From insect-plant interactions to ecological networks / Das interações inseto-planta às redes ecológicas

Abstract Since its inception, biodiversity has largely been understood as species diversity and assessed as such. Interactions among species or functional groups are gradually becoming part of an expanded concept of biodiversity. As a case study of the development of a research program in biodiversity, we summarize our multi-decade studies on interactions of Asteraceae and flowerhead-feeding insects in Brazil. Initially, host species were treated as independent replicates in order to assess the local and turnover components of their herbivore diversity. Research then expanded into sampling entire interactive communities of host plants and their associated herbivores in different localities and regions, enabling new research lines to be pursued. Interaction diversity could be assessed and factored into spatial and among-host components, suggesting a new field of interaction geography. Second, host specialization, a key component of interaction diversity, was reframed considering simultaneously relatedness and local availability of plant hosts. Third, with the influence of complex network theory, community-wide species interactions were probed for topological patterns. Having identified the modular structure of these plant-herbivore systems, later we demonstrated that they fit a compound hierarchical topology, in which interactions are nested within large-scale modules. In a brief survey of research funded by Fapesp, especially within the Biota-Fapesp program, we highlight several lines of internationally recognized research on interaction diversity, notably on plant-frugivore and plant-pollinator interactions, together with new theoretical models. The interplay of field studies with new theoretical and analytical approaches has established interaction diversity as an essential component for monitoring, conserving and restoring biodiversity in its broader sense.

Resumo Desde seu início, a biodiversidade geralmente tem sido entendida e avaliada principalmente como diversidade de espécies. Interações entre espécies ou grupos funcionais vêm sendo incorporadas em um conceito expandido de biodiversidade. Como um estudo de caso da evolução de um programa de pesquisa em biodiversidade, resumimos aqui nossos estudos das interações de Asteráceas com insetos endófagos em capítulos no Brasil, desenvolvidos por várias décadas. Inicialmente a diversidade de herbívoros foi estimada em diferentes espécies hospedeiras, tratando-as como réplicas independentes para estimar os componentes locais e de substituição da diversidade dos insetos associados. Posteriormente, passamos a amostrar comunidades interativas de plantas e insetos associados em diferentes localidades e regiões, o que abriu novas linhas de investigação. A diversidade de interações, agora fatorada em componentes espaciais e inter-hospedeiras, sugere um novo campo, a geografia de interações. Em segundo lugar, um componente essencial da diversidade de interações, a especialização trófica, foi redefinida como função da contiguidade filogenética bem como da disponibilidade local de plantas hospedeiras. Terceiro, sob influência da teoria de redes complexas, foram investigados padrões topológicos de comunidades interativas. Identificamos a estrutura modular dessas comunidades de plantas e herbívoros; posteriormente, demonstramos a topologia hierárquica dessas interações, composta por módulos internamente aninhados. Numa revisão sucinta de pesquisas sustentadas pela Fapesp, especialmente no programa Biota-Fapesp, destacamos diversas linhas de pesquisa sobre diversidade de interações que alcançaram reconhecimento internacional, tais como interações de plantas e frugívoros ou polinizadores, além de novos modelos teóricos. A conjugação de estudos de campo com novas abordagens teóricas e analíticas firmou a diversidade de interações como um componente essencial para monitorar, conservar e restaurar a biodiversidade em seu sentido mais amplo.

Host age predicts parasite occurrence, richness, and nested infracommunities in a pilot whale-helminth network.

Ecological data on marine mammal parasites represent an excellent opportunity to expand our understanding of host-parasite systems. In this study, we used a dataset of intestinal helminth parasites on 167 long-finned pilot whales Globicephala melas (Traill, 1809) from seven localities in the Faroe Islands to evaluate the extent to which the host's age and sex influence the occurrence, richness, and nested pattern of helminth parasites and the importance of individual hosts to the helminth community. We found positive effects of age on both the occurrence and richness of helminths. Older host individuals showed an ordered accumulation of parasites, as evidenced by the nested pattern in their composition. Males had a higher occurrence of parasites than females, but the richness of helminths did not differ between sexes. Our findings suggest that differences in host-parasite interactions in long-finned pilot whales result mainly from age-structured variations in biological and behavioral characteristics.

Pollinator restoration in Brazilian ecosystems relies on a small but phylogenetically-diverse set of plant families.

