*Dirección para correspondencia

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Abstract

Simplification of natural habitats leads to a modification of the community associated with a host plant. Pequi trees (Caryocar brasiliense) are common to find in central Brazil, especially in the middle of monocultures, such as soy, corn, pasturelands or Eucalyptus plantations. On this scenario we hypothesized that habitat modification differentially affects the diversity of ants and herbivore insects associated with this species. The aim of the work was to test if C. brasiliense trees located in human modified habitats, support a lower species richness and abundance of ants, and a greater species richness and abundance of insect herbivores, compared to preserved cerrado habitats. The study was conducted in a Cerrado area located in Northern Minas Gerais State, Brazil. Ants and herbivore insects were collected monthly during 2005 using beating technique. The results showed that ant species richness was higher in pequi trees located in preserved Cerrado, followed by trees in pastureland and Eucalyptus plantation, respectively. The ant abundance was lower in the Eucalyptus plantation but no difference in ant abundance was observed between trees in pastureland and the preserved Cerrado. Moreover, herbivore insects exhibited lower number of species and individuals in trees located in the preserved Cerrado than in the pastureland and Eucalyptus plantation. We concluded that habitats simplified by human activities may result in diversity loss and may change species interactions.

Key words: environmental complexity, habitat management, insect diversity, pequi trees, tri-trophic interactions.

Resumen

La simplificación de los hábitats naturales conduce a una modificación de la comunidad asociada con una planta huésped. En la región central de Brasil es muy común encontrar árboles aislados de “pequi” (Caryocar brasiliense) en medio de monocultivos de soya, maíz, pastos o plantaciones de eucalipto. Bajo este escenario, nosotros predecimos que la modificación del hábitat afecta diferencialmente la diversidad de hormigas y herbívoros asociados a árboles de “pequi”. El objetivo de este artículo fue determinar que árboles de “pequi” localizados en hábitats modificados por actividades humanas (i.e. pastizales y plantaciones de Eucalyptus), soportan una menor abundancia y riqueza de especies de hormigas. Por el contrario, se espera una mayor abundancia y riqueza de especies de herbívoros en hábitats modificados. Este estudio fue realizado en un área de Cerrado (sabana brasileña) localizado en el Norte del estado de Minas Gerais, Brasil. Las hormigas y los herbívoros fueron muestreados usando técnicas de golpe. La riqueza de especies de hormigas fue mayor en árboles de “pequi” localizados en áreas preservadas de Cerrado, seguida por árboles de pastizales y finalmente por árboles de plantaciones de Eucalyptus. La abundancia de hormigas fue menor en plantaciones de Eucalyptus, pero no hubo diferencias en la abundancia de hormigas entre árboles de pastizales y áreas preservadas de cerrado. Por otra parte, el número de especies de insectos herbívoros fue menor en árboles de áreas preservadas de Cerrado que en pastizales y plantaciones de Eucalyptus. Concluimos que las actividades humanas reducen la complejidad del hábitat resultando en la pérdida de la diversidad de insectos y procesos ecológicos.

Palabras clave: complejidad ambiental, manejo de hábitat, diversidad de insectos, árboles de “pequi”, interacciones tri-tróficas.

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Understanding natural patterns of ]]>

Caryocar brasiliense Camb. (Caryocaraceae) is a typical tree of the Brazilian Cerrado and it can be found from the Southern of Pará State, along the edge of the Amazon region, until the South of Paraná State and also in Paraguay (Gribel & Hay 1993). The extraction of pequi fruits is considered an important economic activity in different regions of ]]>

The pequi tree is legally protected in Minas Gerais State (Law 10,883 of 02-20-1992), but their natural ]]>

Besides the direct negative effect of ants on herbivores, habitat structure can modify ant diversity, causing an indirect effect on herbivores (Hoffmann & Andersen 2003, Lassau & Hochuli 2004, Rosumek et al. 2009). Few studies have focused on insect diversity in human modified habitats, including both, Eucalyptus forests and agricultural systems (Szinicz et al. 2005, ]]>

