The Cerrado occupies about 23% of the Brazilian territory (Da Silva & Bates 2002) and is characterized by high diversity of plants and insects and represents a high degree of endemism (Bridgewater et al. 2004). Due to increasing threats to its biodiversity, the Cerrado has been selected as a biodiversity hotspot (Myers et al. 2000). The primary use of the Cerrado is for grain and cattle production (Aguiar & Camargo 2004). In addition, reforestation with exotic species, primarily Eucalyptus (Zanuncio et al. 2002) is underway. Through several governmental mechanisms and incentives the cerrado has been devastated in the last 5 decades leaving only 20% of the land intact (Klink & Machado 2005). Naturally, the cerrado is formed by a complex mosaic of phytophysiographies that range from open cerrado formations (campo limpo) up to tall and woody forests of 10–15 meters high, called Cerradão (Oliveira & Marquis 2002). In southeastern Brazil, large patches of this rich cerrado are seen immersed in a matrix of agriculture (primarily soybean and sugar cane), cattle farms and cities (urbanization). This is the case in Montes Claros in northern Minas Gerais state.

Caryocar brasiliense Camb. (Malpighiales: Caryocaraceae), a flagship species of the Cerrado for fomenting support for conservation, is widely distributed (Brandão & Gavilanes 1992; Bridgewater et al. 2004; Leite et al. 2006a) and can reach up to 10 meters high while the canopy may reach 6 meters wide (Leite et al. 2006a, 2011a, 2012a). The leaves of C. brasiliense are alternate, trifoliate and have high trichome density; the flowers are hermaphrodite but mostly cross pollinated. Fruit production is annual, and C. brasiliense blooms between Jul and Sep (dry period) and bears fruit from Oct into Jan (rainy season) (Leite et al. 2006a). The fruit is a drupe with 1–4 seeds, weighing 158.49 ± 8.14 g (fresh weigh) and with a volume of 314.90 ± 20.93 cm³ (Leite et al. 2006a). Its fruit has an internal mesocarp rich in oil, vitamins, and proteins, and contain many compounds of medicinal importance. Not surprisingly, pequi is widely used by humans for food, production of cosmetics, lubricants, and in the pharmaceutical industry (Segall et al. 2005; Ferreira & Junqueira 2007; Garcia et al. 2007; Khouri et al. 2007). This species represents the main source of income of many communities (Leite et al. 2006a). Caryocar brasiliense trees are protected by federal laws, and hence are left in deforested areas of the Cerrado. Fruit collectors have asserted that the leaves, flowers and fruits of isolated trees suffer high damage inflicted by sucking insects (Hemiptera) (personal communication from collectors of C. brasiliense fruits). On the other hand, the insects that damage C. brasiliense are poorly known and, in general, with only 1 species (Freitas & Oliveira 1996; Oliveira 1997; Lopes et al. 2003; Boiça et al. 2004; Leite et al. 2009, 2011a,b,c,d,e, 2012a,b,c). Insect pests of C. brasiliense number about 10 and include Eunica bechina (Talbot, 1852) (Lepidoptera: Nymphalidae), Edessa rufomarginata (De Geer, 1773) (Hemiptera: Pentatomidae), Prodiplosis floricola (Felt, 1908) (Diptera: Cecidomyiidae), Carmenta sp. (Lepidoptera: Sesiidae), Trigona spinipes (Fabr.) (Hymenoptera: Apidae), Eurytoma sp. (Hymenoptera, Eurytomidae), Bruchophagus sp. (Hymenoptera: Eurytomidae), and species belonging to Eulophidae (Hymenoptera), and Cossidae (Lepidoptera). The damages to C. brasiliense caused by these species individually or jointly are poor known and, in general, previous studies have focused on individual pest species without regard to others (Freitas & Oliveira 1996; Oliveira 1997, Lopes et al. 2003; Boiça et al. 2004; Leite et al. 2009, 2011a,b,c,d,e, 2012a,b,c). However, in the present study as many pest species as possible were included.

In order to better manage and protect the remaining C. brasiliense in the wild and on plantations, it is necessary to understand the ecology of the insects that interact with this economically valuable tree.

Our objective was to research the seasonality of sucking insects (Hemiptera) and their arthropod predators, and the phenophases of C. brasiliense that influences these arthropods on this tree, in strict sense Cerrado (a species-rich dense scrub of shrubs and trees, 8–10 m high and a dense understory) at Montes Claros in the state of Minas Gerais, Brazil.

MATERIAL AND METHODS

RESULTS

We observed 7 rare, 2 common, and 1 constant species of sucking insects; and 4 rare, 8 common, and 1 constant species of predatory arthropods on C. brasiliense trees (Table 1). The numbers of individuals of sucking insects were similar (P > 0.05) among the seasons of the year. However, there were more species and greatest diversity in the winter. Predators were most abundant in spring and winter, with highest diversity and number of species in winter (Tables 2 and 3).

