The Cerrado occupies about 23% of the Brazilian territory and is characterized by great diversity of plants and insects and a great degree of endemism, and Caryocar brasiliense A. St.-Hil. (Malpighiales: Caryocaraceae) is widely distributed in this region. The diversity and abundance of hemipterans and their natural enemies were studied on trees of C. brasiliense in the Cerrado, pasture, and anthropic area in Montes Claros, Minas Gerais State, Brazil. We observed 1 rare, 8 common, and 1 frequent species of sucking insects; and 2 rare, 7 common, and 6 frequent species of natural enemies. Sucking insects and their natural enemies were most abundant in the pasture and least abundant in the Cerrado. Increasing diversity indices and numbers of species and individuals of sucking insects were followed by similar trends in the populations of natural enemies. Increasing populations of sucking insects led to greater numbers of individuals of ants, green lacewings, predator thrips, and ladybeetles. Aluminum level positively affected the number of species and individuals, and the pH of the soil reduced those of sucking insects. Leafhoppers had greater numbers on plants on soils with low pH values and high aluminum levels, but the opposite was noted for the aphids.
Caryocar brasiliense A. St.-Hil. (Malpighiales: Caryocaraceae) trees have a wide distribution in the Brazilian Cerrado (Brandão & Gavilanes 1992; Bridgewater et al. 2004; Leite et al. 2006a) and can form a canopy of over 10 m height and 6 m width (Leite et al. 2006a, 2011a,b, 2012). The fruits have a mesocarp rich in oil, vitamins, and proteins and contain many compounds of medicinal importance. The tree is also used by humans for food, the production of cosmetics and lubricants, and in the pharmaceutical industry (Araújo 1995; Segall et al. 2005; Ferreira & Junqueira 2007; Garcia et al. 2007; Khouri et al. 2007). This plant is the main source of income in many communities (Leite et al. 2006a).
Caryocar brasiliense trees are protected by Brazilian laws and thus left in deforested areas of the Cerrado. However, in northern Minas Gerais State, in general, their natural regeneration is restricted to areas with impoverished soils (sandy or rocky outcrop) (Leite et al. 2006a). Isolated trees suffer high leaf, flower, and fruit damage from sucking insects (personal communication from collectors of fruits), but this damage is poorly studied (Araújo 1995), mainly due to lack of specialists (Freitas & Oliveira 1996; Oliveira 1997; Lopes et al. 2003; Boiça et al. 2004; Leite et al. 2009, 2011a,b, 2012).
The diversity and abundance of arthropods can vary among environments, and several hypotheses can explain this fact: 1) complex environments increase the number of herbivore species and their predators associated with a host plant and, generally, decrease their abundance (Auslander et al. 2003; Lazo et al. 2007); 2) host plant attributes such as complex architecture can increase the diversity of herbivorous insects (Espírito-Santo et al. 2007); and 3) soil characteristics that are favorable to trees can indirectly effect herbivorous insects (e.g., through nutritional quality) (Auslander et al. 2003; Espírito-Santo et al. 2007).
We tested, for the first time, these 3 hypotheses—complex environments, host plant attributes, and soil characteristics—in relation to the diversity and abundance of Hemiptera herbivores and their natural enemies on C. brasiliense trees in 3 areas. Each area represented unique habitat conditions: 1) preserved Cerrado, 2) Cerrado cleaned for pasture, and 3) Cerrado converted to urban development, i.e., an anthropic area (a university campus).
Materials and Methods
The study was conducted in the municipality of Montes Claros, Minas Gerais State, Brazil, during 3 consecutive years (Jun 2008 through Jun 2011) in 3 areas of a region with dry winters, rainy summers, and Aw climate (tropical savanna) according to Köppen (Vianello & Alves 2000). The areas were: 1) Cerrado sensu stricto (16.7487778°S, 43.9186944°W, at 943 m, with dystrophic red yellow latosol of sandy texture); 2) pasture, formerly Cerrado vegetation (16.7711389°S, 43.9587222°W, at 940 m, with dystrophic red yellow latosol of loamy texture), and 3) anthropic area, campus of the “Instituto de Ciências Agrárias da Universidade Federal de Minas Gerais” (16.6818056°S, 43.8407778°W, at 633 m, with dystrophic red latosol of medium texture) (Leite et al. 2006a, 2011a), near to a vegetable production area (approx. 400 m distance). We used the soil data already published by Leite et al. (2006a, 2011a), who had collected soil samples in the same areas.
