Introduction
Animal-plant interactions are important for maintaining biodiversity and ecosystem functions (Jordano et al. Reference Jordano, Forget, Lambert, Böhning-Gaese, Traveset and Wright2011). Among vertebrates, mammals receive special attention given their important role in pollination and seed dispersal, which provides gene flow and helps in the proliferation of many plant species (Jordano et al. Reference Jordano, Garcia, Godoy and García-Castaño2007, Golin et al. Reference Golin, Santos-Filho and Pereira2011). Interactions between animals and plants are influenced by biological attributes, such as fruit biomass, that shape species interactions (Fuzessy et al. Reference Fuzessy, Janson and Silveira2018). At the same time, several biological characteristics of the species may constitute morphological or spatiotemporal barriers that limit some types of pairwise interactions, which are described as the ‘forbidden links’ hypothesis (Jordano et al. Reference Jordano, Bascompte and Olesen2003). Therefore, large fruits tend to be dispersed by large mammals, as they could not be dispersed by other animal groups due to the morphological restrictions inherent to small dispersers (Jordano et al. Reference Jordano, Garcia, Godoy and García-Castaño2007, Lim et al. Reference Lim, Svenning, Göldel, Faurby and Kissling2020).
Interaction networks have been used as tools to understand the complexity of ecological interactions and the influence of morphological traits and have been considered a powerful methodology that maps interactions, characterizes the functional roles of species within communities, the diversity of relationships established between frugivores and plants, and the importance of the species involved (Bascompte & Jordano Reference Bascompte and Jordano2007). Network analyses include interactions between species as an additional layer in ecological evaluations, resulting in great advances in understanding the establishment of biological communities in different ecosystems (Delmas et al. Reference Delmas, Besson, Brice, Burkle, Dalla Riva, Fortin, Gravel, Guimarães, Hembry, Newman, Olesen, Pires, Yeakel and Poisot2019). Recently, this approach has provided important information on the ecological role of vertebrates in seed dispersal (Vidal et al. Reference Vidal, Pires and Guimarães2013), in addition to revealing the drastic reduction in the abundance of the dispersers and changes in the functional roles of species (Galetti et al. Reference Galetti, Guevara, Cortes, Fadini, Von Matter, Leite, Labecca, Ribeiro, Carvalho, Collevatti, Pires, Guimaraes, Brancalion, Ribeiro and Jordano2013, Carreira et al. Reference Carreira, Dáttilo, Bruno, Percequillo, Ferraz and Galetti2020).
The use of the interaction network approach can help in conservation and restoration strategies, ensuring the best functioning of ecosystems (Harvey et al. Reference Harvey, Gounand, Ward and Altermatt2017, Raimundo et al. Reference Raimundo, Guimarães and Evans2018) and avoiding species extinctions (Carreira et al. Reference Carreira, Dáttilo, Bruno, Percequillo, Ferraz and Galetti2020). In this sense, the investigation of legally protected areas that can serve to define conservation strategies emerges as part of environmental planning for the maintenance of biodiversity and ecological processes in threatened ecosystems. These protected areas have remnants of natural vegetation that are important for the maintenance of biodiversity due to the existing complex structure (Sukma et al. Reference Sukma, Di Stefano, Swan and Sitters2019, Magioli et al. Reference Magioli, Barros, Chiarello, Galetti, Setz, Paglia, Abregoi, Ribeiro and Ovaskainen2021a, Magioli et al. Reference Magioli, Rios, Benchimol, Casanova, Ferreira, Rocha, Melo, Dias, Narezi, Crepaldi, Mendes, Nobre, Chiarello, García-Olaechea, Nobre, Devids, Cassano, Koike, Bernardo, Homem, Ferraz, Abreu, Cazetta, Lima, Bonfim, Lima, Prado, Santos, Nodari, Giovanelli, Nery, Faria, Ferreira, Gomes, Rodarte, Borges, Zuccolotto, Sarcinelli, Endo, Matsuda, Camargos and Morato2021b) and serve as stepping stones for connection with smaller fragments (Wintle et al. Reference Wintle, Kujala, Whitehead, Cameron, Veloz, Kukkala, Moilanen, Gordon, Lentini, Cadenhead and Bekessy2019). The low degree of human intervention in these areas allows for the occurrence of several groups of animals and plants, including a high diversity of mammals, which play an important role in seed dispersal, especially of plants that produce large fruits, that, due to morphological restrictions, have their seeds dispersed only by a specific set of mammals (Bello et al. Reference Bello, Galetti, Pizo, Magnago, Rocha, Lima, Peres, Ovaskainen and Jordano2015, Magioli et al. Reference Magioli, Barros, Chiarello, Galetti, Setz, Paglia, Abregoi, Ribeiro and Ovaskainen2021a).