The alarming rate of global pollinator decline has made habitat restoration for pollinators a conservation priority. At the same time, empirical and theoretical studies on plant-pollinator networks have demonstrated that plant species are not equally important for pollinator community persistence and restoration. However, the scarcity of comprehensive datasets on plant-pollinator networks in tropical ecosystems constrains their practical value for pollinator restoration. As closely-related species often share traits that determine ecological interactions, phylogenetic relationships could inform restoration programs in data-scarce regions. Here, we use quantitative bee-plant networks from Brazilian ecosystems to test if priority plant species for different restoration criteria (bee species richness and visitation rates) can be identified using interaction networks; if phylogenetic relationships alone can guide plant species selection; and how restoration criteria influence restored network properties and function. We found plant species that maximised the benefits of habitat restoration for bees (i.e., generalists and those with distinct flower-visitor species) were clustered in a small number of phylogenetically-diverse plant families, and that prioritising the recovery of bee visitation rates improved both stability and function of restored plant-pollinator networks. Our approach can help guide restoration of pollinator communities, even where information on local ecosystems is limited.

Changing interactions among persistent species as the major driver of seasonal turnover in plant-caterpillar interactions.

ß diversity of herbivorous insects in the tropics is usually very high, and there is often strong dissimilarity in herbivore species composition across different spatial scales and different abiotic gradients. Similarly, turnover is high for trophic interactions between herbivorous insects and their host plants. Two factors have been proposed to explain temporal or spatial differences in trophic interactions: changes in species composition and temporal changes in the behavior of shared species. The goal of this study was to evaluate determinants of high ß diversity of trophic interactions between lepidopteran caterpillars and their host plants across dry and rainy seasons and their transitions. Over the course of a year, interaction diversity data were collected from 275 temporary plots in Cerrado vegetation, comprising 257 species of caterpillars, 137 species of host plants and 503 different trophic interactions. All these diversity parameters varied across seasons. Species assemblages of caterpillars and plants were different among the four seasons, and there was a high turnover of interactions between the seasons. The high temporal ß diversity of trophic interactions was mostly due to interaction rewiring between co-occurring species, as opposed to changes in species composition over time.

Host-Plant Specialization Mediates the Influence of Plant Abundance on Host Use by Flower Head-Feeding Insects.

Among-population variation in host use is a common phenomenon in herbivorous insects. The simplest and most trivial explanation for such variation in host use is the among-site variation in plant species composition. Another aspect that can influence spatial variation in host use is the relative abundance of each host-plant species compared to all available hosts. Here, we used endophagous insects that develop in flower heads of Asteraceae species as a study system to investigate how plant abundance influences the pattern of host-plant use by herbivorous insects with distinct levels of host-range specialization. Only herbivores recorded on three or more host species were included in this study. In particular, we tested two related hypotheses: 1) plant abundance has a positive effect on the host-plant preference of herbivorous insects, and 2) the relative importance of plant abundance to host-plant preference is greater for herbivorous species that use a wider range of host-plant species. We analyzed 11 herbivore species in 20 remnants of Cerrado in Southeastern Brazil. For 8 out of 11 herbivore species, plant abundance had a positive influence on host use. In contrast to our expectation, both the most specialized and the most generalist herbivores showed a stronger positive effect of plant species abundance in host use. Thus, we found evidence that although the abundance of plant species is a major factor determining the preferential use of host plants, its relative importance is mediated by the host-range specialization of herbivores.

The Effect of Host-Plant Phylogenetic Isolation on Species Richness, Composition and Specialization of Insect Herbivores: A Comparison between Native and Exotic Hosts.

Understanding the drivers of plant-insect interactions is still a key issue in terrestrial ecology. Here, we used 30 well-defined plant-herbivore assemblages to assess the effects of host plant phylogenetic isolation and origin (native vs. exotic) on the species richness, composition and specialization of the insect herbivore fauna on co-occurring plant species. We also tested for differences in such effects between assemblages composed exclusively of exophagous and endophagous herbivores. We found a consistent negative effect of the phylogenetic isolation of host plants on the richness, similarity and specialization of their insect herbivore faunas. Notably, except for Jaccard dissimilarity, the effect of phylogenetic isolation on the insect herbivore faunas did not vary between native and exotic plants. Our findings show that the phylogenetic isolation of host plants is a key factor that influences the richness, composition and specialization of their local herbivore faunas, regardless of the host plant origin.

