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Agricultural and Biological Sciences » "Biodiversity in Ecosystems - Linking Structure and Function", book edited by Yueh-Hsin Lo, Juan A. Blanco and Shovonlal Roy, ISBN 978-953-51-2028-5, Published: April 17, 2015 under CC BY 3.0 license. © The Author(s).

Chapter 3

Biodiversity and Ecosystem Functioning in Tropical Habitats — Case Studies and Future Perspectives in Atlantic Rainforest and Cerrado Landscapes

By Tathiana G. Sobrinho, Lucas N. Paolucci, Dalana C. Muscardi, Ana C. Maradini, Elisangela A. Silva, Ricardo R. C. Solar and José H. Schoereder
DOI: 10.5772/59042

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Relationship between abundance of ants and abundance of herbivore insects in the three studied phytophysiognomies. The continuous curve (circles) represent the decrease of herbivores in Cerradão and Campo Cerrado (χ2=0.7; p=0.02), and the dashed line (triangles) the increase of herbivores in Cerrado Strictu Senso (χ2=1.7; p=0.05).
Figure 1. Relationship between abundance of ants and abundance of herbivore insects in the three studied phytophysiognomies. The continuous curve (circles) represent the decrease of herbivores in Cerradão and Campo Cerrado (χ2=0.7; p=0.02), and the dashed line (triangles) the increase of herbivores in Cerrado Strictu Senso (χ2=1.7; p=0.05).
Relationship between SAP-sucking insects in the three phytophysiognomies. C – Cerradão, CC – Campo Cerrado, CSS – Cerrado Stricto Sensu. C and CC did not differed statistically.
Figure 2. Relationship between SAP-sucking insects in the three phytophysiognomies. C – Cerradão, CC – Campo Cerrado, CSS – Cerrado Stricto Sensu. C and CC did not differed statistically.
Relationship between the proportion of chewing insects and ant species richness. While ant species richness increased chewing herbivores in Cerradão (circles; continuous line), in decreases this proportion in Cerrado Stricto Sensu and Campo Cerrado (triangles; dashed line). The relationship between sap-sucking insects and ants follows a pattern contrary to the above, as these proportions are complementary.
Figure 3. Relationship between the proportion of chewing insects and ant species richness. While ant species richness increased chewing herbivores in Cerradão (circles; continuous line), in decreases this proportion in Cerrado Stricto Sensu and Campo Cerrado (triangles; dashed line). The relationship between sap-sucking insects and ants follows a pattern contrary to the above, as these proportions are complementary.
Seed removal rates increased with ant species richness (F1,6=11.01; p=0.021), and were higher in Eucalyptus crop.
Figure 4. Seed removal rates increased with ant species richness (F1,6=11.01; p=0.021), and were higher in Eucalyptus crop.
NMDS map of species composition according to treatment (Native or Eucalyptus crop). We analyzed significance by using Permanova test, which was non-significant.
Figure 5. NMDS map of species composition according to treatment (Native or Eucalyptus crop). We analyzed significance by using Permanova test, which was non-significant.

Biodiversity and Ecosystem Functioning in Tropical Habitats — Case Studies and Future Perspectives in Atlantic Rainforest and Cerrado Landscapes

Tathiana G. Sobrinho1, Lucas N. Paolucci1, Dalana C. Muscardi1, Ana C. Maradini1, Elisangela A. Silva1, Ricardo R. C. Solar1 and José H. Schoereder1

1. Introduction

Currently, environmental changes can be seen as an intrinsic feature of ecosystems, once finding ecosystems that do not suffer of anthropogenic pressures, either direct or indirect, is rare [1]. Such pressures come from the continuous and exponential human population growth, which propels urbanization, activities and processes directly linked to the use of fossil fuels, mining, agriculture and cattle growth. The maintenance of current human population growth implies in the supply of a huge demand for food and technology, resulting in rising pollution and loss of habitats and entire ecosystems [2-5].

Anthropogenic impacts alter the physical environmental characteristics, climate, temperature, soil and water quality, and biogeochemical cycles, interfering directly on the biota [6-11]. The immense resource consumption exerted by the human population demands an ongoing exploitation of natural resources. This causes a constant increase of greenhouse gas emissions and, consequently, the temperature around the globe, also generating an intense conversion of soil use [12,13]. The shift from natural environments into cultivated soils became noteworthy in several countries mainly after the Green Revolution, and together with the frequent use of fertilizers, have changed or destroyed natural habitats, decreasing biodiversity directly or indirectly [9,14]. In addition to these factors, species overexploitation and species invasion have contributed to the decline of biodiversity [15]. Current data indicates that almost 30% of known species in the World became extinct or are endangered due to anthropogenic pressures.

The loss of biodiversity itself is not the only problem associated with human disturbance, as such habitat changes may have a harmful cascade effects that alter other environmental properties. Every biodiversity loss may be translated into a loss of functional diversity [16], which is related to the characteristics of organisms that allow them to perform different function in the ecosystem [16,17]. These functions, such as seed dispersal [18,19], pest and weed biological control [20], pollination [21], nutrient cycling [22], and the decomposition of organic matter, among others, are essential to ecosystem functioning maintenance. Ecosystem functioning include biogeochemical and ecosystem processes [23], responsible by matter cycling and energy flow, being directly related to resource dynamics and ecosystem stability [17]. Generally, the ecosystem functioning can be estimated as the magnitude and dynamics of ecosystem processes resultant from the interactions within and between different levels of biota [24].

Traditionally, the main parameters used for estimate ecosystem functioning are linked to plant communities, such as primary productivity and biomass stability [25-27]. Processes mediated by other organisms, including arthropods, have seldom been used for such estimates [28,29], regardless their crucial role. Arthropods are very diverse organisms, abundant everywhere, highly successful and spread across the globe. They represent more than 80% of all described biodiversity and, among them, insects are the most abundant [30]. Arthropods perform several functions in ecosystems, at different levels. These organisms inhabit from the underground soil layers to the top of tress, are engaged in several trophic levels, and interfere in the occurrence and distribution of several other organisms through intricate interactions such as predation, competition, herbivory and mutualism. Arthropods perform soil bioturbation [31], pest, weed, parasite and disease control [32-34], pollination [35,36], seed dispersal [18,37], dung and carrion removal [37], and act in decomposition and nutrient cycling [22,38,39]. Thus, it is expected that changes in the diversity of arthropods can also trigger changes in the ecosystem functioning.

Functional features of species may influence how ecosystem functioning will be altered with biodiversity loss [40]. Different species may be redundant in the functions they play in the ecosystem, and in this case species loss would be compensated by another one that performs the same function. Hence, biodiversity loss would not necessarily cause decrease on ecosystem functioning, as well as it would not increase if new species were added (redundancy hypothesis, or null hypothesis). Alternatively, some species may be singular or unique in the functions they play within the ecosystems, and their loss would eventually result in a decrease of ecosystem functioning (linearity hypothesis). Finally, the effect of species loss or gain on ecosystem functioning may be dependent on the conditions (community species composition or soil fertility, for instance) under which these biodiversity alterations occur, and the outcome would be unpredictable (idiosyncrasy hypothesis) [40].

The linearity hypothesis is a pattern frequently reported in studies carried out in temperate regions [41], while in the tropics the null hypothesis seems to be the most common. This difference in the reported patterns may be linked to higher biodiversity levels found in the tropics, suggesting a possible functional redundancy among species, which does not seem to occur in temperate regions. Notably, tropical regions harbor the highest World biodiversity [42,43], once 16 of the 25 biodiversity hotspots are located in these regions [43,44]. Conversely tropical regions also exhibit the highest rates of species loss due to human activities [45,46]. Among the main human alterations that cause biodiversity loss is land use change [47-49] and, according to estimates, it will remain as the main activity during the next 100 years [50]. Several tropical biomes have experienced high biodiversity loss due to land use change and, in Brazil, the Atlantic Forest and the Cerrado (Brazilian savanna) may be highlighted [8,51-53].

The Atlantic Forest originally covered ca. 150 million hectares along the Brazilian coast [52], occurring in tropical and subtropical regions, and including sites with large altitude variation, humidity, temperature and rainfall regimes. Such a variation in abiotic conditions allowed the differentiation of several phytophysiognomies, high endemism and the occurrence of numerous rare species, harboring ca. of 8% of Worlds’ biodiversity. However, recent estimates indicate that more than 90% of its vegetation cover has been lost, and the Atlantic Forest is nowadays composed by forest fragments, mostly smaller than 250 ha, immerse in a landscape of different human modified habitats [52]. The effects of habitat loss due to human activities are extensively reported in the literature concerning the Atlantic Forest [8,54-56], but the effects of biodiversity decrease on the processes related to ecosystem functioning still need more consistent information. The Brazilian Cerrado is the second larger biome of the country, occupying originally approximately 22% of its area [57], and stands out by its high biodiversity and endemism. The Cerrado is currently suffering an elevated degree of human exploitation, and nowadays remains less than 30% of its original area [43]. High fragmentation and conversion in pasture or agriculture areas, cause biodiversity loss, soil erosion, arrival and establishment of invasive species, and shifts on fire regimes, carbon cycles and climate [51-53].

In this chapter we aimed to evaluate the relationship between biodiversity and ecosystem functioning in the tropical biomes Atlantic Forest and Cerrado. We report here three case studies that investigate different ecosystem processes modulated by arthropods: litter decomposition, seed dispersal and protection against herbivores. In these studies we seek to understand the relative importance of species richness and of the presence of keystone species on the studied ecosystem functions.

We performed the first case study in a secondary forest fragment, in the Atlantic Forest biome. In this study we test the relationship between litter decomposition and the biodiversity of several functional groups of soil and litter arthropods. We performed the second case study in the Cerrado biome, testing the effect of ants biodiversity that visit extrafloral nectaries on the protection of these plants against herbivores and herbivory.

Lastly, in the third case study, carried out in the same region of the first one, we analyzed the effect of ant biodiversity on seed removal, comparing secondary forests and Eucalyptus crops. In this study we test the direct effect of land use change on the relationship between biodiversity and functioning. From the analysis of these three case studies we concluded this chapter presenting some future perspectives of studies on this subject, to solve some knowledge gaps related to the biodiversity and ecosystem functioning relationship in tropical ecosystems.

2. Case study 1

Decomposition is the process that transforms nutrients retained in organic matter into their inorganic form, making them available in the soil to the primary producers [58,59], and is therefore a key supporting process for the functioning of ecosystems. This process is ruled by three main factors: the physicochemical environment, the quality of the decomposing material and the soil and litter fauna [58,60-63]. These factors present different interaction routes [64] and the relative importance of each component changes in different time and spatial scales [65].