Herein, we aim to describe the structure of the interaction network between frugivorous non-flying mammals and seven plant species that produce large fruits, in a protected savanna-forest mosaic in the Brazilian Cerrado, and to evaluate the individual contribution of the species involved. Our hypothesis is that the interaction network will present a modularity and non-nested structure, due to the existing biodiversity in the area (Santos-Filho & Silva Reference Santos-Filho and Silva2002, Santos-Filho et al. Reference Santos-Filho, Frieiro-Costa, Ignácio and Silva2012) and the presence of morphological barriers that restrict consumption of the large fruits evaluated, which can form a set of species closely linked within modules (Almeida-Neto et al. Reference Almeida-Neto, Guimaraes, Guimaraes, Loyola and Ulrich2008, Donatti et al. Reference Donatti, Guimarães, Galetti, Pizo, Marquitti and Dirzo2011). We also expect a positive relationship between mammalian biomass and its relevance in the context of mutualistic interactions, since larger and heavier species tend to have less morphological restrictions concerning the ingestion of large fruits, besides needing a greater energy demand, which drives the consumption of fruits (Donatti et al. Reference Donatti, Guimarães, Galetti, Pizo, Marquitti and Dirzo2011, Galetti & Dirzo Reference Galetti and Dirzo2013).
Materials and methods
Study area
The study was carried out at the Serra das Araras Ecological Station (hereafter SAEE), a Federal Integral Protection area that occupies an area of 28.700 hectares, between the municipalities of Porto Estrela and Cáceres in the State of Mato Grosso, Brazil (15°38’32.0” S 57°11’27.3” W) (Brasil 2016). The predominant climate is of the semi-humid hot tropical type, classified as megathermal Aw with two seasons: dry, which extends from May to October, and rainy from November to April, with annual precipitation around 1.500 mm and maximum average temperature of 30º C and minimum 20º C (Alvares et al. Reference Alvares, Stape, Sentelhas, Moraes Gonçalves and Sparovek2013). From a biogeographic perspective, the SAEE is located in an ecotone area with high biodiversity, inserted in the Cerrado and in contact with two other Brazilian biomes, the Amazon Forest and Pantanal wetland (Vitorino et al. Reference Vitorino, da Frota, Castrillon and Nunes2018). Inside the SAEE, the samples were taken in a vegetation mosaic of semi-deciduous seasonal forest, savanna woodland (cerrado sensu stricto) and gallery forest.
Data collection
In the SAEE, we collected data between September 2019 and September 2020, totalling 13 months of consecutive field expeditions. We used the photographic trapping methodology to record frugivorous mammal-fruit interactions because this method is efficient for sampling interactions between mammals and plants, and it is a minimally invasive methodology (Bogoni et al. Reference Bogoni, Graipel and Peroni2018). To record information about the interactions, camera traps were installed about 50 cm above the ground and attached to the trunks of the trees (Raíces et al. Reference Raíces, Ferreira, Mello and Bergallo2017, Carreira et al. Reference Carreira, Dáttilo, Bruno, Percequillo, Ferraz and Galetti2020). To record the frugivorous species with arboreal habits and their ecological interactions established there (Zhu et al. Reference Zhu, Li, Gregory, Wang, Ren, Zeng, Kang, Ding and Si2021, Moore et al. Reference Moore, Soanes, Balbuena, Beirne, Bowler, Carrasco-Rueda, Cheyne, Coutant, Pierre-Michel, Haysom, Houlihan, Olson, Lindshield, Martin, Tobler, Whitworth and Gregory2021), a wooden structure was created, in the centre of which the camera was fixed and hoisted so that it could be placed on the branches with the greatest abundance of fruits (Figure S1). The cameras remained active for 24 hours each day and were configured to record 10-second videos after motion detection, with intervals of five seconds between videos.