The colonisation of exotic species does not have to trigger faunal homogenisation: lessons from the assembly patterns of arthropods on oceanic islands.

Human-caused disturbances can lead to the extinction of indigenous (endemic and native) species, while facilitating and increasing the colonisation of exotic species; this increase can, in turn, promote the similarity of species compositions between sites if human-disturbed sites are consistently invaded by a regionally species-poor pool of exotic species. In this study, we analysed the extent to which epigean arthropod assemblages of four islands of the Azorean archipelago are characterised by nestedness according to a habitat-altered gradient. The degree of nestedness represents the extent to which less ubiquitous species occur in subsets of sites occupied by the more widespread species, resulting in an ordered loss/gain of species across environmental or ecological gradients. A predictable loss of species across communities while maintaining others may lead to more similar communities (i.e. lower beta-diversity). In contrast, anti-nestedness occurs when different species tend to occupy distinct sites, thus characterising a replacement of species across such gradients. Our results showed that an increase in exotic species does not promote assemblage homogenisation at the habitat level. On the contrary, exotic species were revealed as habitat specialists that constitute new and well-differentiated assemblages, even increasing the species compositional heterogeneity within human-altered landscapes. Therefore, contrary to expectations, our results show that both indigenous and exotic species established idiosyncratic assemblages within habitats and islands. We suggest that both the historical extinction of indigenous species in disturbed habitats and the habitat-specialised character of some exotic invasions have contributed to the construction of current assemblages.

The patterns of organisation and structure of interactions in a fish-parasite network of a neotropical river.

The use of the complex network approach to study host-parasite interactions has helped to improve the understanding of the structure and dynamics of ecological communities. In this study, this network approach is applied to evaluate the patterns of organisation and structure of interactions in a fish-parasite network of a neotropical Atlantic Forest river. The network includes 20 fish species and 73 metazoan parasite species collected from the Guandu River, Rio de Janeiro State, Brazil. According to the usual measures in studies of networks, the organisation of the network was evaluated using measures of host susceptibility, parasite dependence, interaction asymmetry, species strength and complementary specialisation of each species as well as the network. The network structure was evaluated using connectance, nestedness and modularity measures. Host susceptibility typically presented low values, whereas parasite dependence was high. The asymmetry and species strength were correlated with host taxonomy but not with parasite taxonomy. Differences among parasite taxonomic groups in the complementary specialisation of each species on hosts were also observed. However, the complementary specialisation and species strength values were not correlated. The network had a high complementary specialisation, low connectance and nestedness, and high modularity, thus indicating variability in the roles of species in the network organisation and the expected presence of many specialist species.

Contrasting effects of land use intensity and exotic host plants on the specialization of interactions in plant-herbivore networks.

Human land use tends to decrease the diversity of native plant species and facilitate the invasion and establishment of exotic ones. Such changes in land use and plant community composition usually have negative impacts on the assemblages of native herbivorous insects. Highly specialized herbivores are expected to be especially sensitive to land use intensification and the presence of exotic plant species because they are neither capable of consuming alternative plant species of the native flora nor exotic plant species. Therefore, higher levels of land use intensity might reduce the proportion of highly specialized herbivores, which ultimately would lead to changes in the specialization of interactions in plant-herbivore networks. This study investigates the community-wide effects of land use intensity on the degree of specialization of 72 plant-herbivore networks, including effects mediated by the increase in the proportion of exotic plant species. Contrary to our expectation, the net effect of land use intensity on network specialization was positive. However, this positive effect of land use intensity was partially canceled by an opposite effect of the proportion of exotic plant species on network specialization. When we analyzed networks composed exclusively of endophagous herbivores separately from those composed exclusively of exophagous herbivores, we found that only endophages showed a consistent change in network specialization at higher land use levels. Altogether, these results indicate that land use intensity is an important ecological driver of network specialization, by way of reducing the local host range of herbivore guilds with highly specialized feeding habits. However, because the effect of land use intensity is offset by an opposite effect owing to the proportion of exotic host species, the net effect of land use in a given herbivore assemblage will likely depend on the extent of the replacement of native host species with exotic ones.

A simple stochastic model for complex coextinctions in mutualistic networks: robustness decreases with connectance.