The physicochemical environment is related to the climate, or microclimate, mainly humidity and temperature [66,67]. Abiotic conditions may indirectly affect decomposition, altering litter characteristics, or directly, controlling the activity of decomposers [66,68]. Litter quality is usually associated to foliar material degradability [69], as the concentration of some nutrients has been frequently associated to its palatability to organisms [70]. Usually a higher initial nitrogen concentration reflects in a higher organic matter quality to decomposers. Finally, organisms living in litter and soil are crucial for decomposition processes and nutrient release [60,71-73]. These organisms revolve, mix, break and digest the detritus, metabolizing the litter constituents [58]. Among the components of the soil community, fungi and bacteria are the main decomposing agents. Nevertheless, the micro and mesofauna of soil and litter arthropods have an important role in the decomposition process, through fragmentation of organic matter, through the mixing and vertical movement of organic matter [74]. The existence of an abundant and diversified arthropod fauna is expected, then, to favor an enhanced nutrient cycling [75] and a subsequent faster plant growth [76].

The abundant arthropod fauna composing soil and litter communities can be categorized into different guilds or functional groups, according to their activities, which may affect the microbial community by several ways [77]. Fungivores and bacteriovores consume exclusively the microorganisms, decreasing their abundance. Moreover, they can decrease their prey species richness, through an intense predation, or else an increase of this species richness, through the top-down control of the more competitive species, mediating their coexistence. Detritivores, on the other hand, consume part of organic matter together with the film of microorganisms, releasing the broken and partially digested organic matter in their faeces. As a result, besides their negative effects on microorganisms due to predation, detritivores may increase litter fragmentation, resulting in more decomposing surface and higher decomposer abundance an species richness. These organisms interact in complex food webs and therefore diversity and abundance changes of a given functional group or guild may alter abundance, diversity and functioning of another group [78,79]. It is important hence the investigation of the functional groups role on the decomposition process, as different guilds may interfere more than others.

The process of litter decomposition, as well as the intricate relationships among the diverse components of the edaphic fauna associated to the litter, offers an excellent study system of the relationship between biodiversity and ecosystem processes, mainly in tropical environments with their huge diversity. In this study case we verify how soil and litter arthropod biodiversity affects litter decomposition in a tropical habitat. Our hypothesis is that increasing arthropod abundance and species richness cause higher decomposition rates, and that some functional groups may have stronger roles in this process.

2.1. Methods

We carried out this study from July 2008 to February 2009, in a ca. 300 ha secondary forest in Viçosa, Minas Gerais, Southeast Brazil (20°45'S e 42°55'W). The main vegetation is composed by Semidecidual Seasonal Atlantic Forest, located within the domain of the Atlantic Forest [80]. In the study area we set two 75m parallel transects, apart 5 m from each other. Along each transect we delimited 15 1m2 squares, 5m distant from each other, in a total of 30 sampling points. We collected approximately 200g of freshly fallen leaves from predominant tree species in each sampling point. These leaves were mixed and oven-dried at 60°C for 72 hours. Dried leaves were weighted and separated in groups of 5g, which were placed into litter bags, measuring 15 x 15 cm, with a mesh of 2 mm [81,63]. In each sampling point we set 15 litter bags and, after 30 days we started to remove them. Litter bags were removed fortnightly along 225 days. At the end of the experiment we took a 20 cm deep soil sample in each sampling point, which were taken to soil analyses. The soil analyses were performed at the Soil Lab analyses of the Federal University of Viçosa, and consisted of organic matter content and macroporosity, variables that could interfere in the decomposition process.

After removal, we placed litter bags in Berlese funnels for 48 hours, to extract the arthropods. After their identification, arthropods were sorted according to their feeding habits: detritivores, fungivores and predators [82-86]. The arthropods that we cannot sort in the above categories, because we could not identify feeding habits, were classified as “other arthropods”, and were considered only in the analyses that included all arthropods.

After the arthropod extraction, litter was oven-dried at 60°C for 72 hours and weighted to compare with the initial weight (5g). We considered litter weight loss as the difference between initial and final weight (after 225 days), and we used this as an estimate of decomposition in each sampling point.

2.2. Statistical analyses

To test the hypothesis that more arthropod richness and abundance leads to a higher litter decomposition rate we used a model selection approach [87,88]. The response variable was litter weight loss, and explanatory variables were: total abundance and richness of arthropods, abundance and richness of fungivores, detritivores and predators, as well as macroporosity and soil organic matter. Before structuring the model, we carried out a correlation test among the explanatory variables, using the package “psych”, and whenever two variables presented a correlation higher than 0.7 we removed the variable considered biologically less relevant [89]. Variables that presented correlation higher than 0.7 were: total arthropod species richness and predator species richness (0.73) and total arthropod abundance and detritivore abundance (0.94). We opted, then, to remove predator species richness and total arthropod abundance, as the former represents a possible action of organisms distant from the focal process of decomposition and the latter because it is an estimate more general that detritivore abundance.

The procedure of model selection involved the “MuMIn” package [90], that allows the construction of all possible models starting from the global model containing all variables. For each model, the procedure calculates model weight, based on the Akaike Information Criteria– AICc(ω). After doing so, it ranks all models and the best models are those containing lower AICc and higher weight values. We standardized and centralized all explanatory variables [91], using the package “arm” and the models were built with these transformed variables prior to model selection. All models within ΔAICc < 2 bounds were considered to obtain a good evidence of support [87]. In the case of more than one model, we averaged the models to obtain only one final model with averaged model coefficients, including their respective confidence internal. Parameters for which the confidence interval crossed zero were considered non-significant [88]. All analyses were performed under the platform R [92].

2.3. Results and discussion

2.3.1. Litter arthropod fauna

We sampled 2,284 individual and 198 arthropod species, from seven classes: (i) Arachnida, (ii) Malacostraca, (iii) Symphyla, (iv) Chilopoda, (v) Diplopoda, (vi) Entognatha and (vii) Insecta. The class with more orders was Insecta (10 orders), followed by Arachnida (four), Entognatha (three), Malacostraca, Symphyla, Chilopoda and Diplopoda (one order each). The most abundant arthropods in our sampling were Acari and Collembola, which are usually described as more abundant in soil and litter [93]. Besides, high abundance of these two groups had already been reported by [94] and [95], who studied forest fragments in the same region. Oribatid mites were the most respresentative group in all sampling, and these mites have an important role in decomposition process, as most are detritivore [93]. Collembola also presented high abundance and species richness in the samples. These organisms are fungivores and their trophic activity includes both the direct consumption of microorganisms and organic matter fragmentation [96]. Besides, they constitute an important source of food to predatory organisms, being very important in food webs to soil and litter [97].

2.3.2. Arthropod biodiversity and ecosystem functioning

Opposed to what we expected, there was no effect of arthropod species richness and abundance on decomposition rates, both considering total arthropods and when they were sorted by their feeding habits. Although our final model presented soil macroporosity and detritivore species richness as explanatory variables, their 95% confidence interval includes zero, and were considered non-significant (Table 1).

Response variable Explanatory variables (parameters) Estimate SE Lower CI Upper CI
(litter weight loss)Macroporosity0.09770.0953-0.07770.2732
Detritivore species richness-0.09200.0897-0.26790.0838

Table 1.

Summary of model averaging results, detailing the explanatory variables present in the final average model. Parameters estimates were obtained from standardized variables.

Our results contrast with others, which reported a positive effect of species richness on ecosystem processes [98-103]. The lack of relationship in our study may have occurred due to a high functional redundancy among arthropod species [40,104]. Accordingly, we infer that the studied community is composed by species with similar functions, thus species loss does not cause changes on ecosystem functioning. However, this possible redundancy assumed in this case study does not necessarily exclude another hypothesis to explain the biodiversity-functioning observed: the linearity hypothesis. Two curves may be generated by these two hypotheses: a linear relationship (Type I curve) in the case of singular species and an asymptotic curve (Type II curve) in the case of redundant species [105]. Therefore, both hypotheses may be explained by the same curve, depending on the scale data was sampled. Linearity, then, would be a component of redundancy curve, but that would only be expected in cases with low diversity. From a given species richness a saturation of the functions would occur, with species playing similar roles. Data obtained in the present study would fit into this latter diversity scale. To test such assumption one can manipulatively reduce arthropod abundance and richness, studying a broad range of species richness, and effectively testing the redundancy hypothesis in tropical environments.

Another possible explanation to the absence of relationship between arthropod diversity and litter decomposition is the similar litter constitution across all sampling points. It is known that the chemical and physical composition of litter has an effect on decomposition rates [61,62,70,106,107]. The manipulation of litter diversity and composition in litter bags may lead to the establishment of different arthropod communities, according to leaf degradability. The manipulation of species richness and composition of plants under decomposition may lead to different responses of arthropod species richness, which might mirror variation in decomposition rates.

Furthermore, in this study we evaluated only the role of arthropod diversity of the soil-litter system. It is known, however, that fungi and bacteria (the microflora) are the decomposers and responsible for organic matter mineralization [58,60,71]. Conversely arthropods act indirectly on decomposition and, even though they facilitate the action of true decomposers, detecting their action on decomposition may be less straightforward.

The absence of relationship between litter decomposition and arthropod species richness and abundance must be evaluated with caution, because assuming functional redundancy among species may be uncertain. Such outcome may lead us to the wrong conclusion that species loss does not affect ecosystem functioning at all, and this early, which may be wrong as discussed above.

Our conclusion is that litter decomposition process in the tropics and other hyper diverse habitats may be more complex than it is for the well known temperate habitats. Studying only one component may not give a precise response, due to the immense assembly of components in complex habitats and their equally complex interactions. Manipulative experiments, microbial activity estimates, as well as manipulation of litter diversity and composition should give us a more precise knowledge of the biodiversity role on ecosystem key processes.

3. Case study 2

Besides the ecosystem processes, as decomposition and nutrient cycling, species interactions are also important in the maintenance of ecosystem stability. The importance of predation and competition in community structuring is well studied [108-110], although mutualism may also have a central role in species distribution in ecosystems [111,112].Ants may establish a wide variety of mutualistic associations with plants [113,114]. Plants may offer resources like shelter, food, or both, that may be used by ants in several ways. The mutualistic interactions between ants and plants vary from diffuse, such as secondary seed dispersal [115] and use of extrafloral nectaries (EFNs) by generalist species [116], to more specialized interactions, such as domatia colonization by Azteca sp. [117-119,]. On the other hand, ants may also be beneficial to plants, increasing seed dispersal or reducing herbivory, for example [120].