The criteria for selecting the trees to be sampled were to be in the fruiting period of the focal plant species (Table S2), to have fleshy and/or attractive fruits for frugivorous species with a size greater than 40 mm (Table S2), as described by Kuhlmann (Reference Kuhlmann2018), and presenting a minimum distance of 200 metres from the other individuals sampled. Thus, the cameras were installed focusing on seven species, viz., Hymenaea courbaril L. (Fabaceae), Genipa americana L. (Rubiaceae), Pouteria ramiflora (Mart.) Radlk. (Sapotaceae), Cordiera macrophylla (K.Schum.) Kuntze (Rubiaceae), Dipteryx alata Vogel (Fabaceae), Diospyros hispida ADC. (Ebenaceae), and Attalea speciosa Mart. ex Spreng. (Arecaceae).
We used 79 camera traps operating an average of 30 days on each individual of the seven plant species, in which we carried out a sampling effort of 28,344 hours of monitoring with the camera traps on the canopy and 68,288 hours on the ground, totalling 97,632 hours of sampling. The sampling effort conducted for each species was based on the number of individuals present in the area, as well as on species phenology (i.e., availability of fruits over time), so that the most representative species were sampled for a longer time (Table 1).
Table 1. Number of camera traps installed and sampling effort in hours per fruit plant species in the Serra das Araras Ecological Station.
We defined an interaction event (i.e., frequency) every time a mammal ingested or carried a fruit with its seed. We consider as independent records all interactions that were separated from each other by an interval equal to or greater than 30 seconds (sensu Carreira et al. Reference Carreira, Dáttilo, Bruno, Percequillo, Ferraz and Galetti2020). The taxonomic classification for plants and mammals followed Brazilian Flora (Brazil Flora 2020) and List of Mammals of Brazil (Abreu-Jr et al. Reference Abreu-Jr, Casali, Garbino, Loretto, Loss, Marmontel, Nascimento, Oliveira, Pavan and Tirelli2020), respectively. Non-flying mammals were separated into three categories: small mammals, with a body mass of up to one kilogram, medium-sized mammals, with body mass between one and seven kilograms (Chiarello Reference Chiarello2000), and large mammals with a body mass greater than seven kilograms (Emmons & Feer Reference Emmons and Feer1997). Information on the body mass of mammal species was obtained from Wilman et al. (Reference Wilman, Belmaker, Simpson, de la Rosa, Rivadeneira and Jetz2014).
Data analysis
For the analysis of interaction networks, we created a matrix weighted by the frequency of interactions collected in the field. All subsequent analyses were performed in the R software (R Development Core Team 2019). The completeness of our sampling was obtained by dividing the total number of observed links (which quantifies the pairing between species) by the estimated number via Chao 1 (Chao Reference Chao1984), using the iNEXT R-package (Hsieh et al. Reference Hsieh, Ma and Chao2020). We used the bipartite R-package (Dormann et al. Reference Dormann, Fruend and Gruber2020) to assess the network metrics: species richness of both mammals and plants (network size); number of interactions; number of links; nestedness, using NODF (Nestedness metric based on Overlap and Decreasing Fill, Almeida-Neto et al. Reference Almeida-Neto, Guimaraes, Guimaraes, Loyola and Ulrich2008) and wNODF (Weighted Nestedness metric based on Overlap and Decreasing Fill (Almeida-Neto & Ulrich Reference Almeida-Neto and Ulrich2011), that describes the pattern of interaction in which specialist species interact with a subset of generalist species; and modularity (Q w ), which identifies the presence of subsets of species that tend to interact more often with each other than with species from other subsets (Olesen et al. Reference Olesen, Bascompte, Dupont and Jordano2007). Specifically, for NODF, wNODF, and Q w , we evaluated the level of significance by comparing the results obtained with those of 1,000 random networks generated according to null models using the vaznull function, which maintains the same patterns of connectance and total marginals in relation to the observed matrix (Vázquez et al. Reference Vázquez, Melián, Williams, Blüthgen, Krasnov and Poulin2007, Dormann et al. Reference Dormann, Fruend and Gruber2020).