With respect to sucking insects (Table 4), the numbers of Aconophora sp. (Membracidae) on fruits and Frequenamia sp. (Cicadellidae) on leaves were greatest in the winter; also greatest on the leaves in the spring were Aphis gossypii (Glover) (Aphididae) and Mahanarva sp. (Cercopidae). On the other hand Dikrella sp. (Hemiptera: Cicadellidae) were most abundant on the leaves in summer and autumn. With respect to predators (Table 5), Crematogaster sp. (Hymenoptera: Formicidae), had the lowest abundance on the leaves in the summer, and highest abundance in the flowers in the winter and spring, while it was prevalent on the fruits in the spring; Trybonia intermedius (Bagnall, 1910) and Trybonia mendesi (Moulton, 1933) (Thysanoptera: Phlaeothripidae) were most prevalent on the leaves in the autumn.

Higher numbers of ants Crematogaster sp. were observed in Caryocar brasiliense trees that had large numbers of Dikrella sp. (Hemiptera: Cicadellidae). Higher numbers of predators Trybonia sp. (Thysanoptera: Phlaeothripidae), Chrysoperla sp. (Neuroptera: Chrysopidae), and total of predator thrips were associated with decreasing numbers of Dikrella sp., A. gossypii, and total of sucking insects, respectively. The increase in the numbers of individuals and species of predators were correlated with the reduction of these same ecological parameters of the sucking insects (Fig. 1).

The highest temperatures and rainfall amounts were observed in spring, the highest RH in the summer, and longest daily h of sunlight in autumn and winter, but the lowest wind velocities were recorded in autumn (Table 6). Temperatures correlated negatively with the Hill's index of a number of predators, the number of species of sucking insects, the numbers of Trybonia sp. Thysanoptera per tree, and the number of Aconophora sp. (Membracidae) on the fruits per tree. On the other hand, increased of temperature correlated with increased numbers of Crematogaster sp. in flowers per tree and the numbers of Chrysoperla sp. on the leaves per tree (Fig. 2). Sunlight correlated negatively with the number of Crematogaster sp. on fruits per tree and Mahanarva sp. on the leaves per tree; rainfall correlated positively with the number of Crematogaster sp. on the flowers per tree and RH correlated negatively with the number of Zelus armillatus (Lep. and Servi) (Reduviidae) on the leaves per tree (Fig. 3).

TABLE 1.

ORDERS AND FAMILIES OF SPECIES OBSERVED ON CARYOCAR BRASILIENSE TREES, THE OBJECTS ON WHICH THEY FED AND THE FREQUENCIES OF THEIR OCCURRENCES DURING THE DAY AT MONTES CLAROS, MINAS GERAIS STATE, BRAZIL DURING AUTUMN 2008 TO AUTUMN 2011.

TABLE 2.

HILL'S DIVERSITY INDEX VALUES, NUMBERS OF INDIVIDUALS SPECIES OF ARTHROPOD PREDATORS, AND SUCKING INSECTS (HEMIPTERA) PER CARYOCAR BRASILIENSE TREE AT MONTES CLAROS, MINAS GERAIS STATE, BRAZIL DURING AUTUMN 2008 TO AUTUMN 2011.

TABLE 3.

ANOVA ANALYSIS OF THE EFFECT OF THE SEASONS ON THE ECOLOGICAL INDICES AND ABUNDANCES OF SUCKING INSECTS (HEMIPTERA) AND ARTHROPOD PREDATORS AT MONTES CLAROS, MINAS GERAIS STATE, BRAZIL DURING AUTUMN 2008 TO AUTUMN 2011.

TABLE 4.

NUMBERS OF SUCKING INSECTS (HEMPITERA)) ON LEAVES, FLOWERS AND FRUITS PER TREE OF CARYOCAR BRASILIENSE AT MONTES CLAROS, MINAS GERAIS STATE, BRAZIL DURING AUTUMN 2008 TO AUTUMN 2011.

TABLE 5.

NUMBERS OF ARTHROPOD PREDATORS ON LEAVES, FLOWERS AND FRUITS PER TREE OF CARYOCAR BRASILIENSE AT MONTES CLAROS, MINAS GERAIS STATE, BRAZIL DURING AUTUMN 2008 TO AUTUMN 2011.

TABLE 6.

TEMPERATURE (°C), RAINFALL (MM), RELATIVE HUMIDITY OF AIR (%), SUNLIGHT (H), AND VELOCITY OF WIND (M/SEC) AT MONTES CLAROS, MINAS GERAIS STATE, BRAZIL DURING AUTUMN 2008 To AUTUMN 2011.

DISCUSSION

The greater species richness and diversity of sucking insects in the winter is probably determined by the reduction in the number of C. brasiliense leaves available due to their gradual loss during the dry period and by the end of this season (Leite et al. 2006a), which results in a concentration of herbivore insects per leaf. The greatest species richness, abundance and diversity of the predators, which was observed in the winter, probably indicates that their populations depend on their prey and follow those of the sucking insects (Oberg et al. 2008; Venturino et al. 2008).