The Cerrado sensu stricto (a species-rich dense scrub of shrubs and trees, 8–10 m in height, with a dense understory), common for the Brazilian Cerrado, is an open grassland (Ribeiro & Walter 1998; Durigan et al. 2002). The Cerrado area of our study had 44.87% grass (soil covering), 5.78% shrubs, 23.51% small trees, 8.76% big trees, and 17.00% C. brasiliense trees per ha. The pasture area had 84.19% grass (soil covering) (Brachiaria decumbens Stapf; Poales: Poaceae), 0.19% shrubs, 4.76% small trees, 2.76% big trees, and 42.30% C. brasiliense trees per ha. The anthropic area had 100% grass (soil covering) (Paspalum notatum Flüggé) and 100 C. brasiliense trees per ha (for detailed description of the sites see Leite et al. 2006a, 2011a).
Mature C. brasiliense trees were 4.07 ± 0.18 m high (mean ± standard error) with a crown width of 2.87 ± 0.13 m in the Cerrado; 5.20 ± 0.18 m high with a crown width of 3.96 ± 0.14 m in the pasture; and 3.79 ± 0.15 m high with a crown width of 1.66 ± 0.13 m in the anthropic area (Leite et al. 2006a, 2011a). We used the plant data already published by Leite et al. (2006a, 2011a) and collected from the same plants and areas.
Leaves of C. brasiliense are alternate, trifoliate, and with high trichome density; flowers are hermaphrodite but mostly cross-pollinated (Araújo 1995). Fruit production is annual, and C. brasiliense trees bloom between Jul and Sep (dry period) with fructification from Oct to Jan (rainy season) (Leite et al. 2006a). Fruits are a drupe with 1 to 4 seeds, weigh 158.49 ± 8.14 g (fresh weigh), and have a volume of 314.90 ± 20.93 cm3 (Leite et al. 2006a).
The design was completely randomized with 12 replications (1 tree per replicate) and 3 treatments (areas). Caryocar brasiliense trees were identified in a 600 m straight line per area, and every 50 m a random plant was evaluated. Mature trees of C. brasiliense (producing fruits) were randomly sampled per collection, except in the anthropic area, where trees were evaluated every time.
The number of Hemiptera and arthropod natural enemies was evaluated monthly in the morning on 4 leaves, 4 flowers, and 4 fruits per tree and area by direct observation during 3 yr (Horowitz 1993). Insects on leaves, flowers, and fruits were collected with tweezers, brush, or aspirators and preserved in vials with 70% alcohol for identification.
The number of sucking insects and natural enemies, species richness, and diversity were calculated per tree and area. All ecological indices were measured by calculating the dataset of taxa by samples in BioDiversity Pro Version 2 software. Hill's formula (Hill 1973) was used to calculate the diversity and the Simpson indices for abundance and species richness (Lazo et al. 2007). Species of sucking insects and natural enemies were classified as: a) frequent (frequency ≥⃒ 50%), b) common (10% < frequency ≤⃒ 49%), and c) rare (frequency ≤⃒ 10%) in the samples.
Simple regression analyses were made to compare the diversity index, number of individuals. and number of species of sucking insects with the diversity index, number of individuals, and number of species of natural enemies; the numbers of ants, predator thrips and bugs, spiders, ladybeetles, and green lacewings with those of sucking insects; and the chemical characteristics of the soils (Leite et al. 2006a) and height and crown width of the plants (Leite et al. 2006a) with the numbers of sucking insects and their natural enemies. Results were subjected to analysis of variance (ANOVA) (P < 0.05) and simple regression analysis (P < 0.05) using the System of Statistical and Genetics Analysis of the Federal University of Viçosa. The effect of the areas on ecological indices and number of individuals per species of sucking insects and their natural enemies was tested with ANOVA (P < 0.05) and Tukey's test (P < 0.05), carried out using the same software.
Hill's diversity index, number of individuals, and number of species of sucking insects and their natural enemies per Caryocar brasiliense tree in 3 areas of Montes Claros, Minas Gerais, Brazil.
