026ndash;293. https://doi.org/10.6165/tai.2017.62.283\u003c/li\u003e\n\u003cli\u003eWheelwright NT, Janson CH (1985) Colors of fruit displays of bird-dispersed plants. Am Nat 126:777\u0026ndash;799\u003c/li\u003e\n\u003cli\u003eZambrano J, Garzon-Lopez CX, Yeager L, Fortunel C, Cordeiro NJ, Beckman NG (2019) The effects of habitat loss and fragmentation on plant functional traits and functional diversity: what do we know so far? Oecologia 191:505\u0026ndash;518. https://doi.org/10.1007/s00442-019-04505-x\u003c/li\u003e\n\u003c/ol\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":true,"highlight":"","institution":"","isAcceptedByJournal":false,"isAuthorSuppliedPdf":false,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true},"keywords":"drylands, functional diversity, frugivory, seed dispersal, dispersal syndrome","lastPublishedDoi":"10.21203/rs.3.rs-4469206/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-4469206/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003cp\u003eAlthough chronic disturbance is widely recognized as a main driver of biodiversity loss in tropical dry forests, their consequences beyond the taxonomic loss perspective (i.e the functional dimension of diversity) still need to be clarified, especially in those plant traits associated with dispersal. Here, we evaluated the effects of chronic disturbance on the functional diversity of a seasonally dry tropical forest, and their potential effects on the frugivores guild. We characterized eight plant traits related to seed dispersal and calculated the community weighted means and functional diversities for trees and the whole woody community. We used generalized linear models to evaluate the effects of the disturbance on these functional estimates in relation with the abundance and diversity of fruits as resources for wildlife. Our results revealed that, the dominance of plants with costly fruiting species was reduced with disturbance. Functional richness and divergence were reduced with the disturbance, mainly in the qualitative traits. Finally, the availability of resources was slightly different between groups of dispersers, observing a general pattern of reduction in the availability and richness of fruits with disturbance. Our results suggest that the changes in species richness and abundance are not random but the result of filtering on traits related to dispersal costs and their subsequent ability to withstand environmental stress. The observed changes in vegetation have a direct effect on the availability of resources for frugivorous species, which in the medium term can affect the woody species persistence and catalyze the woody species loss.\u003c/p\u003e","manuscriptTitle":"Fewer berries and more pods: losers and winners of chronic disturbance in an Ecuadorian tropical dry forest","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2024-06-12 08:06:28","doi":"10.21203/rs.3.rs-4469206/v1","editorialEvents":[{"type":"communityComments","content":0}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true}}],"origin":"","ownerIdentity":"3b70fe4b-3c70-49c4-a1a2-ca28a281c8b6","owner":[],"postedDate":"June 12th, 2024","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"posted","subjectAreas":[],"tags":[],"updatedAt":"2024-09-17T04:36:23+00:00","versionOfRecord":[],"versionCreatedAt":"2024-06-12 08:06:28","video":"","vorDoi":"","vorDoiUrl":"","workflowStages":[]},"version":"v1","identity":"rs-4469206","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-4469206","identity":"rs-4469206","version":["v1"]},"buildId":"qtupq5eGEP_6zYnWcrvyt","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}