Understanding and predicting species extinctions and coextinctions is a major goal of ecological research in the face of a biodiversity crisis. Typically, models based on network topology are used to simulate coextinctions in mutualistic networks. However, such topological models neglect two key biological features of species interactions: variation in the intrinsic dependence of species on the mutualism, and variation in the relative importance of each interacting partner. By incorporating both types of variation, we developed a stochastic coextinction model capable of simulating extinction cascades far more complex than those observed in previous topological models. Using a set of empirical mutualistic networks, we show that the traditional topological model may either underestimate or overestimate the number and likelihood of coextinctions, depending on the intrinsic dependence of species on the mutualism. More importantly, contrary to topological models, our stochastic model predicts extinction cascades to be more likely in highly connected mutualistic communities.

Amphibian beta diversity in the Brazilian Atlantic Forest: contrasting the roles of historical events and contemporary conditions at different spatial scales.

Current patterns of biodiversity distribution result from a combination of historical and contemporary processes. Here, we compiled checklists of amphibian species to assess the roles of long-term climate stability (Quaternary oscillations), contemporary environmental gradients and geographical distance as determinants of change in amphibian taxonomic and phylogenetic composition in the Brazilian Atlantic Forest. We calculated beta diversity as both variation in species composition (CBD) and phylogenetic differentiation (PBD) among the assemblages. In both cases, overall beta diversity was partitioned into two basic components: species replacement and difference in species richness. Our results suggest that the CBD and PBD of amphibians are determined by spatial turnover. Geographical distance, current environmental gradients and long-term climatic conditions were complementary predictors of the variation in CBD and PBD of amphibian species. Furthermore, the turnover components between sites from different regions and between sites within the stable region were greater than between sites within the unstable region. On the other hand, the proportion of beta-diversity due to species richness difference for both CBD and PBD was higher between sites in the unstable region than between sites in the stable region. The high turnover components from CBD and PBD between sites in unstable vs stable regions suggest that these distinct regions have different biogeographic histories. Sites in the stable region shared distinct clades that might have led to greater diversity, whereas sites in the unstable region shared close relatives. Taken together, these results indicate that speciation, environmental filtering and limited dispersal are complementary drivers of beta-diversity of amphibian assemblages in the Brazilian Atlantic Forest.

An integrated framework to improve the concept of resource specialisation.

Resource specialisation, although a fundamental component of ecological theory, is employed in disparate ways. Most definitions derive from simple counts of resource species. We build on recent advances in ecophylogenetics and null model analysis to propose a concept of specialisation that comprises affinities among resources as well as their co-occurrence with consumers. In the distance-based specialisation index (DSI), specialisation is measured as relatedness (phylogenetic or otherwise) of resources, scaled by the null expectation of random use of locally available resources. Thus, specialists use significantly clustered sets of resources, whereas generalists use over-dispersed resources. Intermediate species are classed as indiscriminate consumers. The effectiveness of this approach was assessed with differentially restricted null models, applied to a data set of 168 herbivorous insect species and their hosts. Incorporation of plant relatedness and relative abundance greatly improved specialisation measures compared to taxon counts or simpler null models, which overestimate the fraction of specialists, a problem compounded by insufficient sampling effort. This framework disambiguates the concept of specialisation with an explicit measure applicable to any mode of affinity among resource classes, and is also linked to ecological and evolutionary processes. This will enable a more rigorous deployment of ecological specialisation in empirical and theoretical studies.

Plant-pollinator coextinctions and the loss of plant functional and phylogenetic diversity.

Plant-pollinator coextinctions are likely to become more frequent as habitat alteration and climate change continue to threaten pollinators. The consequences of the resulting collapse of plant communities will depend partly on how quickly plant functional and phylogenetic diversity decline following pollinator extinctions. We investigated the functional and phylogenetic consequences of pollinator extinctions by simulating coextinctions in seven plant-pollinator networks coupled with independent data on plant phylogeny and functional traits. Declines in plant functional diversity were slower than expected under a scenario of random extinctions, while phylogenetic diversity often decreased faster than expected by chance. Our results show that plant functional diversity was relatively robust to plant-pollinator coextinctions, despite the underlying rapid loss of evolutionary history. Thus, our study suggests the possibility of uncoupled responses of functional and phylogenetic diversity to species coextinctions, highlighting the importance of considering both dimensions of biodiversity explicitly in ecological studies and when planning for the conservation of species and interactions.

Developmental stage of parasites influences the structure of fish-parasite networks.