EFNs, are nectar producing structures associated to plant vegetative organs, as leaves or petioles [121]. Extrafloral nectar is a liquid resource, composed by glucose, sucrose and fructose, and containing sometimes amino acids and proteins [122]. EFN-bearing plants are more visited by ants than plants without them [123], and ants that use extrafloral nectar as a resource may establish a generalist association of protection in exchange for food [114,119]. Therefore, the benefits arising from this interaction may explain its success [124]. The interaction between ants visiting EFNs and the plants has been the subject of several studies, although there are some divergences among the obtained results. Several studies relate advantages for EFN-bearing plants, such as decreasing the herbivory and the abundance of herbivores, or even positive effects on plant fitness [120,121,123,125-127]. However, some studies did not spot beneficial effects of visiting ants [128,131,132], indicating that in some cases ants may not be efficient in reducing herbivory [128]. The outcome of the interaction between ants and plants may depend on feeding habits of the herbivores, due to the interaction between ants and sap-feeding insects. Several authors [123,130-134] suggest that generalist ants feeding on their honeydew protect these insects from predators and competitors over chewing insects [130]. Moreover, plant protection may be related to ant species composition, as different ant species present varied behavior and defensive characteristics [129].

The interaction among ants, EFN-bearing ants and herbivores is very common in the Brazilian Cerrado. This biome is composed by herbs, shrubs and small trees that vary in density, composing different phytophysiognomies [135]. These physiognomies are usually divided in three groups, characterized by fields, savannas and forests [136]. Qualea grandiflora (Vochysiacveae) is among the several EFN-bearing plant species of Cerrado, which are medium to large-sized trees that reach 30 meters [137]. It is very studied in the Cerrado as it has a large distribution and abundance, and also because it attracts several ant species to their EFNs, placed at the basis of the petioles, near to leaf insertion [138].

This case study evaluates whether the ants foraging on Qualea grandiflora protect these plants against herbivory. We tested the hypotheses that increased ant species richness and abundance (i) decreases herbivore species richness and abundance, and (ii) changes the proportion of herbivore guilds in Cerrado.

3.1. Methods

Sampling was carried out in Panga Ecologic Station (PEE), situated in Minas Gerais, Brazil (19o09'20"-19o11'10" S, 48o23'20"-48o24'35" W). The area is a 409 ha of Cerrado, with several phytophysiognomies [139, 140]. Climate is Aw, tropical with a rainy summer and dry winter [141]. The average temperature during winter is 18°C and during summer is 23°C, and monthly rainfall is 60 mm during winter and 250 mm during summer.

Insects were sampled during January 2013, during the rainy season. We chose 90 individuals of Qualea grandiflora, 30 in each phytophysiognomy: Cerradão (Forest), Cerrado Stricto Sensu (Dense Savanna) and Campo Cerrado (Field Savanna). As it is known that ant species richness and abundance may vary with tree density in Cerrado [142], we expect that sampling in three different plant densities would produce a higher range of variation on ant community parameters. We sampled herbivores by beating, using an entomological umbrella of 1 m2 [143,144]. We did 10 beatings in each tree, and all insects were collected. All herbivores were counted, identified up to the family level, and sorted into two groups (guilds): leaf chewing insects and sap-sucking insects. Ants were sampled by pitfall traps, placed in the trunk of trees at 1.5 meters above ground level. In each tree we installed four pitfalls, to maximize ant sampling. Pitfall traps remained open for 48 hours, and ants were identified to the lower level as possible (genus or species). When identification up to species level was not possible, we asserted the individuals into morphospecies. Herbivores eventually collected in the pitfall traps were added to the beating sampling.

3.2. Statistical analyses

To test whether an increase of ant species richness and abundance decreases herbivore species richness and abundance, we carried out an ANCOVA (analysis of covariance), with Poisson distribution, considering phytophysiognomies as covariates. To test the hypothesis that increasing ant species richness and abundance decreases the proportion of leaf chewing insects and increases sap-sucking insects, we carried out an ANCOVA to one of the herbivore guilds, using a binomial distribution, corrected for overdispersion. Only one analysis is needed in this case, as the two response variables (proportion of each guild) are complementary. All analyses were carried out in R platform and models were simplified by removing non-significant variables and obtaining the minimal adequate model [145].

3.3. Results and discussion

We sampled 2,597 ants, from 150 species, 25 genera and seven subfamilies. The most abundant subfamily was Formicinae (1,293 individuals), followed by Myrmicinae (737), Dolichoderinae (426), Pseudomyrmecinae (110), Ectatomminae (22), Ponerinae (eight) and Heteroponerinae (one). The subfamily with the highest species richness was Myrmicinae (55 species), followed by Formicinae (40), Pseudomyrmecinae and Dolichoderinae (20 species each), Ectatomminae (three), Ponerinae (two) and Heteroponerinae (one). We sampled 233 herbivore insects, and Coleoptera was the most abundant order (141 individuals), followed by Hemiptera (75), Lepidoptera (11) and Orthoptera (six). Herbivores were sorted in 97 species, and the order with highest species richness was Coleoptera (62 species), followed by Hemiptera (24), Orthoptera (six) and Lepidoptera (five).

Ant species richness did not affect both herbivores abundance and species richness. As the studied plant species is a mirmecophile, it was not expected to maintain obligatory associations with ant species, being visited by generalist ant species foraging both during the day and the night. Several species in a given community may have a redundant role in some ecological functions, such as predation [146]. Moreover, as mirmecophyles are usually visited by several ant species, species richness may not contribute effectively for herbivore decrease. Therefore, ant species richness visiting EFN-bearing plants may not contribute to herbivore decrease because (i) they may be highly redundant, and/or (ii) they encompass non-aggressive ant species.

Nevertheless, we observed a decrease of herbivore abundance with the increase of abundance of ants in the trees of Cerradão and Campo Cerrado2=0.7; p=0.02) (Figure 1). The higher number of ants present in a given site gives a higher probability of encounters between them and herbivores, decreasing the number of herbivores [147]. Some ant species may present aggressive behavior, or efficient recruitment ability, and if the most frequent ants have these attributes, there would be a higher chance of herbivore attack and decreasing.

Conversely, we also observed that herbivore abundance increased with the abundance of ants in Cerrado Stricto Sensu2=1.7; p=0.05) (Figure 1). Another interesting result regards a higher sap-sucker insect abundance in Cerrado Stricto Sensu, in comparison with the other two phytophysiognomies (Figure 2). This latter result may explain the positive relationship between ant and herbivore abundance, because most of the herbivores belong to sap-sucking insects, and the positive association between them and ants is well known. As there are more sap-sucking insects in the Cerrado Stricto Sensu, ants may be consuming more sugars from the honeydew than from the EFNs [148], possibly leading to a dominance of more aggressive, abundant and frequent ants [149]. Therefore, the association between ants and EFN-bearing plants may shift from mutualistic to antagonistic when sap-sucking insects are present. When there is high resource competition on the plants, ants have a tendency to consume more honeydew than nectar [150], protecting sap-sucking insects and harming the plants.

Although the above scenario may arise from the three trophic level interaction mentioned above, it has been suggested that ants may also repel chewing insects by consuming honeydew, decreasing their abundance and activity on plants [133]. The different responses of herbivores to abundance of ants found in our study suggest that the effect of ants on herbivores is dependent of herbivore feeding habits. Several studies have reported non-obligatory interactions between ants and sap-sucking insects [123,130-134]. In this interaction, ants feed on the honeydew and protect the insects against predators and competitors [130]. Such an interaction may produce an explanation for the above results, because most ants participating in this interaction are generalists, consuming both honeydew and nectar from EFNs. Therefore, both sap-sucking insects and plants may be protected by the ants, as both provide resources to them. In this scenario, leaf chewing herbivores would be repelled or predated by the foraging ants.


Figure 1.

Relationship between abundance of ants and abundance of herbivore insects in the three studied phytophysiognomies. The continuous curve (circles) represent the decrease of herbivores in Cerradão and Campo Cerrado2=0.7; p=0.02), and the dashed line (triangles) the increase of herbivores in Cerrado Strictu Senso2=1.7; p=0.05).

However, ant species distribution and their consequent effect on interactions may be modulated by habitat type and conditions [151]. Habitats with larger resource availability may facilitate the coexistence of ant species [131]. As Cerrado is composed by vegetation types with different tree abundances [136], the relationships among organisms may also vary accordingly. EFN-bearing plants were found to be more frequent in the Forest formations of Cerrado (Cerradão) than in other phytophysiognomies, which indicates more extrafloral nectar in this vegetation type [152]. As tree density and species richness influences ant species richness due to higher resource availability to generalist and specialist species [142], mutualistic interactions may be dependent of resource amount and distribution. More heterogeneous habitats may generate diverse resource availability, promoting the found differences among the phytophysiognomies studied here. As there are more resources in the Cerradão, ant foraging may be more opportunistic, resulting in a less effective protection against herbivory by chewing insects. Additionally, as there are more resources provided by EFNs, associations between sap-sucking insects and ants may be less effective, decreasing their abundance.


Figure 2.

Relationship between SAP-sucking insects in the three phytophysiognomies. C – Cerradão, CC – Campo Cerrado, CSS – Cerrado Stricto Sensu. C and CC did not differed statistically.


Figure 3.

Relationship between the proportion of chewing insects and ant species richness. While ant species richness increased chewing herbivores in Cerradão (circles; continuous line), in decreases this proportion in Cerrado Stricto Sensu and Campo Cerrado (triangles; dashed line). The relationship between sap-sucking insects and ants follows a pattern contrary to the above, as these proportions are complementary.

4. Case study 3

The conversion of pristine environments into human-modified landscapes is rising around the World. Such habitat conversions may culminate in altered environmental conditions, reduction in the availability of resources and decrease in habitat heterogeneity [153]. Consequently, many authors have been warning to the existence of a biodiversity crisis [154,155]. In general the conversion of natural systems introduces newer and simplified ecosystems composed by one or few economically valuable crop species. Whereas habitat loss per se is enough to generate local extinctions [156,157], what is observed is that these habitats are usually substituted by agricultural systems as well. Therefore, most human-modified landscapes are altered by the joint action of these processes, habitat loss and conversion.

Habitat heterogeneity can be defined as the variety and the relative amount of different microhabitats available to organisms, and has been considered over the years a major variable determinant on local species richness and abundance [158-160]. Structurally more complex habitats provide more spatial niches and different types of resource exploitation, thus increasing species diversity [153,161-162], although this relationship may not be always straight [163,164]. Habitat heterogeneity reduction, for instance, can lead to lower resource availability, changes in environmental conditions and eventually species and ecosystem functions losses [165,166].