To determine the role of species in the network, we calculated the metrics Species Strength (SS), which quantifies the importance of each species based on the sum of the dependencies of their respective partners, and Closeness Centrality (CC), which measures the proximity of a species to all others, indicating the capacity of a species to act as a hub and increase the cohesion of the network (Martín González et al. Reference Martín González, Dalsgaard and Olesen2010, Delmas et al. Reference Delmas, Besson, Brice, Burkle, Dalla Riva, Fortin, Gravel, Guimarães, Hembry, Newman, Olesen, Pires, Yeakel and Poisot2019). Also, we verified the role of species in the modular structure, calculating the standardized pattern and connectivity of species between modules (c-score) and within their respective module (z-score). In this approach, species can be classified as peripheral, when they present low values of c- and z-score; connector, with high c-score and low z-score; module hub, with high z-score and low c-score and; network hub, with high c- and z-score values (Olesen et al. Reference Olesen, Bascompte, Dupont and Jordano2007). We determined the cut-off values of c- and z-score from 100 null matrices, following Dormann & Strauss (Reference Dormann and Strauss2014), which in our case was c- critical = 0.71 and z- critical = 1.86. Next, we performed a non-parametric Wilcoxon test to assess whether there was variation in the metrics at the species level (Species Strength, Closeness Centrality, c- and z-score) concerning different trophic levels (mammals and plants).
Additionally, we used a principal component analysis (PCA) to synthesize the role of mammals according to the metrics Species Strength, Closeness Centrality, and c- and z-score. The first principal component (PC1) explained 67% of the variation of the metrics and was used as the descriptor of the contributions exerted by the species. Thus, the higher the value of PC1, the greater the relevance of the species in the structuring of the network. Finally, we tested the mammals’ body mass (logarithmized for better fit) as a possible predictor to determine the role of these species in the network, using a linear model (LM).
Results
We identified 18 mammal species, grouped according to their body size into small (n = 5), medium (n = 9) and large (n = 4), interacting with seven plant species. Moreover, we recorded 515 frugivory events distributed into 48 links. The number of estimated links was 76, resulting in a sampling completeness of 63%. The interaction network evaluated was not significantly nested (NODF = 54.95, p > 0.05; wNODF 23.45, p > 0.05) but significantly modular (Qw = 0.43, p < 0.05). The mammal species that consumed fruits the most were Tapirus terrestris, Dicotyles tajacu, and Cuniculus paca, with 130, 69, and 66 frugivory events, respectively. Among the plant species with the largest number of interactions, Diospyros hispida (n = 164), Pouteria ramiflora (n = 129), and Dipteryx alata (n = 60) stand out (Figure 1). When evaluating the Species Strength metric, among the mammals Tapirus terrestris (2.15), Cuniculus paca (1.17), and Cerdocyon thous (0.76) had the highest ones, while among the plants the highest values were of Dipteryx alata (5.10), Cordiera macrophylla (3.45), and Diospyros hispida (3.32). Regarding the Closeness Centrality measure, the species that had the highest values were Tapirus terrestris (0.06), Mazama sp. (0.06), and Cerdocyon thous (0.06) among the mammals, and Dipteryx alata (0.14), Cordiera macrophylla (0.14), and Diospyros hispida (0.14) among the plants (Tables 2 and 3). By checking the role of species in the modular structure of the network, the mammals Tapirus terrestris (2.18), Cerdocyon thous (1.78) and Dicotyles tajacu (1.78) and the plants Cordiera macrophylla (0.90), Pouteria ramiflora (0.70), and Genipa americana (0.16) showed higher z-score values, while the mammals Tayassu pecari (0.67), Dicotyles tajacu (0.66), and Proechimys longicaudatus (0.64) and the plants Pouteria ramiflora (0.55), Hymenaea courbaril (0.38), and Diospyros hispida (0.36) showed higher c-scores. Tapirus terrestris was the only species in the network classified as a module hub, while the others were peripheral (Figure 2).
Figure 1. Interaction network between frugivorous mammals and plants that produce large fruits, in a Neotropical savanna in the Serra das Araras Ecological Station, Brazil. Modules are highlighted in the network by different colours, and the grey lines represent the interactions established between species of distinct modules.
Table 2. Network metrics evaluated at the species level (Species Strength, Closeness Centrality, c and z-score) of an interaction network between frugivorous mammals and plants that produce large fruits in a Neotropical savanna in the Serra das Araras Ecological Station, Brazil. Mammal body mass was obtained from Wilman et al. (Reference Wilman, Belmaker, Simpson, de la Rosa, Rivadeneira and Jetz2014). The species were separated into small mammals (weighing up to 1 gg), medium-sized mammals (1 to 7 kg) (Chiarello Reference Chiarello2000), and large mammals (more than 7 kg) (Emmons & Feer Reference Emmons and Feer1997).