Materials and methods

Study area: The study was conducted in the Cerrado biome, in Morro Alto (16°53’17” S - 44°00’06’’ W), a district that belongs to Montes Claros municipality, Northern of Minas Gerais State (Brazil). The climate of the region is considered as tropical semi-arid (Peel et al. 2007), characterized by the existence of a severe dry season during the winter. The average temperature is 21°C and the annual rainfall is approximately 1 100mm, concentrated from November to January. To test the hypothesis, three adjacent habitats (500m), with similar soil characteristics and density of pequi trees, were chosen in the study area. Two habitats have been modified ]]> Eucalyptus plantation; and one preserved area (Cerrado strictu sensu physiognomy). In each habitat 15 trees of similar sizes (5-8m heights and diameter at breast height above 5cm) were marked in order to characterize the herbivore insects, and ant richness and abundance.

Sampling of ants and herbivore ]]> The effects of human impact on insect fauna associated with pequi trees were evaluated monthly throughout 2005. Ants and herbivore insects were sampled (08:00-11:00am) using the beating technique (Neves et al. 2010): for each selected plant, a branch was chosen at random (selected branches in small and large trees had approximately the same amount of leaves), and the branch was hit ten times with a beating stick in order to dislodge the associated arthropods on to a tray placed beneath. The insects collected were taken to the laboratory and sorted to the lowest taxonomic level possible, and deposited at the ]]>

A generalized linear model was used to verify the habitat effect on ant and insect herbivore richness and abundance. The mean number of species or individuals per tree over the 12 months of sampling was used as response variables in order to remove the temporal pseudoreplication. The habitats (preserved Cerrado, ]]> Eucalyptus plantation) were used as explanatory variables. The minimal model was constructed from the junction of qualitative factors (habitat), which were statistically different from the full model (analysis of contrast) (Crawley 2007). Next, a residual analysis was conducted to check data adequacy for the assumed probability distribution (Crawley 2007). All analysis was performed using the statistical program R (R Development Core Team 2010).

]]> Results

A total of 2 827 ants belonging to 42 species, 12 genera and four subfamilies were collected from C. brasiliense trees (Table 1). The two richest ant genera were Camponotus and Cephalotes, with 13 and 10 species, respectively. The ant species richness associated with pequi trees varied among habitats (Table 2). The preserved Cerrado trees had a higher ant richness (p<0.05), followed by those in pastureland and Eucalyptus plantation (Fig. 1A). Higher ant abundance was found in trees of the preserved Cerrado and pastureland, with no significant difference between them. While trees ]]> Eucalyptus plantation observed the lowest ant abundance (Fig. 1B).

The herbivore insects sampled on C. brasiliense trees were composed by 1 666 individuals (877 ]]> Table 3). The richness and abundance of chewing insects associated with these trees differed significantly among habitats (Table 2): these were ]]> Eucalyptus plantation (Fig. 1C, D).

The guild of sap-sucking insects sampled was grouped into 15 Hemiptera families. Aetalionidae (234 individuals) and Cicadellidae (21 morphospecies) were the most abundant ]]> Table 3). Sap-sucking insects showed the same pattern observed for chewing insects, with the richness and abundance being lower in pequi trees from the preserved Cerrado (p<0.05) than those from pastureland and Eucalyptus plantation (Table 2, Fig. 1 E, F).
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Discussion

Many studies have shown a positive relationship between diversity of terrestrial arthropods and habitat heterogeneity (Lassau & Hochuli 2004, Sperber et al. 2004). Positive relations between ant diversity and habitat heterogeneity can ]]> Eucalyptus plantation. This result indicates that variations in habitats due human activity negatively affected the ant fauna associated with pequi trees. Thus, the removal of native vegetation to establish Eucalyptus ]]>

We found that ant richness and ]]> Eucalyptus plantation than pasturelands. On the other hand, we did not find differences in ant abundance between preserved Cerrado and pasturelands. Probably this result may be influenced by two main factors. First, structural complexity of the preserved Cerrado seems to be much more similar to pastureland than Eucalyptus plantation. Second, disturbance intensity due human activities is certainty bigger and more frequent in Eucalyptus ]]> Eucalyptus area. This is the first study that shows the negative effect of pastureland and Eucalyptus plantation on ant richness.