Specialized interactions tend to be more common in systems that require strong reciprocal adaptation between species, such as those observed between parasites and hosts. Parasites exhibit a high diversity of species and life history strategies, presenting host specificity which increases the complexity of these antagonistic systems. However, most studies are limited to the description of interactions between a few parasite and host species, which restricts our understanding of these systems as a whole. We investigated the effect of the developmental stage of the parasite on the structure of 30 metazoan fish-parasite networks, with an emphasis on the specificity of the interactions, connectance and modularity. We assessed the functional role of each species in modular networks and its interactions within and among the modules according to the developmental stage (larval and adult) and taxonomic group of the parasites. We observed that most parasite and host species perform a few interactions but that parasites at the larval stage tended to be generalists, increasing the network connectivity within and among modules. The parasite groups did not differ among each other in the number of interactions within and among the modules when considering only species at the larval stage. However, the same groups of adult individuals differed from each other in their interaction patterns, which were related to variations in the degree of host specificity at this stage. Our results show that the interaction pattern of fishes with parasites, such as acanthocephalans, cestodes, digeneans and nematodes, is more closely associated with their developmental stage than their phylogenetic history. This finding corroborates the hypothesis that the life history of parasites results in adaptations that cross phylogenetic boundaries.

Phytophagous insect fauna tracks host plant responses to exotic grass invasion.

The high dependence of herbivorous insects on their host plants implies that plant invaders can affect these insects directly, by not providing a suitable habitat, or indirectly, by altering host plant availability. In this study, we sampled Asteraceae flower heads in cerrado remnants with varying levels of exotic grass invasion to evaluate whether invasive grasses have a direct effect on herbivore richness independent of the current disturbance level and host plant richness. By classifying herbivores according to the degree of host plant specialization, we also investigated whether invasive grasses reduce the uniqueness of the herbivorous assemblages. Herbivorous insect richness showed a unimodal relationship with invasive grass cover that was significantly explained only by way of the variation in host plant richness. The same result was found for polyphagous and oligophagous insects, but monophages showed a significant negative response to the intensity of the grass invasion that was independent of host plant richness. Our findings lend support to the hypothesis that the aggregate effect of invasive plants on herbivores tends to mirror the effects of invasive plants on host plants. In addition, exotic plants affect specialist insects differently from generalist insects; thus exotic plants affect not only the size but also the structural profile of herbivorous insect assemblages.

Integrating economic costs and biological traits into global conservation priorities for carnivores.

BACKGROUND: Prioritization schemes usually highlight species-rich areas, where many species are at imminent risk of extinction. To be ecologically relevant these schemes should also include species biological traits into area-setting methods. Furthermore, in a world of limited funds for conservation, conservation action is constrained by land acquisition costs. Hence, including economic costs into conservation priorities can substantially improve their conservation cost-effectiveness. METHODOLOGY/PRINCIPAL FINDINGS: We examined four global conservation scenarios for carnivores based on the joint mapping of economic costs and species biological traits. These scenarios identify the most cost-effective priority sets of ecoregions, indicating best investment opportunities for safeguarding every carnivore species, and also establish priority sets that can maximize species representation in areas harboring highly vulnerable species. We compared these results with a scenario that minimizes the total number of ecoregions required for conserving all species, irrespective of other factors. We found that cost-effective conservation investments should focus on 41 ecoregions highlighted in the scenario that consider simultaneously both ecoregion vulnerability and economic costs of land acquisition. Ecoregions included in priority sets under these criteria should yield best returns of investments since they harbor species with high extinction risk and have lower mean land cost. CONCLUSIONS/SIGNIFICANCE: Our study highlights ecoregions of particular importance for the conservation of the world's carnivores defining global conservation priorities in analyses that encompass socioeconomic and life-history factors. We consider the identification of a comprehensive priority-set of areas as a first step towards an in-situ biodiversity maintenance strategy.

New host-plant records for neotropical agromyzids (Diptera: Agromyzidae) from Asteraceae flower heads.

Agromyzidae is a large and cosmopolitan fly family with approximately 2,500 known species. Here we present 22 new records of agromyzid-host plant associations. Plants were sampled from 2002 to 2005 in São Paulo state, Brazil. A total of eight agromyzid species were reared from 18 Asteraceae host species. The genus Melanagromyza Hendel was the commonest. This is the first detailed study reporting associations between non-leafmining Agromyzidae and their host plants in Brazil.