Fig. 1.

Relationships between numbers of species and individuals of arthropods predaceous and numbers of species and individuals of sucking insects, respectively; numbers of total predator thrips and numbers of total sucking insects; numbers of green lacewing and numbers of Aphis gossypii; numbers of Dikrella sp. and numbers of Trybonia sp. and Crematogaster sp., respectively, on Caryocar brasiliense trees in Montes Claros, Minas Gerais State, Brazil. Samples = 100.

Caryocar brasiliense loses its leaves in Aug/ Sep with new ones developing in Sep, a period without rainfall, strong winds and much sunlight (Leite et al. 2006a). In Sep we observed higher numbers of Frequenamia sp. cicadellids. Crematogaster sp. ants were also more abundant during the formation of new leaves and flowers at end of the winter probably due to the nectaries of the leaves and the flowers (Oliveira 1997; Orivel & Dejean 2002; Oliveira & Freitas 2004). Caryocar brasiliense begins to produces of fruit at the end of Sep. and start of Oct (Leite et al. 2006a), when Aconophora sp. membracids were very abundant. In addition, Crematogaster sp. visited fruits infested with Coleoptera and Lepidoptera borer species, perhaps because of the presence of sugary exudates of damaged C. brasiliense fruits (Leite et al. 2012b,c).

Fig. 2.

Relationships between temperature and Hill's index of arthropods predaceous, numbers of species of sucking insects, numbers of Crematogaster sp., numbers of Chrysoperla sp., numbers of Trybonia sp., and numbers of Aconophora sp., respectively, on Caryocar brasiliense trees in Montes Claros, Minas Gerais State, Brazil. Samples = 100.

Ants can reduce E. bechina infestations as well as E. rufomarginata, P. floricola and petiole gall insects (Hymenoptera: Chalcidoidea) on C. brasiliense (Freitas & Oliveira 1996; Oliveira 1997). Higher ant visitation to extrafloral nectaries can favor the production of flowers or fruits of this plant and reduce damage to C. brasiliense trees by pests. Sprouting of leaves and flower development before the rainy period is common in perennial plants of the Cerrado (Almeida et al. 1998; Felfini et al. 1999; Pedroni et al. 2002; Almeida et al. 2006; Leite et al. 2006a). This allows plants to increase photosynthetic area when the efficiency of herbivory by insects is lower. In addition, there are no heavy rains during this period, and the low quantity of leaves facilitates the ability of pollinators to find C. brasiliense flowers such as observed by Felfini et al. (1999) with Stryphnodendron adstringens (Mart.) Coville (Fabaceae).

Fig. 3.

Relationships between sunlight and numbers of Crematogaster sp.; rainfall and numbers of Crematogaster sp.; relative humidity of the air and numbers of Zelus armillatus, and sunlight and numbers of Mahanarva sp., on Caryocar brasiliense trees in Montes Claros, Minas Gerais State, Brazil. Samples = 100

In the spring C. brasiliense has new and fully expanded leaves (Leite et al. 2006a) and the weather is rainier; and in spring the populations of A. gossypii and its predator Chrysoperla sp., and Mahanarva sp. spittlebugs were greater. Some aphids species, such as A. gossypii, which is considered an initial pest, could induce undesirable changes in the host plant defense physiology during development (Santos et al. 2003; Men et al. 2004; Rhainds & Messing 2005; Leite et al. 2005a, 2006b, 2007). The increase in RH is the factor responsible for breaking embryonic dormancy of Mahanarva sp. (Gallo et al. 2002). Dikrella sp. and its predator Trybonia sp. were also recorded in this period of new leaves, but the highest Dikrella sp. population occurred 5 mo later, i.e., from Mar of the next year, but decreased again in late Aug and Sep with the new leaf fall. Holopothrips sp. scarify leaves (Cavalleri & Kaminski 2007), create galls (Cabrera & Segarra 2008), or are predators (Almeida et al. 2006), as are the spiders, bugs of the genus Zelus spp. and those of the subfamily Asopinae, Trybonia sp., and Chrysoperla sp. These predators are important in different ecosystems (Molina-Rugama et al. 1998; Landis et al. 2000; Almeida et al. 2006; Mizell 2007; Oberg et al. 2008; Venturino et al. 2008; Leite et al. 2002, 2003, 2005a,b, 2006b, 2007, 2011f).

The sucking insect species with higher potential to become pests in commercial C. brasiliense plantations are Aetalium reticulatum L. treehoppers (Aetalionidae), a pest of mango; E. rufomarginata on flowers and fruits; Dikrella sp. and A. gossypii cited as pest in seedling of this plant specie (Leite et al. 2006c). These insects were also affected by predators on this plant. Moreover our study reinforces the importance of sucking insects and the necessity of studying population dynamics of these organisms in arboreal systems of the Cerrado.