Table 3. Network metrics evaluated at the species level (Species Strength and Closeness Centrality) for the group of plants of an interaction between frugivorous mammals and plants that produce large fruits, in a Neotropical savanna in the Serra das Araras Ecological Station, Brazil.
Figure 2. Species’ role in the modular structure of an interaction network between frugivorous mammals and plants that produce large fruits in a Neotropical savanna at the Serra das Araras Ecological Station, Brazil.
Using the Wilcoxon non-parametric test, we verified that there was significant variation between the two trophic levels for Closeness Centrality (W = 0; p < 0.001) and Species Strength (W = 8; p < 0.001), with plants assuming more central positions and having greater strength of interactions (Figure 3), but we did not observe significant variation for c and z-scores. We did not observe variation between the different trophic levels for c and z-scores (p > 0.05). In addition, we also identified that the body mass of mammalian species acts as an important predictor of the role that these species play in the network, with mammals with higher biomass being the most relevant (R2 adj = 0.40; p < 0.01) (Figure 4).
Figure 3. Significant variation in the species roles of an interaction network between frugivorous mammals and plants that produce large fruits, in a Neotropical savanna in the Serra das Araras Ecological Station, Brazil.
Figure 4. Body mass as a predictor of the role of mammals in the network structure. PC1 Index reflects the species-level metrics Species strength, Closeness centrality, and c- and z-scores.
Discussion
Our findings evidenced a modular but non-nested interaction network, with a high number of frugivorous mammals acting as potential dispersers for several plant species that produce large seeds. Furthermore, we found that disperser biomass was a good predictor of the role that these mammals play in the network. In the evaluated interaction network, the largest (heaviest) mammals were also the most important in the modular structure, assuming a central position and with a high value in the species strength.
We observed significant modularity values of the interaction network of mammals with large fruits in the Cerrado, as previously observed in the Atlantic Forest and Pantanal (Donatti et al. Reference Donatti, Guimarães, Galetti, Pizo, Marquitti and Dirzo2011, Carreira et al. Reference Carreira, Dáttilo, Bruno, Percequillo, Ferraz and Galetti2020), and a non-nested pattern, which was in accordance with our expectations. However, environmental variables such as phenology and plant abundance observed may have influenced the structuring of the interaction network, such as grouping into modules (Vázquez et al. Reference Vázquez, Melián, Williams, Blüthgen, Krasnov and Poulin2007, Encinas-viso et al. Reference Encinas-Viso, Revilla and Etienne2012, Machado-de-Souza et al. Reference Machado-de-Souza, Campos, Devoto and Varassin2019). Regarding modularity, still in line with what was observed for other megadiverse areas, we identified a system in which a set of species tends to interact more with each other than with species from other sets (Olesen et al. Reference Olesen, Bascompte, Dupont and Jordano2007), which results in a more robust and resilient system in the presence of possible indirect and direct impacts (Carreira et al. Reference Carreira, Dáttilo, Bruno, Percequillo, Ferraz and Galetti2020). In non-modular networks, as observed, for example, by Queiroz et al. (Reference Queiroz, Diniz, Vázquez, Quirino, Santos, Mello and Machado2021) and Naniwadekar et al. (Reference Naniwadekar, Chaplod, Datta, Rathore and Sridhar2019), environmental impacts are felt more intensely and can result in a cascade effect if a species disappears from the system, compromising the network of interactions (Olesen et al. Reference Olesen, Bascompte, Dupont and Jordano2007). Neotropical interaction networks tend to be less nested (Dugger et al. Reference Dugger, Blendinger, Böhning-Gaese, Chama, Correia, Dehling, Emer, Farwig, Fricke, Galetti, García, Grass, Heleno, Jacomassa, Moraes, Moran, Muñoz, Neuschulz, Nowak, Piratelli, Pizo, Quitián, Rogers, Ruggera, Saavedra, Sánchez, Sánchez, Santillán, Schabo, Silva, Timóteo, Traveset, Vollstädt and Schleuning2019), as we have observed, which may indicate that large-fruited plants attract different subsets of frugivorous species so that interactions are not necessarily occurring with more generalist mammals (Almeida-Neto et al. Reference Almeida-Neto, Guimaraes, Guimaraes, Loyola and Ulrich2008, Crestani et al. Reference Crestani, Mello and Cazetta2019, Naniwadekar et al. Reference Naniwadekar, Chaplod, Datta, Rathore and Sridhar2019).