New host-plant records for neotropical agromyzids (Diptera: Agromyzidae) from Asteraceae flower heads

Agromyzidae is a large and cosmopolitan fly family with approximately 2,500 known species. Here we present 22 new records of agromyzid-host plant associations. Plants were sampled from 2002 to 2005 in São Paulo state, Brazil. A total of eight agromyzid species were reared from 18 Asteraceae host species. The genus Melanagromyza Hendel was the commonest. This is the first detailed study reporting associations between non-leafmining Agromyzidae and their host plants in Brazil.

A família Agromyzidae contém aproximadamente 2.500 espécies fitófagas conhecidas. Aqui são apresentados 22 novos registros de associação entre agromizídeos e suas plantas hospedeiras. Foram realizadas coletas entre 2002 e 2005 em remanescentes de cerrado no estado de São Paulo. As oito espécies de agromizídeos registradas pertencem ao gênero Melanagromyza Hendel e foram coletadas em 18 espécies de Asteraceae. Este é o primeiro estudo detalhado sobre associações entre agromizídeos não-minadores e suas plantas hospedeiras no Brasil.

Assemblages of endophagous insects on Asteraceae in São Paulo cerrados.

A survey of the endophagous insects fauna associated to Asteraceae capitula was carried out from 2000 to 2002 in eight cerrado sensu stricto sites located in the Brazilian state of Sdo Paulo. Sixty-four endophagous species of Diptera and Lepidoptera were recorded from 49 asteracean host plants. Approximately half of the species were obtained from a single locality, with a large proportion emerging from a single sample (unicates). Thirty percent of the species were singletons (i.e. only one individual was recorded). The large proportion of rare species suggests a high species turnover among localities. Lepidopteran species were recorded on more host species than dipterans, confirming their more polyphagous food habit, also observed in other Brazilian biomes and in Europe. We conclude that the studied cerrado localities, all within São Paulo State, are isolated with its invertebrate fauna composed of many rare and exclusive species. We suggest that the maintenance of Asteraceae biodiversity and their endophagous insects depend on the conservation of all cerrado remnants in the state.

Assemblages of endophagous insects on Asteraceae in São Paulo Cerrados

A survey of the endophagous insects fauna associated to Asteraceae capitula was carried out from 2000 to 2002 in eight cerrado sensu stricto sites located in the Brazilian state of São Paulo. Sixty-four endophagous species of Diptera and Lepidoptera were recorded from 49 asteracean host plants. Approximately half of the species were obtained from a single locality, with a large proportion emerging from a single sample (unicates). Thirty percent of the species were singletons (i.e. only one individual was recorded). The large proportion of rare species suggests a high species turnover among localities. Lepidopteran species were recorded on more host species than dipterans, confirming their more polyphagous food habit, also observed in other Brazilian biomes and in Europe. We conclude that the studied cerrado localities, all within São Paulo State, are isolated with its invertebrate fauna composed of many rare and exclusive species. We suggest that the maintenance of Asteraceae biodiversity and their endophagous insects depend on the conservation of all cerrado remnants in the state.

No presente estudo foi realizado um levantamento da fauna de insetos endófagos de capítulos de Asteraceae (Compostas), de 2000 a 2002, em oito localidades de cerrados sensu stricto no estado de São Paulo. Foram obtidas 64 espécies de endófagos (dípteros e lepidópteros) de 49 espécies de hospedeiras. Aproximadamente metade das espécies foi obtida de apenas uma área, e destas uma grande proporção ocorreu em apenas uma amostra (unicatas). Trinta por cento das espécies foram consideradas "singletons" (apenas um indivíduo foi obtido). A grande quantidade de espécies raras sugere uma forte troca de espécies entre diferentes áreas. Lepidópteros foram registrados em mais espécies hospedeiras que dípteros, confirmando o já observado para o mesmo sistema de insetos e plantas em outros ambientes no Brasil e Europa. As áreas de cerrado sensu stricto estudadas no estado de São Paulo encontram-se isoladas, com uma grande parte da fauna de invertebrados composta por muitas espécies raras e exclusivas. Diante deste quadro, sugere-se que a manutenção da biodiversidade de Asteraceae e seus endófagos em seus níveis atuais depende da conservação de todo o conjunto de remanescentes de cerrado do estado.