Eucalyptus crops are one of the economic activities that may lead to the above mentioned biodiversity loss in the Brazilian biomes. This culture was introduced in the country by the beginning of 19th century, and up to 2012 it is estimated to cover 5.105.246 hectares [167]. Once Eucalyptus is classically grown as a monoculture in Brazil, habitats are extremely simplified and homogeneous, potentially triggering the mentioned effects on biodiversity.

Several functions may be altered in Eucalyptus plantations, potentially due to homogenization, such as litter decomposition [97,168], nutrient cycling [169] and seed dispersal [170]. The latter is usually associated with habitat recovery, as there are several advantages for plants such as avoiding rodent predation [171,172], dispersion for nutrient-rich sites [173], protection against fire [174] and smaller competition with the parental plant [175]. Thereby, such mutualism may play a central role on local plant dynamics [176].

Seed dispersal by animals is considered a diffuse interaction, once can be performed by several generalist frugivores [177,178]. Ants are mainly reported as secondary dispersers, as they take fallen diaspores to their nests. Within the nests conditions are more suitable for the seed, because it is protected from herbivores [179-181], it is a nutrient-rich microhabitat [182,183] and free of competition with the parental plant [175,180,184].

A common observed trend is the reduction in ant species richness with habitat conversion, such as pastures [185], crops [186] and in Eucalyptus cultures [187,188]. Species composition is also usually altered by habitat conversion [185,189]. These changes may strongly alter seed dispersal dynamics by ants in fragmented and modified landscapes [185,190], although no mechanism was proposed to explain this correlation. In this study we tested the effect of natural habitat conversion into Eucalyptus crops and the consequences for seed removal by ants. We hypothesized that higher ant species richness increases seed removal, and this relationship is more pronounced in natural forest ecosystems than in Eucalyptus crops. Furthermore, we hypothesized that ant species composition changes between natural and Eucalyptus crops, and this shift is also responsible for supposed differential seed removal rates. Finally, as we observed differential seed removal between studied habitats we tested the presence of keystone species would influence removal rates.

4.1. Methods

4.1.1. Study site

We carried out the study in Viçosa, Minas Gerais (20°45’S, 42°50’W), Brazil, during summer 2010/2011, the rainy season. The pristine vegetation in this region is within the Atlantic Forest Domain, and is classified as Seasonal Semi-deciduous Forest. From the 1930’s decade an intense fragmentation process has begun, and the native vegetation was mainly substituted by coffee crops and pastures. Now days, the landscape is highly fragmented, and is composed by several secondary forest fragments, intermingled with pasture, coffee and Eucalyptus crop, among others. We arbitrarily chose five forest fragments and five neighboring Eucalyptus for our study sites.

4.1.2. Experimental design

We used Mabea fistulifera (Euphorbiaceae) seeds, an abundant native myrmecochoricous species with elaiosome. Seeds of this species have a diplochoric dispersion, primarily ballistic and secondarily mainly by ants. Seeds, collected directly from branches of several native trees, were obtained from Forest Seeds Laboratory of the Federal University of Viçosa two months before the experimental set up. Seeds had their elaiosomes preserved and were maintained in cold chamber at 20°C straight after natural dehiscence and kept until their use.

In each of the 10 sampling sites (5 native forests and 5 Eucalyptus crops), we set 10 sampling units, which were distributed 10 meters apart from each other. Each sampling unit consisted of one ant sampling point and one seed removal spot, distanced 2 meters from each other. Ant sampling points consisted of unbaited pitfall traps (diameter 8 cm, 12 cm height), buried at soil level, and half filled with a killing solution of water, detergent and salt. Seed removal spots consisted of the provision of 10 seeds of M. fistulifera, which were covered by a cage with a mesh of 10 mm, to avoid seed removal by vertebrates [192]. Both pitfall traps and seeds remained in the field for 48 hours. After that, we counted the number of remaining seeds and the number and identity of ant species.

We identified ants to genera using the keys by [192], and when possible to species by comparisons with the reference collection of the Community Ecology Lab/UFV, where voucher specimens were deposited. Species identification was confirmed by a specialist.

4.2. Statistical analyses

To test the relationship between seed removal and ant species richness we used an ANCOVA, in which the response variable was the proportion of removed seeds in each site, and the explanatory variables were ant species richness and environment type (native forests or Eucalyptus crops). As the response variable was a ratio, we used a binomial error distribution, corrected for overdispersion when necessary. We performed this analysis in the software R [92] and we did residual analysis to check for model fit and distribution suitability.

To test whether ant species composition changes between studied habitats, we performed a NMDS (Non-metric Multidimensional Scaling), using Bray-Curtis dissimilarity index. We computed species abundances as the number of traps they occurred in each sampling site. The significance of differences was checked through PERMANOVA [193]. This analysis was performed in the package vegan within the software R [92]. We tested if the most frequent ant species act as keystone species [194] in seed removal by an ANOVA, in which we compared seed removal in the presence and in the absence of each species.

We removed one of the Eucalyptus areas a priory from all the analyses due to a heavy rain that removed all seeds, and another Eucalyptus area from the ANCOVA after the residual analysis as it was considered an outlier, therefore reducing our total sampling units to eight (five native and three Eucalyptus crops).

4.3. Results

We sampled 43 ant species, from 25 genera and seven subfamilies. From these, 23 species occurred exclusively in the native forests, five were exclusive from Eucalyptus and 15 occurred in both. The most frequent species were Pheidole radoskowskii Mayr, 1884 and Ectatomma muticum Mayr, 1870, which occurred in 40.24% and 30.49% of pitfall traps, respectively.

As expected, ant species richness was higher in native forest than in Eucalyptus crops (χ2=6.93; p=0.008). Moreover, seed removal rate increased with the number of ant species (F1,6=11.01; p=0.021; Fig. 4), however it was higher in the Eucalyptus than in the native forest (F1,6=8.75; p=0.032). Conversely, species composition did not differ between the two habitats (Fig. 5, PERMANOVA F1,7=1.12, p=0.32). Neither the presence of P. radoskowskii (F1,80=0.87; p=0. 35), more frequent in Eucalyptus, nor of E. muticum2=0.94; p=0.33), more frequent in native forests, influenced seed removal.

5. Discussion

Differences in species richness, abundance and composition may affect ecosystem functioning [195]. In this case study we investigated the role of these three biodiversity components on seed removal by ants in native and Eucalyptus forests. Concerning species richness our results confirm the general pattern of reduction in modified habitats. The main causes reported for such pattern include habitat loss, homogenization, and harshness conditions for native species [196]. In comparison with native forest, Eucalyptus crops may be homogeneous habitats, which might have contributed to its lower species richness. Ant species richness is strictly related with environmental features such as higher plant species diversity, litter amount and habitat complexity [142,197-200]. From these, plant species diversity and habitat complexity decrease in Eucalyptus crops, which may have caused the loss of ant species that did not survive in the modified habitat. We observed the expected positive relationship between seed removal and ant species richness, both in the native forests and Eucalyptus crops. Nevertheless, the maximal seed removal at Eucalyptus was around 30% while at native forest was about 65%, which may be related to the smaller capacity of Eucalyptus crops of harboring species when compared to native forests. This pattern could also be attributed to keystone species (sensu [201]) at native forest, thus promoting the observed higher removal rates. However, the sole effect of potential keystone species did not explain the rates we observed, as seed removal did not change in their absence. Therefore, we have no evidence to consider the existence of some specialist seed remover species inhabiting either of the environments, reinforcing the role of ant species richness in the studied process.

On the other hand we did not find differential species composition between the two habitats types, thus we cannot assign the higher seed removal at native forest due to some keystone species. Moreover, seed removal rates at native forest did not differ when we analyzed the effects of the presence of the most abundant ant species (E. muticum). Therefore, we conclude that species richness is the only biodiversity component influencing the ecosystem process in the studied system. The positive relationship between ant species richness and seed removal rate may have important concerns on conservation. The maintenance of natural species richness levels can contribute to a suitable ecosystem functioning due to the role of the seed dispersal for seedling establishment and the community assembly.


Figure 4.

Seed removal rates increased with ant species richness (F1,6=11.01; p=0.021), and were higher in Eucalyptus crop.


Figure 5.

NMDS map of species composition according to treatment (Native or Eucalyptus crop). We analyzed significance by using Permanova test, which was non-significant.

6. Conclusions and perspectives

Although a positive relationship between biodiversity and ecosystem functioning is commonly reported [28, 202], we did not find such evidence from all the studies presented here. The main results presented allow us to conclude that the general effect of arthropods on ecosystem functioning is dependent on the studied process and the proximity with their agents. As more direct is the action of arthropods on the ecosystem processes, more detectable are their effects on functioning.

Arthropods contribute indirectly in the process of litter decomposition by modifying the substrate to the decomposers (the microbiota), besides acting through predation in a top-down effect on these microorganisms. Therefore, their indirect effect on litter decomposition may have produced the lack of relationship between their biodiversity and ecosystem functioning. Similarly, in the second case study we observed an absence of ant species richness and plant defense against herbivory. Nevertheless, in this study we noticed that the abundance of ants partially resulted in a decrease of the abundance of herbivore insects. The results obtained in this case study may reflect the plenty of defense mechanisms against herbivory, and ants are only a further mechanism within several others by which plants achieve a better protection. In the third case study we could evaluate a process that directly involved the importance of biodiversity on ecosystem processes, as there is a direct interaction between ants and the seeds they remove, without intermediate agents between them. Therefore, we could notice that the effect of ant biodiversity on the ecosystem process was stronger when compared to the two previous case studies. The above rationale points that a greater proximity between the agent and process turns the relationship stronger and detectable.

Based on the studies presented here, we suggest the following steps to improve the studies of the relationship between biodiversity and ecosystem functioning. Firstly, the control of variables through manipulative approaches should be increased, as confounding variables might decrease the chance of unveiling significant relationships. Secondly, as described above, it should be investigated relationships in which the processes and their agents are more directly connected. As reported elsewhere [28], the effects on productivity decrease with the increase of the number of trophic levels between manipulated (biodiversity) and estimated (ecosystem process) elements. Finally, studies of less complex systems may produce stronger results, once in complex systems several agents may influence concomitantly a given process, decreasing the chance of detecting a relationship between biodiversity and ecosystem functioning. Our second case study is an example, as several agents may influence plant herbivory, besides the presence of a higher ant species richness and abundance. Similar conclusions have been found in a meta-analysis study involving several results obtained from different regions of the World [28]. Hence, the comparison among our results and those obtained by other authors indicate that, despite the high complexity and biodiversity found in tropical regions, the trends reported here are comparable to those found worldwide.