Using species-level metrics, we highlight three important fruit trees for maintaining the structure of the interaction network: D. alata, C. macrophylla, and P. ramiflora. In addition, we showed that plants have greater strength of interaction and act as connectors in the system. In this sense, this group increases the connectivity and cohesion of the network, suggesting that it is the species that act to maintain the existing biodiversity and the dynamics of the ecosystem, thus avoiding extinctions (Cagua et al. Reference Cagua, Wootton and Stouffer2019, Ramos-Robles et al. Reference Ramos-Robles, Andresen and Díaz-Castelazo2018). These large-seeded plant species are categorized as attractive to fauna due to their high nutritional value (Kuhlmann Reference Kuhlmann2018) and make potential contributions to carbon storage (Bello et al. Reference Bello, Galetti, Pizo, Magnago, Rocha, Lima, Peres, Ovaskainen and Jordano2015). Also, they are important for the maintenance of the mammal community, including rare species for the region where the study was carried out, such as the Kinkajou (Potos flavus), which was recorded interacting with D. alata, this being the first record with documented evidence for the species in the SAEE (see Figure 1).
Our results demonstrate the importance of medium and large mammals in the evaluated interaction network with large fruits. Among the species, we can highlight three T. terrestris, C. thous and T. pecari, two of which are categorized as Vulnerable to Extinction at the national and international level (IUCN 2022) and considered important in other studies of ecological interactions (Donatti et al. Reference Donatti, Guimarães, Galetti, Pizo, Marquitti and Dirzo2011, Vidal et al. Reference Vidal, Pires and Guimarães2013, Bogoni et al. Reference Bogoni, Graipel and Peroni2018). Specifically, the tapir (Tapirus terrestris), identified as module hubs, as explained by Donatti et al. (Reference Donatti, Guimarães, Galetti, Pizo, Marquitti and Dirzo2011), interacts with a high diversity of plant species and stands out for the quality of seed dispersal over long distances (O’Farrill et al. Reference O’Farrill, Galetti and Campos-Arceiz2013, Jordano et al. Reference Jordano, Garcia, Godoy and García-Castaño2007, Fuzessy et al. Reference Fuzessy, Janson and Silveira2018). These results demonstrate the need for identifying the ecological functions performed by the species, such as frugivory and seed dispersal, given that extinctions can cause cascading effects in the system and compromise these ecosystem services (O’Farrill et al. Reference O’Farrill, Galetti and Campos-Arceiz2013, Vidal et al. Reference Vidal, Pires and Guimarães2013, Godínez-Alvarez et al. Reference Godínez-Alvarez, Ríos-Casanova and Peco2020). Regarding C. thous, this species was also mentioned as relevant in ecological interaction studies, especially in degraded ecosystems, due to its tolerance to environmental changes and ability to disperse seeds over long distances (Bogoni et al. Reference Bogoni, Graipel and Peroni2018).
Besides verifying the important species in the evaluated interaction network, we also showed that mammal biomass is an ecological determinant of the role that these species play in the network, with a positive and significant relationship with the metrics used in this study. These results support our hypothesis that large mammals provide a major contribution to network structure and fruit removal. Other studies observed similar results, as highlighted by Donatti et al. (Reference Donatti, Guimarães, Galetti, Pizo, Marquitti and Dirzo2011) in a system evaluated in the Pantanal, in which large frugivores interacted with many plants with fruits of different sizes. Therefore, large mammals are essential elements in the structure of frugivory networks (Palacio et al. Reference Palacio, Valderrama-Ardila and Kattan2016) and play a fundamental role in the processes of seed dispersal and recruitment (Donatti et al. Reference Donatti, Guimarães, Galetti, Pizo, Marquitti and Dirzo2011, Fuzessy et al. Reference Fuzessy, Janson and Silveira2018), including those of plants that produce large seeds, as shown in our study.
