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Introduction
The galling insects are among the most sophisticated in this group because they modify the host plant tissues to produce highly specialized structures where their larvae develop protected from harsh external environment, endophytically, while feeding on a rich material (Silva et al. 2016). These abnormal plant cell growths are called galls and vary in color, aspect, size, phenology, hardness, chemistry, and anatomical structure, besides being rare, univoltine or multivoltine (e.g. Fernandes and Santos 2014).
Galling insects are extremely abundant in all major ecosystems in the world, with many of them damaging plant species of economic importance. Theses insects are totally dependent on the nutrients obtained from the host plant tissues. Thus, they need to manipulate their host plant physiology to adjust their feeding (Espírito-Santo et al. 2012).
Large-scale distribution of galling insects has been studied and some mechanisms may explain their trends. Changes in habitat conditions affect the interactions between gallers and their host plants, transforming their diversity and abundance. These insects are diverse in more complex environments (i.e. higher floristic diversity) (Price 2005), but the factors affecting galling community and population trends, such as host traits mediated by habitat interactions, require further studies (Price 2005).
The system composed by a common and economically important Cerrado (savanna biome) tree species, Caryocar brasiliense Camb. (Malpighiales: Caryocaraceae) (Leite et al. 2006), and its four main galling herbivores in central Brazil is adequate to evaluated their interactions. Four different hymenopterans species, very distinct in shape, morphology and abundance induce galls on C. brasiliense (Leite et al. 2009, 2011a, 2011b, 2011c).
Caryocar brasiliense trees, which are protected by Brazilian federal laws, are the main income source of many communities (Leite et al. 2006; Santos et al. 2018). Hence, these trees are left in the Cerrado areas even after being converted to pasture, urban or agricultural areas, with a common scenario of isolated plants in the agro-urban landscape. The effects of habitats on the diversity and abundance of galling insects and of their natural enemies on C. brasiliense trees were evaluated in three environments: i) preserved Cerrado; ii) Cerrado cleared for pasture; and iii) Cerrado converted into an urban development area. The hypothesis tested was that the diversified of galling insects is higher in more diverse habitats. Therefore, the diversity of galling insects was expected to be higher on trees in the Cerrado compared to the other two habitat types.
Materials and methods
Study sites
This study was performed in the municipality of Montes Claros, Minas Gerais state, Brazil, during 3 consecutive years (June 2008 through June 2011). This region has dry winters and rainy summers with a Aw: tropical savanna climate, according to Köppen. The study was developed in three distinct environments: 1) sensu stricto Cerrado, (16º44’55.6ˮS 43º55’7.3ˮW, at an elevation of 943 masl, with dystrophic yellow red oxisol soil with sandy texture); 2) pasture, formerly with Cerrado vegetation (16º46’16.1ˮS 43º57’31.4ˮW, at an elevation of 940 masl, with dystrophic yellow red oxisol soil with loamy texture); and 3) an urban area in the campus of the “Instituto de Ciências Agrárias da Universidade Federal de Minas Gerais (ICA/UFMG)”, (16º40’54.5ˮS 43º50’26.8ˮW, at an elevation of 633 masl, with dystrophic red oxisol with medium texture which was described by Leite et al. (2006). Permission to collect insects and galls in these locations/activities was granted by the landowner (Universidade Federal de Minas Gerais) and the collected arthropods are neither endangered nor protected species.
The Cerrado area was of the sensu stricto type (a species-rich biome of shrubs and trees 8-10 m high, with a dense understory) in an area with 44.9 % of soil covered by grass, 5.8 % by shrubs, 23.5 % by small trees and 8.8 % by large ones and an average of 17 C. brasiliense trees per ha. The pasture area has 84.2 % of the soil covered by African grass (Brachiaria decumbens (Stapf)), 0.2 % by shrubs, 4.8 % by small trees, 2.8 % by large ones and with 42.3 C. brasiliense trees per ha. The urban area has 100 % of the soil covered by grass (Paspalum notatum Flüggé) with 100 C. brasiliense trees per ha (see Leite et al. 2006). The native Cerrado vegetation is the most diverse habitat, followed by the pasture and the urban habitat, respectively. The high number of C. brasiliense trees per ha in the urban area is explained by it’s use as a designed landscape and as shade source. The Cerrado and pasture were 10 km apart and 20-30 km apart, respectively, from the urban area.