In contrast, pequi trees located in preserved Cerrado had lower richness and abundance of insect herbivores ]]> Eucalyptus plantation. A similar result was found for herbivores from distinct feeding guilds between managed and conserved areas (Speight et al. 2003). Moreover, some studies indicate that insect herbivore’s natural enemies are more effective in pristine areas (Altieri & Letourneau 1982). Normally, predators and parasitoid insects species show high diversity in forest than herbivore insects, that can be pest in agricultural areas (Szinicz et al. 2005). Predators and parasites have a stronger negative effects on herbivores associated with Caryocar brasiliense ]]> Eucalyptus plantation and pastureland had positively affected the insect herbivore richness and abundance in these habitats. In contrast, tropical agroecosystems in Ecuador had a higher ratio of parasitoid to host species and increased parasitism rates (Tylianakis et al. 2007). In fact, many studies have reported high predation pressure by ants on arthropods (Heil & McKey 2003) while others showed that ant presence could reduce the herbivore insects abundance on their host plants (Oliveira 1997, Fagundes et al. ]]>

In addition to ants effects (Top-down effects), herbivore insects performance is also affected by host plant quality (Bottom-up effects) (Coley et al. 1985, Coley & Barone 1996). The resource availability hypothesis (Coley et al. 1985) predicts that plants with readily available light but low nutrient availability have elevated rates of carbon fixation and low investment ]]>

The present study shows that the ]]>

We suggest a decrease in the ]]> Eucalyptus plantations, and in this way the ant top-down effects on herbivore insects. The natural habitat preservation of the Brazilian Cerrado is very important for biodiversity conservation and ecosystem optimum function. Experimental studies on tri-trophic interaction and food webs could be essential to elucidate the patterns of insect distribution and the effect of habitat modification on insect biodiversity and ecological processes.

]]> Acknowledgments

We thanks Ronaldo Reis Júnior and Patrícia de Abreu Moreira for insightful comments on earlier drafts of the manuscript and two other anonymous referees who made valuable contributions to this paper. Financial support by the Fapemig (the Minas Gerais Research Foundation) and CNPq ]]>

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*Correspondencia:
Frederico S. Neves: Laboratório de Biologia da Conservação, Departamento de Biologia Geral, Universidade Estadual de Montes Claros, Montes claros, MG, Brasil/ Laboratório de Ecologia de Insetos, Departamento de Biologia Geral, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brasil. fred.neves@gmail.com.
Rodrigo F. Braga: Laboratório de Biologia da Conservação, Departamento de Biologia Geral, Universidade Estadual de Montes Claros, Montes claros, MG, Brasil. rodrigo.fagundes@yahoo.com.br.
Lucimar S. Araújo: Laboratório de Biologia da Conservação, Departamento de Biologia Geral, Universidade Estadual de Montes Claros, Montes claros, MG, Brasil. lucimar.araujo@gmail.com. ]]> Ricardo I. Campos: Laboratório de Ecologia de Formigas,Universidade Federal de Viçosa, 36570-000, Viçosa, MG, Brasil. ricardoicampos@gmail.com
Marcílio Fagundes: Laboratório de Biologia da Conservação, Departamento de Biologia Geral, Universidade Estadual de Montes Claros, Montes claros, MG, Brasil. marcilio.fagundes@unimontes.br.
1. Laboratório de Biologia da Conservação, Departamento de Biologia Geral, Universidade Estadual de Montes Claros, Montes claros, MG, Brasil; rodrigo.fagundes@yahoo.com.br, lucimar.araujo@gmail.com, marcilio.fagundes@unimontes.br
2. Laboratório de Ecologia de Insetos, Departamento de Biologia Geral, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brasil; fred.neves@gmail.com
3. Laboratório de Ecologia de Formigas,Universidade Federal de Viçosa, 36570-000, Viçosa, MG, Brasil; ricardoicampos@gmail.com

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