This chapter integrated different case studies relating biodiversity and ecosystem functioning, with varying degrees of proximity between the agents and the processes. Because human activities would certainly continue to produce loss of species, we suggest that future studies relating biodiversity and ecosystem processes consider the linkage among the agents involved in the processes, to improve the understanding of this relationship, as well as the prognosis involving changes in biodiversity.


Authors are indebted to Lucas G. Dornelas for providing his data of case study 3. Authors received grants from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq – Brazil), Fundação Capes – Brazil, and Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG).


1 - Barlow J., Gardner TA., Lees AC., Parry L., Peres CA. How pristine are tropical forests? An ecological perspective on the pre-Columbian human footprint in Amazonia and implications for contemporary conservation. Biological Conservation 2012;151(1) 45-49.
2 - Martens P., Rotmans J., Groot D. “Biodiversity: Luxury or Necessity?”. Global Environmental Change 2003;13 75-81.
3 - Chapin III FS., Kofinas GP., Folke C. editors. Principles of ecosystem stewardship: resilience-based natural resource management in a changing world. Springer: New York; 2009.
4 - Gardner TA. Monitoring forest biodiversity: improving conservation through ecologically-responsible management. Earthscan; London; 2010.
5 - Tscharntke T., Tylianakis JM,, Rand TA., Didham R., Fahrig L, Batáry P., Bengtsson J., Clough Y., Crist TO., Dormann CF., Ewers RM., Fründ J., Holt RD., Holzschuh A., Klein AM., Kleijn D., Kremen C., Landis DA., Laurance W., Lindenmayer D., Scherber C., Sodhi N., Steffan-Dewenter I., Thies C., Putten WH., Westphal C. Landscape moderation of biodiversity patterns and processes-Eight hypotheses. Biological Reviews 2012;87(3) 661-685.
6 - Fritz H., Saïd S., Renaud PC., Mutake S., Coid C., Monicat F. The Effects of agricultural fields and human settlements on the se of rivers by wildlife in the mid-Zambezi valley, Zimbabwe. Landscape Ecology 2003;18(3) 293-302.
7 - Jiang Z., Liu J., Chen J., Chen Q., Yan X., Xuan J., Zeng J. Responses of summer phytoplankton community to drastic environmental changes in the Changjiang (Yangtze River) estuary during the past 50 years. Water Research 2014;54 1-11.
8 - Colombo AF., Joly AC. Brazilian Atlantic Forest Lato Sensu:the most ancient Brazilian forest, and a biodiversity hotspot,is highly threatened by climate change. Brazilian Journal of Biology 2010;70(3) 697-708.
9 - Cardini U., Bednarz VN., Foster RA., Wild C. Benthic N2 fixation in coral reefs and the potential effects of human-induced environmental change. Ecology and Evolution 2014;4(9) 1706-1727.
10 - Gruber N. The marine nitrogen cycle: overview and challenges. In: Capone DG., Bronk DA., Mulholland MR., Carpenter EJ. (eds.) Nitrogen in the Marine Environment. Salt lake city: Academic press; 2008. p1-50.
11 - Halpern BS., Walbridge S., Selkoe KA., Kappel CV., Fiorenza M., D’Agrosa C., Bruno JF., Casey KS., Ebert C., Fox HE., Fujita R., Heinemann D., Lenihan HS., Madin EMP., Perry MT., Selig ER., Spalding M., Steneck R., Watson R. A global map of human impact in marine ecosystem. Science 2008;319(5865) 948-952.
12 - IPCC. Climate Change: The scientific basis. Cambridge: University Press; 2001.
13 - Grau HL., Aide M. Globalization and land-use transition in Latin America. Ecology and Society 2008;13(2) 16.
14 - Carr DL., Lopez AC., Bilsborrow RE. The population, agriculture, and environment nexus in Latin America: country-level evidence from the latter half of the twentieth century. Population and Environment 2009;30(6) 222-246.
15 - Morris RJ. Anthropogenic impacts on tropical forest biodiversity: a network structure and ecosystem functioning perspective. Philosophical Transactions of the Royal Society B: Biological Sciences 2010;365(1558) 3709-3718.
16 - Tilman D. Functional diversity. Encyclopedia of Biodiversity 2001;3(1) 109-120.
17 - Díaz S., Cabido M. Vive la différence: plant functional diversity matters to ecosystem processes. Trends in Ecology and Evolution 2001;16(11) 646-655.
18 - Gorb SN., Gorb EV., Punttila P. Effects of redispersal of seeds by ants on the vegetation pattern in a deciduous forest: A case study. Acta Oecologica 2000;21(4) 293-301.
19 - Dominguez-Haydar Y., Armbrecht I. Response of ants and their seed removal in rehabilitation areas and forest at El Cerrejón coal mine in Colombia. Restoration Ecology 2011;19(201) 178-184.
20 - Gordon CE., McGill B., Ibarra-Núñez G., Greenberg R., Perfecto I. Simplification of a coffee foliage-dwelling beetle community under low-shade management. Basic and Applied Ecology 2009;10(3) 246-254.
21 - Vergara CH., Badano EI. Pollinator diversity increases fruit production in Mexican coffee plantations: the importance of rustic management systems. Agriculture, Ecosystems & Environment 2009;129(1) 117-123.
22 - Nichols E., Spector S., Louzada J., Larsen T., Amezquitad S., Favila ME. Ecological functions and ecosystem services provided by Scarabaeinae dung beetles. Biological Conservation 2008;141(6) 1461-1474.
23 - Naeem S., Bunker DE., Hector A., Loreau M., Perrings C. Introduction: the ecological and social implications of changing biodiversity. An overview of a decade of biodiversity and ecosystem functioning research. In Naeem S., Bunker DE., Hector A., Loreau M., Perrings C. (eds.). Biodiversity, Ecosystem Functioning, and Human Wellbeing: An Ecological and Economic Perspective. Oxford: University Press; 2009.
24 - Naeem S., Chair FS., Chapin III FS., Costanza R., Ehrlich PR., Golley FB., Hooper DU., Lawton JH., O’Neill RV., Mooney HA., Sala OE., Symstad AJ., Tilman D. Biodiversity and Ecosystem Functioning: Maintaining Natural Life Support Processes. Ecological Society of America 1999;4 1-11.
25 - Naeem S., Thompson LJ., Lawler P., Lawton JH., Woodfin RM. Declining biodiversity can alter the performance of ecosystems. Nature 1994;386 734-737.
26 - Tilman D., Wedin D., Knops J. Productivity and sustainability influenced by biodiversity in grassland ecosystems. Nature 1996;379(6567) 718-720.
27 - Aarssen LW. High productivity in grassland ecosystems: effected by species diversity or productive species? Oikos 1997;80 183-184.
28 - Balvanera P., Pfisterer AB., Buchmann N., Jing-Shen H., Nakashizuka T., Raffaelli D., Schmid B. Quantifying the evidence for biodiversity effects on ecosystem functioning and services. Ecology Letters 2006;9(10) 1146-1156.
29 - Slade EM., Mann DJ., Villanueva JF., Lewis OT. Experimental evidence for the effects of dung beetle functional group richness and composition on ecosystem function in a tropical forest. Journal of Animal Ecology 2007;76(6) 1094-1104.
30 - Borror DJ., Triplehorn CA., Johnson NF. An introduction to the study of insects. 7ed. Connecticut: Cengage Learning; 2004.
31 - Lavelle P., Decaëns T., Aubert M., Barot S., Blouin M., Bureau F., Margerie P., Mora P., Rossi JP. Soil invertebrates and ecosystem services. European Journal of Soil Biology 2006;42(1) 3-15.
32 - Perfecto I. Ants (Hymenoptera: Formicidae) as natural control agents of pests in irrigated maize in Nicaragua. Journal of Economic Entomology 1991;84(1) 65-70.
33 - Perfecto I., Sediles A. Vegetacional diversity, ants (Hymenoptera, Formicidae), and herbivorous pests in a neotropical agroecossystem. Environmental Entomology 1992;21 61-67.
34 - Philpott SM., Armbrecht I. Biodiversity in tropical agroforests and the ecological role of ants and ant diversity in predatory function. Ecological Entomology 2006;31(4) 369-377.
35 - Farwig N., Bailey D., Bochud E., Herrmann JD., Kindler E., Reusser N., Schüepp C., Schmidt-Entling MH. Isolation from forest reduces pollination, seed predation and insect scavenging in Swiss farmland. Landscape Ecology 2009;24(7) 919-927.
36 - Vergara CH., Badano EI. Pollinator diversity increases fruit production in Mexican coffee plantations: the importance of rustic management systems. Agriculture, ecosystems and environment 2009;129(1) 117-123.
37 - Andresen E. Effect of forest fragmentation on dung beetle communities and functional consequences for plant regeneration. Ecography 2003;26(1) 87-97.
38 - Cerdà A., Jurgensen MF. The influence of ants on soil and water losses from an orange orchard in eastern Spain. Journal of Applied Entomology 2008;132(4) 306-314.
39 - Dostal P., Breznova M., Kozlickova V., Herben T., Kovar P. Ant-induced soil modification and its effect on plant below-ground biomass. Pedobiologia 2005;49(2) 127-137.
40 - Naeem S., Loreau M., Inchausti P. Biodiversity and ecosystem functioning: the emergence of a synthetic ecological framework. In: Naeem S., Loreau M., Inchausti P. (eds.) Biodiversity and Ecosystem Functioning: Synthesis and Perspective. Oxford: University Press; 2002. p3-11.
41 - Loreau M., Naeem S., Inchausti P. Biodiversity and ecosystem functioning: synthesis and perspectives. Oxford: University Press; 2002.
42 - Mittermeier RA., Myers N., Thomsen JB., Da Fonseca GA., Olivieri S. Biodiversity Hotspots and Major Tropical Wilderness Areas:approaches to setting conservation priorities. Conservation Biology 1998;12(3) 516-520.
43 - Myers N., Mittermeier RA., Mittermeier CG., Da Fonseca GA., Kent J. Biodiversity hotspots for conservation priorities. Nature 2000;403(6772) 853-858.
44 - Brooks TM., Mittermeier RA., Mittermeier CG., Da Fonseca GA., Rylands AB., Konstant WR., Flick P., Pilgrim J., Oldfield S., Magin G., Hilton-Taylor C. Habitat loss and extinction in the hotspots of biodiversity. Conservation biology 2002;16(4) 909-923.