Order, family, and species of arthropods and their feeding behavior and abundance observed on Caryocar brasiliense trees in Montes Claros, Minas Gerais, Brazil.
In total, 1,728 leaves, 300 flowers (Jul–Sep), and 320 fruits (Sep–Jan) of C. brasiliense were evaluated during the 3 yr in the 3 areas. The diversity index of sucking insects and natural enemies was similar between areas. However, sucking insects and natural enemies were more abundant in the pasture than in the Cerrado. The number of species of sucking insects and their natural enemies was greatest in the pasture and smallest in the Cerrado (Table 1). One rare, 8 common, and 1 frequent species of sucking insects and 2 rare, 7 common, and 6 frequent species of natural enemies were found on C. brasiliense trees (Table 2).
The numbers of the Hemiptera Aconophora sp. (Membracidae) on fruit peduncles and Dikrella caryocar Coelho, Leite and Da Silva (Coelho et al. 2014) (Cicadellidae), Edessa rufomarginata De Geer (Pentatomidae), Frequenamia sp. (Cicadellidae), and Mahanarva sp. (Cercopidae) on leaves of C. brasiliense trees were greater in the pasture than in the other areas. On the other hand, aphids, whiteflies, and a membracid (unidentified) had larger populations in the anthropic area than in the other areas (Table 3).
The number of natural enemies Crematogaster sp. (Hymenoptera: Formicidae) was greatest on leaves, flowers, and fruits of C. brasiliense trees in the pasture; those of Epipolops sp. (Hemiptera: Geocoridae) bugs, Neocalvia fulgurata Mulsant (Coleoptera: Coccinellidae) lady beetles, and Trybonia sp. (Thysanoptera: Phlaeothripidae) thrips on leaves, and of spiders on flowers also were greatest in the pasture (Table 4). Numbers of Pseudomyrmex termitarius Smith (Hymenoptera: Formicidae) ants on leaves were greatest in the Cerrado, whereas numbers of Camponotus novogranadensis Mayr (Hymenoptera: Formicidae) ants, green lacewings (Chrysoperla sp.; Neuroptera: Chrysopidae), spiders, and Zelus armillatus (Lepeletier & Serville) (Hemiptera: Reduviidae) bugs on leaves were greatest in the anthropic area (Table 4). Holopothrips sp. (Thysanoptera: Phlaeothripidae) thrips showed lowest abundance on leaves of C. brasiliense trees in the Cerrado (Table 4).
Numbers of sucking insects on leaves (L), flowers (Fl), and fruits (Fr) per Caryocar brasiliense tree in 3 areas of Montes Claros, Minas Gerais, Brazil.
The diversity index, number of species, and number of individuals of sucking insects and those values for natural enemies were positively correlated. Population increase of sucking insects was also positively correlated with that of ants, green lacewings, predator thrips, and lady beetles (Fig. 1).
Increasing level of aluminum positively affected the number of species and individuals and that of pH in the soil negatively affected the number of individuals of sucking insects on C. brasiliense trees (Fig. 2). Numbers of D. caryocar were greater on plants on soils with lower pH and higher aluminum level, but the opposite was noted for the aphids (Fig. 3).
Canopy size also influenced the abundance and diversity of sucking insects and their natural enemies. The diversity index and number of individuals of sucking insects, diversity index, number of species, and number of individuals of natural enemies (Fig. 2), number of D. caryocar (Fig. 3), and the number of ants, predator thrips, and lady beetles (Fig. 4) were higher on C. brasiliense trees with larger than on trees with smaller canopy.
Numbers of natural enemies on leaves (L), flowers (Fl), and fruits (Fr) per Caryocar brasiliense tree in 3 areas of Montes Claros, Minas Gerais, Brazil.