The disappearance of large mammals is one of the current problems of the Anthropocene and is the result of fragmentation, habitat loss, and hunting (Dirzo et al. Reference Dirzo, Young, Galetti, Ceballos, Isaac and Collen2014, Ripple et al. Reference Ripple, Newsome, Wolf, Dirzo, Everatt, Galetti, Hayward, Kerley, Levi, Lindsey, Macdonald, Malhi, Painter, Sandom, Terborgh and Valkenburgh2015). Defaunated ecosystems, where the large fauna is extinct, present showchanges in ecological processes (Young et al. Reference Young, McCauley, Galetti and Dirzo2016, Lim et al. Reference Lim, Svenning, Göldel, Faurby and Kissling2020) and in functional roles (Carreira et al. Reference Carreira, Dáttilo, Bruno, Percequillo, Ferraz and Galetti2020). This favours mesocarnivores and generalists at small scales (Ripple et al. Reference Ripple, Newsome, Wolf, Dirzo, Everatt, Galetti, Hayward, Kerley, Levi, Lindsey, Macdonald, Malhi, Painter, Sandom, Terborgh and Valkenburgh2015), increases seed predation (Galetti et al. Reference Galetti, Bovendorp and Guevara2015, Lacher et al. Reference Lacher, Davidson, Fleming, Gómez-Ruiz, McCracken, Owen-Smith, Peres and Vander Wall2019), and changes the carbon and nitrogen cycles (Bello et al. Reference Bello, Galetti, Pizo, Magnago, Rocha, Lima, Peres, Ovaskainen and Jordano2015, Villar et al. Reference Villar, Paz, Zipparro, Nazareth, Bulascoschi, Bakker and Galetti2020).
Body mass and species richness are related to ecosystem services and ecological function. Thus, the presence of large mammals in large remnants indicates the importance of preserving these areas (Magioli et al. Reference Magioli, Barros, Chiarello, Galetti, Setz, Paglia, Abregoi, Ribeiro and Ovaskainen2021a, Magioli et al. Reference Magioli, Rios, Benchimol, Casanova, Ferreira, Rocha, Melo, Dias, Narezi, Crepaldi, Mendes, Nobre, Chiarello, García-Olaechea, Nobre, Devids, Cassano, Koike, Bernardo, Homem, Ferraz, Abreu, Cazetta, Lima, Bonfim, Lima, Prado, Santos, Nodari, Giovanelli, Nery, Faria, Ferreira, Gomes, Rodarte, Borges, Zuccolotto, Sarcinelli, Endo, Matsuda, Camargos and Morato2021b). Therefore, our results emphasize the importance of conserving areas of Cerrado, to preserve species and promote the stability of ecological interactions (Ferreira et al. Reference Ferreira, Collen, Newbold, Oliveira, Pinheiro, Pinho, Rowcliffe and Carbone2020). Researches carried out in this context provide data that enable the implementation of efficient measures to keep communities viable and prevent extinctions (Carreira et al. Reference Carreira, Dáttilo, Bruno, Percequillo, Ferraz and Galetti2020), ensuring better ecological functioning (Harvey et al. Reference Harvey, Gounand, Ward and Altermatt2017, Raimundo et al. Reference Raimundo, Guimarães and Evans2018).
Conclusions
In summary, we highlight the importance of a protected environment in the savannas of the Neotropical region for the maintenance of interactions between species of the fauna and flora. In general, the seven observed plant species strongly contribute to the structure of the interaction network with non-flying mammals. We emphasize the importance of large mammals in this process, especially Tapirus terrestris, which is a threatened species. The disappearance of large mammals can harm the structure of interaction networks, mainly compromising the maintenance of plant species that have large fruits and, consequently, other ecosystem services. Thus, our results demonstrate the importance of the large fauna, indicating that the absence or loss of large frugivores will have negative consequences on ecological dynamics.
Supplementary material
To view supplementary material for this article, please visit https://doi.org/10.1017/S0266467422000505
Acknowledgments
We are grateful to the postgraduate programme in Environmental Sciences at Universidade do Estado de Mato Grosso, campus of Cáceres. The Chico Mendes Institute for Biodiversity Conservation and the Serra das Araras Ecological Station. We thank Carlos de Souza Ferreira, Marcelo Andrade, Felipe Mendes, Erinalda Mendes, Vicente da Costa, Victor Hugo de Oliveira Henrique and Derick Victor de Souza Campos for their support and field logistics, Daiane Cristina Carreira and Leticia Prado Munhoes for the valuable discussions about the work, Dandara Sebastian for identifying the plant species, Edson Fiedler de Abreu-Jr for identifying species of Sciurini and Márcio Leite de Oliveira for identifying species of Cervidae.
Financial support
This study was partially funded by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brazil (CAPES) – Financing Code 001, and the Fundação de Amparo à Pesquisa do Estado de Mato Grosso (FAPEMAT): LGAG received a CAPES scholarship; BDV and AVBF received a scholarship from FAPEMAT/CAPES 007/2018.
Competing interests
The authors declare none.