45 - Hansen MC., Potapov PV., Moore R., Hancher M., Turubanova SA., Tyukavina A., Thau D., Stehman SV., Goetz SJ., Loveland TR., Kommareddy A., Egorov A., Chini L., Justice CO., Townshend JRG. High-resolution global maps of 21st-century forest cover change. Science 2013;342(6160) 850-853.
46 - Putz FE., Zuidema PA., Synnott T., Peña-Claros M., Pinard MA., Sheil D., Vanclay JK., Sist P., Gourlet-Fleury S., Griscom B., Palmer J., Zagt R. Sustaining conservation values in selectively logged tropical forests: the attained and the attainable. Conservation Letters 2012;5(4) 296-303.
47 - Fearnside PM. Global warming and tropical land-use change: greenhouse gas emissions from biomass burning, decomposition and soils in forest conversion, shifting cultivation and secondary vegetation. Climatic Change 2000;46(1-2) 115-158.
48 - Gardner TA., Barlow J., Sodhi NS., Peres CA. A multi-region assessment of tropical forest biodiversity in a human-modified world. Biological Conservation 2010;143(10) 2293-2300.
49 - Gibson L., Lee TM., Koh LP., Brook BW., Gardner TA., Barlow J., Peres CA., Sodhi N.S. Primary forests are irreplaceable for sustaining tropical biodiversity. Nature 2011;478(7369) 378-381.
50 - Sala OE., Chapin III FS., Armesto JJ., Berlow E., Bloomfield J., Dirzo R., Huber-Sanwald E., Huenneke LF., Jackson RB., Kinzig A., Leemans R., Lodge DM., Mooney HA., Oesterheld M., Poff LeRoy N., Sykes MT., Walker BH., Walker M., Wall DH. Global Biodiversity Scenarios for the Year 2010. Science 2000;287(5459) 1770-1774.
51 - Klink CA., Machado RB. Conservation of the Brazilian Cerrado. Conservation Biology 2005;19(3)707-713.
52 - Ribeiro MC., Metzger JP., Martensen AC., Ponzoni FJ., Hirota MM. The Brazilian Atlantic Forest: How much is left, and how is the remaining forest distributed? Implications for conservation. Biological Conservation 2009;142(6) 1141-1153.
53 - Almeida S., Louzada J., Sperber C., Barlow J. Subtle land-use change and tropical biodiversity: dung beetle communities in Cerrado grasslands and exotic pastures. Biotropica 2011;43(6) 704-710.
54 - Chiarello AG. Density and Population Size of Mammals in Remnants of Brazilian Atlantic Forest. Conservation Biology 2000;14(6) 1649-1657.
55 - Filho JAS., Tabarelli M. Bromeliad species of the Atlantic forest of north-east Brazil: losses of critical populations of endemic species. Oryx 2006;40(2) 218-224.
56 - Silva RR., Machado Feitosa RS., Eberhardt F. Reduced ant diversity along a habitat regeneration gradient in the southern Brazilian Atlantic Forest. Forest Ecology an. Management 2007;240(1) 61-69.
57 - Oliveira-Filho AT., Ratter A. Vegetation physiognomies and woody flora of the Cerrado biome. In: P. S. Oliveira PS., Marquis RJ. editors. The Cerrados of Brazil: ecology and natural history of a Neotropical savanna. New York: Columbia University Press; 2002. P91-120.
58 - Hattenschwiler S., Gasser P. Soil animals alter plant litter diversity effects on decomposition. Proceedings of the National Academy of Sciences of the United States of America 2005;102(5) 1519-1524.
59 - Bragazza L., Siffi C., Iacumin P., Gerdol R. Mass loss and nutrient release during litter decay in peatland: The role of microbial adaptability to litter chemistry. Soil Biology and Biochemistry 2007;39(1) 257-267.
60 - González G., Seastedt TR. Soil fauna and plant litter decomposition in tropical and subalpine forests. Ecology 2001;82(4) 955-964.
61 - Xuluc-Tolosa FJ., Vester HFM., Ramírez-Marcial N., Castellanos-Albores J., Lawrence D. Leaf litter decomposition of tree species in three successional phases of tropical dry secondary forest in Campeche, Mexico. Forest Ecology and Management 2003;174(1) 401-412.
62 - Harguindeguy NP., Blundo CM., Gurvich DE., Díaz S., Cuevas E. More than the sum of its parts? Assessing litter heterogeneity effects on the decomposition of litter mixtures through leaf chemistry. Plant and Soil 2008;303(1-2) 151-159.
63 - Castanho CT., Oliveira AA. Relative effect of litter quality, forest type and their interaction on leaf decomposition in south-east Brazilian forests. Journal of Tropical Ecology 2008;24(2) 149-156.
64 - Muscardi DC., Schoereder JH., Sperber CF. Biodiversity and ecosystem functioning: a conceptual model of leaf litter decomposition. In: Oscar Grillo. (ed.). Biodiversity-The Dynamic Balance of the Planet. Rijeka: Intech; 2014. p33-50.
65 - Lavelle P., Blanchart E., Martin S., Martin A. A hierarchical model for decomposition in terrestrial ecosystems: Application to soils in the humid tropics. Biotropica 1993;25(2) 130-150.
66 - Aerts R. Climate, leaf litter chemistry and leaf litter decomposition in terrestrial ecosystems: a triangular relationship. Oikos 1997;79(3) 439-449.
67 - Cotrufo M., Del Gado F., Piermatteo ID. Litter decomposition: concepts, methods and future perspectives. In: Soil Carbon Dinamics. An integrated methodology. Kutsch WL., Bahn M., Heinemeyer A. (eds.). Cambridge: University Press; 2009. p76-90.
68 - Hättenschwiler S., Coq S., Barantal S., Handa IT. Leaf traits and decomposition in tropical rainforests: revisiting some commonly held views and towards a new hypothesis. New Phytologist 2011;189(4) 950-965.
69 - Melillo JM., Aber JD., Muratore JF. Nitrogen and lignin control of hardwood leaf litter decomposition dynamics. Ecology 1982;63(3) 621-626.
70 - Li LJ., Zeng DH., Yu ZY., Fan ZP., Yang D., Liu YX. Impact of litter quality and soil nutrient availability on leaf decomposition rate in a semi-arid grassland of Northeast China. Journal of Arid Environments 2011;75(9) 787-792.
71 - Smith VC., Bradford MA. Do non-additive effects on decomposition in litter-mix experiments result from differences in resource quality between litters? Oikos 2003;102(2) 235-242.
72 - Kurzatkowski D., Martius C., Höfer H., Garcia M., Förster B., Beck L., Vlek P. Litter decomposition, microbial biomass and activity of soil organisms in three agroforestry sites in central Amazonia. Nutrient Cycling in Agroecosystems 2004;69(3) 257-267.
73 - Wickings K., Grandy AS. The oribatid mite Scheloribates moestus (Acari:Oribatida) alters litter chemistry and nutrient cycling during decomposition. Soil Biology and Biochemistry 2011;43(2) 351-358.
74 - Pramanik R., Sarkar K., Joy VC. Efficiency of detritivore soil arthropods in mobilizing nutrients from leaf litter. Tropical Ecology 2001;42(1) 51-58.
75 - Coleman DC., Crossley DA. Fundamentals of Soil Ecology. London: Academic Press; 1996.
76 - Spain AV., Lavelle P., Mariotti A. Stimulation of plant growth by tropical earthworms. Soil Biology and Biochemistry 1992;24(12) 162-1633.
77 - Bardgett RD., Chan KF. Experimental evidence that soil fauna enhance nutrient mineralization and plant nutrient uptake in montane grassland ecosystems. Soil Biology and Biochemistry. Oxford 1999;31(7) 1007-1014.
78 - Hunt HW., Wall DH. Modelling the effects of loss of soil biodiversity on eco-system function. Global Change Biology 2002;8(1) 33-50.
79 - Duffy JE., Cardinale BJ., France KE., McIntyre PB., Thébault E., Loreau M. The functional role of biodiversity in ecosystems: Incorporating trophic complexity. Ecology Letters 2007;10(6) 522-538.
80 - Veloso HP., Rangel Filho ALR., Lima JCA. editors. Classificação da vegetação brasileira, adaptada a um sistema universal. Rio de Janeiro: IBGE; 1991.
81 - Mason CF. Decomposição. São Paulo: Editora da Universidade de São Paulo; 1980.
82 - Moore JC., Walter DE., Hunt HW. Arthropod regulation of micro-and mesobiota in bellow-ground detrital food webs. Annual Reviews of Entomology 1988;33 419-439.
83 - Höfer H., Hanagarth W., Martius C., Beck L., Garcia M. Soil fauna and litter decomposition in primary and secondary forest and a mixed culture system in Amazonia. Manaus: EMBRAPA; 1998.
84 - Delabie JHC., Agosti D., Nascimento IC. Litter ant communities of the Brazilian Atlantic rain forest region. In: Agosti D., Majer JD., Tennant L., Schultz T. (eds). Sampling Ground-dwelling Ants: Case. Studies from the World’s Rainforests. Western Australia: Curtin-School of Environmental Biology; 2000.
85 - Correia MEF. Potencial de Utilização dos Atributos das Comunidades de Fauna de Solo e de Grupos Chave de Invertebrados como Bioindicadores do Manejo de Ecossistemas. Seropédica: Embrapa Agrobiologia; 2002.
86 - Marinoni RC, Ganho NG, Monné ML, Mermudes JRM. Hábitos alimentares de Coleoptera (Insecta). Ribeirão Preto: Holos; 2003.
87 - Burnham KP., Anderson DR. Model selection and multimodel inference: a practical information-theoretic approach. New York: Springer; 2002.
88 - Grueber CE., Nakagawa S., Laws RJ., Jamieson IG. Multimodel inference in ecology and evolution: challenges and solutions. Journal of Evolutionary Biology 2011;24(4) 699-711.
89 - Zuur AF., Ieno EN., Elphick CS. A protocol for data exploration to avoid common statistical problems. Methods in Ecology and Evolution 2010;1 3-14.
90 - Barton, K. Package ‘MuMIn’. Model selection and model averaging based on information criteria. 2012. R package version 1.7.11
91 - Schielzeth H. Simple means to improve the interpretability of regression coefficients. Methods in Ecology and Evolution 2010;1(2) 103-113.
92 - R Development Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna: Austria; url; 2014.
93 - Krantz GW., Walter DE. A manual of acarology. 3ed. Texas: Tech University Press; 2009.
94 - Collevatti RG., Schoereder JH. Microclimate ordination and litter arthropod distribution. Journal of the Brasilian Association for the Advanced of Science 1995;47 38-40.