The largest number of sucking insects and their natural enemies on C. brasiliense trees in the pasture (versus in the Cerrado and in the anthropic area) may be explained by a combination of factors. First, the pasture environment, in our study, with C. brasiliense trees, grass, and other trees and shrubs had a more diversified condition than a traditional pasture (grass only) (Leite et al. 2006a, 2011a), increasing the number of sucking insect species. Second, C. brasiliense trees presented wider and higher crowns (complexity in the structure) in the pasture than in the other 2 areas, increasing food resources (Leite et al. 2006a). Third, soil characteristics in the pasture were most favorable to C. brasiliense trees—increasing their crown and consequently their fruit production (Leite et al. 2006a, 2011a, 2012), which indirectly benefitted hemipteran herbivores and natural enemies. The large numbers of aphids, whiteflies, and mealybugs and their natural enemy green lacewings on C. brasiliense trees in the anthropic area may be due to its proximity to vegetable production areas (i.e., okra, tomato). Environmental complexity and host plant attributes (such as architecture and nutritional quality) influence the diversity of arthropods, both phytophagous ones and natural enemies (Auslander et al. 2003; Espírito-Santo et al. 2007; Lazo et al. 2007; Leite et al. 2011b, 2012). The number of species associated with a given host in less complex environments may be low but with generally high population abundance, hence giving herbivores pest status (Landis et al. 2000; Gonçalves-Alvim & Fernandes 2001; Gratton & Denno 2003; Coyle et al. 2005).
The positive correlation between sucking insects on C. brasiliense plants with high aluminum level and acidic soils, except Aphis gossypii (Glover) (Hemiptera: Aphididae) (a pest of several crops), may be due to the loamier soil in the pasture than in the anthropic area (silt and compressed texture) and the Cerrado (sandy texture) (Leite et al. 2006a). Soils of the Cerrado are generally deep and loamy (excellent storage capacity for rainfall water) but poor in nutrients, rich in aluminum, and with low pH (Sousa & Lobato 2004). The soil in the pasture had higher levels of aluminum and lower pH values along with lower levels of calcium, potassium, and magnesium than soil in the anthropic area (Leite et al. 2006a). Caryocar brasiliense (Oliveira 1997; Leite et al. 2006a) and its native sucking insect species may have adapted to these conditions.
The greatest number of the predators Z. armillatus, Holopothrips sp., and spiders on C. brasiliense trees in the anthropic area might be due to higher number of leaves galled by Eurytoma sp. (Hymenoptera: Eurytomidae) in these trees than in trees of the other 2 areas (unpublished data). These predators preyed on galling insects that colonize up to 70% of leaf area with galls (Leite et al. 2009). Eurytoma sp. and aphids are very abundant on leaves of seedlings and mature C. brasiliense trees in the anthropic area (Leite et al. 2006b, 2007).
The positive correlation between natural enemies and sucking insects on C. brasiliense trees shows that mobile predators can respond to local increase in vegetation complexity and alternative prey to effectively suppress herbivores (Auslander et al. 2003). Ants can reduce infestations by E. rufomarginata, Eunica bechina Hewitson (Lepidoptera: Nymphalidae), Prodiplosis floricola (Felt) (Diptera: Cecidomyiidae), and petiole gall insects (Hymenoptera: Chalcidoidea) on C. brasiliense (Freitas & Oliveira 1996; Oliveira 1997). Also, spiders, predator bugs and thrips, green lacewings, and lady beetles are important natural enemies in various ecosystems (Landis et al. 2000; Almeida et al. 2006; Mizell 2007; Oberg et al. 2008; Venturino et al. 2008). Spiders and invertebrate predators often have a high population density in complex vegetation (plant architecture) independent of prey (Landis et al. 2000). High population density of these natural enemies was also attributed to microclimate or reduction of cannibalism and intraguild competition (Langellotto 2002).
A more diverse environment and, principally, higher structure of plant crown (complexity of the architecture) favored populations of sucking insects and of their natural enemies. The positive effect of high aluminum levels and acidic soils on sucking insects (except aphids) indicates the adaptation of these species to the Cerrado conditions. Besides, it reinforces the importance of sucking insects in arboreal systems of the Brazilian Cerrado and the necessity of studying their population dynamics.
We thank A. D. Brescovit (Instituto Butantã; Arachnida), A. M. Bello (Coleoptera), I. C. Nascimento (EMBRAPA; Formicidae), C. Matrangolo (UNIMONTES; Formicidae), C. R. S. Silva (UFSCAR; Aphididae), A. L. B. G. Peronti (UFSCAR; Pseudococcidae), L. B. N. Coelho (UFRJ; Cicadellidae), and R. C. Monteiro (Thysanoptera) for the identification of the specimens collected. We also thank CNPq, FAPEMIG, and Secretaria de Ciência e Tecnologia do Estado de Minas Gerais for financial support.