95 - Louzada JNC., Schoereder JH., De Marco Jr P. Litter decomposition in semideciduous forest and Eucalyptus spp. crop in Brazil: a comparison. Forest Ecology and Management 1997;94(1) 31-36.
96 - Correia MEF., Andrade AD., Santos GA., Camargo FDO. Formação de serapilheira e ciclagem de nutrientes. Fundamentos da matéria orgânica do solo: ecossistemas tropicais e subtropicais. Porto Alegre: Gênesis; 1999.
97 - Lavelle P. Diversity of soil fauna and ecosystem function. Biology International 1996;33 3-16.
98 - Tilman D. Biodiversity: population versus ecosystem stability. Ecology 1996;77(2) 350-363.
99 - Tilman D., Knops J., Wedin D., Reich P., Ritchie M., Siemann E. The influence of functional diversity and composition on ecosystem processes. Science 1997;277(5330) 1300-1302.
100 - Hooper DU., Vitousek PM. Effects of plant composition and diversity on nutrient cycling. Ecological Monographs 1998;68(1) 121-149.
101 - Symstad AJ., Tilman D. Diversity loss, recruitment limitation, and ecosystem functioning: lessons learned from a removal experiment. Oikos 2001; 92(3) 424-435.
102 - Tilman D., Knops J., Wedin D., Reich P. Plant diversity and composition: effects on productivity and nutrients dynamics of experimental grasslands. In: In: Naeem S., Loreau M., Inchausti P. (eds.) Biodiversity and Ecosystem Functioning: Synthesis and Perspective. Oxford: University Press: 2002. P12-294.
103 - Aarssen LW., Laird RA., Pither J. Is the productivity of vegetation plots higher or lower when there are more species? Variable predictions from interaction of the 'sampling effect' and 'competitive dominance effect' on the habitat templet. Oikos 2003;102(2) 427-432.
104 - Wardle DA., Bonner KI., Nicholson KS. Biodiversity and plant litter: experimental evidence which does not support the view that enhanced species richness improves ecosystem function. Oikos 1997;79(2) 247-258.
105 - Schwartz MW., Brigham CA., Hoeksema JD., Lyons KG., Mills MH., Mantgem PJ. Linking biodiversity to ecosystem function: implications for conservation ecology. Oecologia 2000;122(3) 297-305.
106 - Wang S., Ruan H., Wang B. Effects of soil micro arthropods on plant litter decomposition across an elevation gradient in the Wuyi Mountains. Soil Biology and Biochemistry 2009;41(5) 891-897.
107 - Song F., Fan X., Song R. Review of mixed forest litter decomposition researches. Acta Ecologica Sinica 2010;30(4) 221-225.
108 - Inouye RS., Byers GS., Brown JH. Effects of predation and competition on survivorship, fecundidy, and community structure of desert annuals. Ecology 1980;61(6) 1344-1351.
109 - Menge BA., Sutherland J.P. Community regulation: variation in disturbance, competition and predation in relation to environmental stress and recruitment. American Naturalist 1987;130(5) 730-757.
110 - Savolainen R., Vepsalainen K. A competition hierarchy among boreal ants: Impact on resource partitioning and community structure. Oikos 1988;51(2) 135-155.
111 - Stachowics JJ. Mutualism, facilitation, and the structure of ecological communities positive interactions play a critical, but underappreciated, role in ecological communities by reducing physical or biotic stresses in existing habitats and by creating new habitats on which many species depend. BioScience 2001;51(3) 235-246.
112 - Heil M., McKey D. Protective ant-plant interactions as model systems in ecological and evoluctionary Research. Annual Review of Ecology, Evolution, and Systematics 2003;34 425-453.
113 - Rudgers JA. Enemies of herbivores can shape plant traits: Selection in a facultative ant-plant mutualism. Ecology 2004;85(1) 192-205.
114 - Chamberlain SA., Holland JN. Quantitative synthesis of context dependency in ant-plant protection mutualisms. Ecology 2009;90(9) 2384-2392.
115 - Nathan R., Muller-Landau HC. Spatial patterns of seed dispersal, their determinants and consequences for recruitment. Trends in ecology and evolution 2000;15(7) 278-285.
116 - Schoereder JH., Sobrinho TG., Madureira MS., Ribas CR., Oliveira PS. The arboreal ants community visiting extrafloral nectaries in the Neotropical Cerrado Savanna. Terrestrial Arthropod Reviews 2010;3(1) 3-27.
117 - Davidson DW., McKey D. Evolutionary Ecology of Symbiotic ant-plant relationships. Journal of Hymenoptera Research 1993;2(1) 13-83.
118 - Oliveira PS., Pie MR. Interaction between ants and plants bearing extrafloral nectaries in Cerrado vegetation. Anais da Sociedade Entomologica do Brasil 1998;27(2) 161-176.
119 - Goitía W., Jaffé K. Ant-Plant Associations in different forests in Venezuela. Neotropical Entomology 2009;38(1) 7-31.
120 - Bronstein JL., Alárcon R., Geber M. The evolution of plant-insects mutualisms. New Phytologist 2006;172(3) 412-428.
121 - Rico-Gray V., Oliveira PS. The ecology and evolution of ant-plant interactions. Chicago: The University of Chicago Press; 2007.
122 - Baker DA., Hall JL., Thorpe JL. A study of the extrafloral nectaries of Ricinus communis. New Phytologist 1978;81(1) 129-137.
123 - Oliveira PS., Freitas AVL. Ant-plant-herbivore interaction in the neotropical cerrado savanna. Naturwessenschaften 2004;91(12) 557-570.
124 - Del-Claro K., Berto V., Réu W. Effect of herbivore deterrance by ants on the fruit set of an extrafloral nectary plant Qualea multiflora (Vochysiaceae). Journal of Tropical Ecology 1996;12(6) 887-892.
125 - Costa FM., Oliveira-Filho AT., Oliveira PS. The role of extrafloral nectaries in Qualea grandiflora (Vochysiaceae) in limiting herbivory: An experiment of ant protection in Cerrado vegetation. Ecological Entomology 1992;17(4) 363-365.
126 - Sobrinho TG., Schoereder JH., Rodrigues LL., Collevatti RG. Ant Visitation (Hymenoptera: Formicidae) to Extrafloral Nectaries Increases Seed Set and Seed Viability in the Tropical Weed Triumfetta semitriloba. Sociobiology 2002;39(2) 353-368.
127 - Rosumek FB., Silveira FAO., Neves FS., Barbosa NPU., Diniz L., Oki Y., Pezzini F., Fernandes GW., Cornelissen T. Ants on plants: a meta-analysis of the roles of ants as plant biotic defenses. Oecologia 2009;160(3) 537-549.
128 - O’Dowd DJ., Cathpole EA. Ants and extrafloral nectaries: No evidence for plant protection in Helicrysum spp. Oecologia 1983;59(2-3) 191-200.
129 - Byk J., Del-Claro K. Nectar-and pollen-gathering Cephalotes ants provide no protection against herbivory: A new manipulative experiment to test ant protective capabilities. Acta Ethologica 2010;13(1) 33-38.
130 - Way MJ. Mutualism between ants and honeydew-producing Homoptera. Annual Review of Entomol 1963;8(1) 307-344.
131 - Davidson DW. The role of resource imbalances in the evolutionary ecology of tropical arboreal ants. Biological Journal of the Linnean Society 1997;81(2) 153-181.
132 - Delabie JHC. Trofhobiosis between Formicidae and Hemiptera (Sternoeehyncha and Auchenorryncha): an Overview. Neotropical Entomology 2001;30(4) 501-516.
133 - Grinath JB., Inouye BD., Underwood N., Billick I. The indirect consequences of a mutualism: comparing positive and negative components of the net interaction between honeydew-tending ants and host plants. Journal of Animal Ecology 2012;81(2) 494-502.
134 - Rice KB., Eubanks MD. No Enemies Needed: Cotton Aphids (Hemiptera: Aphididae) Directly Benefit from Red Imported Fire Ant (Hymenoptera: Formicidae) Tending. Florida Entomologist 2013;96(3) 929-932.
135 - Ratter JA., Ribeiro JF., Bridgewater S. The Brazilian cerrado vegetation and threats to its biodiversity. Annals of Botany 1997;80(3) 223-230.
136 - Ribeiro JF., Walter BMT., Sano SM., Almeida SD. Fitofisionomias do bioma Cerrado. Cerrado: ambiente e flora. Brasília: Embrapa; 1998.
137 - Almeida SD., Proença SEB., Sano SM., Ribeiro JF. Cerrado: Espécies Vegetais Úteis. Brasília: Embrapa; 1998.
138 - Oliveira PS., Da Silva AF., Martins AB. Ant foraging on extrafloral nectaries of Qualea grandiflora (Vochysiaceae) in Cerrado vegetation: ants as potential antiherbivore agents. Oecologia 1987;74(2) 228-230.
139 - Schiavini I., Araújo GM. Considerações sobre a vegetação da Reserva Ecológica do Panga (Uberlândia). Sociedade e Natureza 1989;1 61-66.
140 - Moreno MIC., Schiavini I. Relação entre vegetação e solo em um gradiente florestal na Estação Ecológica do Panga, Uberlândia (MG). Revista Brasileira de Botânica 2001;24(4) 537-544
141 - Rosa R., Lima SC., Assunção LW. Abordagem preliminar das condições climáticas de Uberlândia (MG). Sociedade e Natureza 1991;3 91-108.
142 - Ribas CR., Schoereder JH., Pic M., Soares SM. Tree heterogeneity, resource availability, and larger scale processes regulating arboreal ant species richness. Austral Ecology 2003;28(3) 305-314.
143 - Gallo D., Nakano O., Silveira Neto S., Carvalho RL., Batista GD., Berti Filho E., Parra JRP., Zucchi RA., Alves SB., Vendramim J. D. Manual de Entomologia Agrícola. 2vol. São Paulo: Agronômica Ceres;1978.
144 - Basset Y. Diversity and abundance of insect herbivores collected on Castanopsis acuminatissima (Fagaceae) in New Guinea: Relationship with leaf production and surrounding vegetation. European Journal of Entomology 1999;96(4) 381-391.
145 - Crawley MJ. The R Book. Hoboken: Wiley; 2007
146 - Joner F., Blanco C., Sosinski Jr EE., Muller SC., Pillar VD. Riqueza, redundância funcional e resistência de comunidades campestres sob pastejo. Revista Brasileira de Biociências 2008;5 528-530.
147 - Bentley BR. The protective function of ants visiting the extrafloral nectaries of Bixa orellana (Bixaceae). Journal of Ecology 1977;65 27-38.
148 - Katayama N., Hembry DH., Hojo MK., Suzuki N. Why do ants shift their foraging from extrafloral nectar to aphid honeydew?. Ecological Research, 2013;28(5) 919-926.
149 - Bluthgen N., Verhaagh M., Goitía W., Jaffé K., Morawetz W., Barthlott W. How plants shape the ant community in the Amazonian rainforest canopy: the key role of extrafloral nectaries and homopteran honeydew. Oecologia 2000;125(2) 229-240.
150 - Savage AM., Rudgers JA. Non-additive benefit or cost? Disentangling the direct effects that occur when plants bearing extrafloral nectaries and honeydew-producing insects share exotic ants mutualists. Annals of Botany 2013;111 1295-1307.
151 - Perfecto I., Snelling R. Biodiversity and the transformation of a tropical agrosystem: Ants in coffe plantations. Ecological Application 1995;5 1084-1097.
152 - Oliveira OS., Oliveira-Filho AT. Distribution of Extrafloral Nectaries in the Wood Flora of Tropical Communities in Western Brazil. In: Price PW., Lewinsohn TM., Fernandes G W., Benson WW. (eds.) Plant-Animal Interactions: Evolutionary Ecology in Tropical and Temperate Regions: New York: Wiley-Interscience; 1991.
153 - Stein A., Gerstner K., Kreft H. Environmental heterogeneity as a universal driver of species richness across taxa, biomes and spatial scales. Ecology letters 2014;17(7) 866-880.
154 - Hoekstra JM., Boucher TM., Ricketts TH., Roberts C. Confronting a biome crisis: global disparities of habitat loss and protection. Ecology Letters 2005;8(1) 23-29.
155 - Turner WR., Brandon K., Brooks TM., Costanza R., Da Fonseca GA., Portela R. Global conservation of biodiversity and ecosystem services. Bioscience 2007;57(10) 868-873.
156 - Fahrig L. Effects of habitat fragmentation on biodiversity. Annual Review of Ecology, evolution, and Systematics 2003;34 487-515.
157 - Swift TL., Hannon SJ. Critical thresholds associated with habitat loss: a review of the concepts, evidence, and applications. Biological Reviews 2010;85(1) 35-53.
158 - MacArthur RH., MacArthur JW. On bird species diversity. Ecology 1961;42(3) 594-598.
159 - Lawton JH. Plant architecture and the diversity of phytophagous insects. Annual Review of Entomology 1983;28(1) 23-39.
160 - Tews JU., Brose V., Grimm K., Tielbörger MC., SchwagerWM., Jeltsch F. Animal species diversity driven by habitat heterogeneity/diversity: the importance of keystone structures. Journal of Biogeography 2004;31(1) 79-92.
161 - Hutchinson GE. Concluding remarks. Cold Spring Harbor Symposia on Quantitative Biology 1957;22 415-427.
162 - Chase JM., Leibold MA. Ecological Niches: linking classical and contemporary approaches. Chicago: University Press; 2003.
163 - Kadmon R., Allouche O. Integrating the effects of area, isolation, and habitat heterogeneity on species diversity: a unification of island biogeography and niche theory. The American Naturalist 2007;170(3) 443-454.
164 - Allouche O., Kalyuzhny M., Moreno-Rueda G., Pizarro M., Kadmon R. Area–heterogeneity tradeoff and the diversity of ecological communities. Proceedings of the National Academy of Sciences 2012;109(43) 17495-17500.
165 - MacArthur RH. Environmental factors affecting birds pecies diversity. American Naturalist 1964;98 387-396.
166 - Kerr JT., Packer L. Habitat heterogeneity as determine mammalian of species richness in high-energy regions. Nature 1997;385(6613) 252-254.
167 - ABRAF. Anuário estatístico ABRAF 2013 ano base 2012. Brasília: ABRAF; 2013. p148.
168 - Barlow J., Gardner TA., Ferreira LV., Peres CA. Litter fall and decomposition in primary, secondary and plantation forests in the Brazilian Amazon. Forest Ecology and Management 2007;247(1) 91-97.
169 - Parrotta JA. Productivity, nutrient cycling, and succession in single-and mixed-species plantations of Casuarina equisetifolia, Eucalyptus robusta, and Leucaena leucocephala in Puerto Rico. Forest Ecology and Management 1999;124(1) 45-77.
170 - Neuschulz EL., Botzat A., Farwig N. Effects of forest modification on bird community composition and seed removal in a heterogeneous landscape in South Africa. Oikos 2011;120(9) 1371-1379.
171 - Bond W., Slingsby P. Collapse of an ant-plant mutalism: the Argentine ant (Iridomyrmex humilis) and myrmecochorous Proteaceae. Ecology 1984;65(4) 1031-1037.
172 - Auld TD., Denham AJ. The role of ants and mammals in dispersal and post-dispersal seed predation of the shrubs Grevillea (Proteaceae). Plant Ecology 1999;144(2) 201-213.
173 - Davidson DW., Morton SR. Myrmecochory in some plants (F. Chenopodiaceae) of the Australian arid zone. Oecologia 1981;50(3) 357-366.
174 - Beattie AJ. The evolutionary ecology of ant-plant mutualisms. Cambridge: University Press; 1985.
175 - Boyd RS. Ecological benefits of myrmecochory for the endangered chaparral shrub Fremontodendron decumbens (Sterculiaceae). American Journal of Botany 2001;88(2) 234-241.
176 - Christian CE. Consequences of a biological invasion reveal the importance of mutualism for plant communities. Nature 2001;413(6856) 635-639.
177 - Wheelwright NT., Orians GH. Seed dispersal by animals: contrasts with pollen dispersal, problems of terminology, and constraints on coevolution. American Naturalist 1982;119 (3) 402-413.
178 - Blüthgen N., Menzel F., Hovestadt T., Fiala B., Blüthgen N. Specialization, constraints, and conflicting interests in mutualistic networks. Current Biology 2007;17(4) 341-346.
179 - Heithaus ER. Seed predation by rodents on three antdispersed plants. Ecology 1981;62(1) 136-145.
180 - Higashi S., Tsuyuzaki S., Ohara M., Ito F. Adaptive advantages of ant-dispersed seeds in the myrmecochorous plant Trillium Tschonoskii (Liliaceae). Oikos 1989;54 389-394.
181 - Manzaneda AJ., Fedriani JM., Rey PJ. Adaptive advantages of myrmecochory: The predator-avoidance hypothesis tested over a wide geographic range. Ecography 2005;28(5) 583-592.
182 - Culver DC., Beattie AJ. Myrmecochory in Viola: dynamics of seed-ant interactions in some West Virginia species. The journal of Ecology 1978;66(1) 53-72.
183 - Hanzawa FM., Beattie AJ., Culver DC. Directed dispersal: demographic analysis of an ant-seed mutualism. American Naturalist 1988;131(1) 1-13.
184 - Andersen AN. Dispersal distance as a benefit of myrmecochory.Oecologia 1988;75(4) 507-511.
185 - Lomov B., Keith DA., Hochuli DF. Linking ecological function to species composition in ecological restoration: Seed removal by ants in recreated woodland. Austral Ecology 2009;34(7) 751-760.
186 - Armbrecht I., Rivera L., Perfecto I. Reduced diversity and complexity in the leaf-litter ant assemblage of Colombian coffee plantations. Conservation Biology 2005;19(3) 897-907.
187 - Braga DL., Louzada JNC., Zanetti R., Delabie JHC. Avaliação rápida da diversidade de formigas em sistemas de uso do solo no sul da Bahia. Neotropical Entomology 2010;39(4) 464-469.
188 - Suguituru SS., Silva RR., Souza DRD., Munhae CDB., Morini MSDC. Ant community richness and composition across a gradient from Eucalyptus plantations to secondary Atlantic Forest. Biota Neotropica 2011;11(1) 369-376.
189 - Schmidt FA., Ribas CR., Schoereder JH. How predictable is the response of ant assemblages to natural forest recovery? Implications for their use as bioindicators. Ecological Indicators 2013;24 158-166.
190 - Crist TO. Biodiversity, species interactions, and functional roles of ants (Hymenoptera: Formicidae) in fragmented landscapes: a review Myrmecological News 2009;12 3-13.
191 - Silveira JM., Barlow J., Louzada J., Moutinho P. Factors Affecting the Abundance of Leaf-Litter Arthropods in Unburned and Thrice-Burned Seasonally-Dry Amazonian Forests. Plos One 2010;5(9) 12877.
192 - Palacio EE., Fernández F. Claves para las subfamilias y géneros. In: Fernández F. (ed). Introducción a las hormigas de la region Neotropical. Bogotá: Instituto de Investigación de Recursos Biológicos Alexander von Humbolt 2003. P26-398.
193 - Anderson MJ. A new method for non-parametric multivariate analysis of variance. Austral Ecology 2001;26(1) 32-46.
194 - Gove AD., Majer JD., Dunn RR. A keystone ant species promotes seed dispersal in a ‘‘diffuse’’ mutualism. Oecologia 2007;153(3) 687-697.
195 - Loreau M., Naeem S., Inchausti P., Bengtsson J., Grime J. P., Hector, A., Hooper D. U., Huston M. A., Raffaelli D., Schmid B., Tilman D., Wardle DA. Biodiversity and ecosystem functioning: current knowledge and future challenges. Science 2001;294 (5543) 804-808.
196 - Western D. Human-modified ecosystems and future evolution. Proceedings of the National Academy of Sciences 2001;98(10) 5458-5465.
197 - Majer JD, Day JE, Kabbay ED, Perriman WS. Recolonization by ants in bauxite mines rehabilitated by a number of different methods. Journal of Applied Ecology 1984; 21 355-375.
198 - Palmer TM. Spatial habitat heterogeneity influences competition and coexistence in an african acacia ant guild. Ecology 2003;84(11) 2843-2855.
199 - Lassau SA., Cassis G., Flemons PKJ., Wilkie L., Hochuli DF. Using high-resolution multi-spectral imagery to estimate habitat complexity in open-canopy forests: can we predict ant community patterns? Ecography 2005;28(4) 495-504.
200 - Paolucci LN., Solar RRC., Schoereder JH. Litter and associated ant fauna recovery dynamics after a complete clearance. Sociobiology 2010;55(1) 133-144.
201 - Loreau M. Are communities saturated? On the relationship between alpha, beta and gamma diversity. Ecology Letters 2000;3(2) 73-76.
202 - Hooper, DU., Adair EC., Cardinale BJ., Byrnes J E K., Hungate BA., Matulich K L., Gonzalez A., Duffy J E., Gamfeldt L., O’Connor M I. A global synthesis reveals biodiversity loss as a major driver of ecosystem change. Nature 2012;486 105-108.