Study host plants and galling species
Adult C. brasiliense trees (reproductive stage) in the Cerrado, pasture and urban environment were 4.1 ± 0.2 m, 2.9 ± 0.1 m and 3.8 ± 0.2 m high (average ± SE) with crown width of 5.2 ± 0.2 m, 4.0 ± 0.1 m and 1.7 ± 0.1 m (average ± SE) (Leite et al. 2006).
The hymenopteran galls studied on C. brasiliense leaves were: i) Eurytoma sp. globoid galls, with 2.53, 1.28, and 0.90 mm of height, length and width, respectively, with walls covered by yellowish trichomes with one larval chamber and one galling larva each; ii) Bruchophagus sp. vein galls, with 1.91, 2.04, and 5.56 mm of height, length and width, respectively, greenish and glabrous; iii) Eulophidae spherical galls, with 1.61 and 1.84 mm of diameter and height, respectively, brownish and glabrous; and iv) Hymenopteran discoid galls, with 3.70 and 0.57 mm of diameter and height, respectively, greenish and glabrous. For detailed information on the natural history of the galling insects and their distribution within trees, as well as descriptions of the natural enemies in this system, see Leite (2014). There, the following summary of these species is shown. I) Predators: The spiders Cheiracanthium inclusum Hentz, 1847 (Miturgidae); Peucetia rubrolineata (Keyserling, 1877) (Oxyopidae); Anelosimus sp., Achaearanea hirta (Taczanowski, 1873) (Theridiidae); Gastromicans albopilosa Simon, 1903; Chira bicirculigera Soares and Camargo, 1948; Rudra humilis Mello-Leitão, 1945; Thiodina melanogaster Mello-Leitão, 1917 and Lyssomanes pauper (Mello-Leitão, 1945) (Salticidae); Dictyna sp. and sp.1 (Dictynidae); Tmarus sp. and sp.1 (Thomisidae); Argiope argentata (Fabricius, 1775); Gasteracantha cancriformes (L., 1758); Argiope sp.; Parawixia sp. and sp.1 (Araneidae); and Anyphaenidae are important generalist predators (Leite et al. 2013). The ants Crematogaster sp., Pseudomyrmex termitarius Smith, 1855, and Camponotus novograndensis Mayr, 1870 (Hymenoptera: Formicidae) and the predatory thrips Holopothrips sp., Trybonia intermedius Bagnall, 1910 and Trybonia mendesi Moulton, 1933 (Thysanoptera: Phlaeothripidae) can reduce defoliation by lepidopteran leaf miners and/or sucking insects (Leite et al. 2012a, 2012b, 2012c), and this factor may favor the colonization of the leaves on C. brasiliense by galling insects (free space). Zelus armillatus (Lepeletier & Serville, 1825) (Hemiptera: Reduviidae) is an important predator of Eurytoma Illiger, 1807 galls as well as defoliators and leaf-mining insects (Leite et al. 2012a, 2012c, 2013). Epipolops sp. (Hemiptera: Geocoridae) can also prey on defoliators and leaf-mining insects (Leite et al. 2012a). II) Parasitoids: Sycophila sp. (Hymenoptera: Eurytomidae) is the major parasitoid of Eurytoma sp. (Leite et al. 2013), but Ablerus magistretti Blanchard, 1942 (Hymenoptera: Aphelinidae) is also a parasitoid of this galling insect and apparently competition occur between these two species for their galling host (Leite et al. 2013). III) Hyperparasitoids: Quadrastichus sp. (Hymenoptera: Eulophidae) is a possible hyperparasitoid of Sycophila sp. (Leite et al. 2013). IV) Inquiline: Eurytoma occupy the galls belonging to the Alycauline (Diptera) (Leite et al. 2013).
Study design
The study design was completely randomized, with 12 replicates (12 trees) and 3 treatments (habitats). Data were collected on C. brasiliense adult trees at every 50 m along a 600 m transect at each site (Cerrado, pasture and urban area). For the 12 replicates, we collected data during 3 consecutive years, collecting samples of all insects’ species (i.e., rare species) per year and area. No fertilizers or pesticides were used in these three areas.
The distribution of galling insects and their galls, predators, parasitoids and inquilines, and the percentage of leaves infested with galls, was recorded on 4 fully expanded leaves (three leaflets/leaf) of each 12 C. brasiliense trees per area. Sampling was performed in the morning (7:00-11:00 a.m.) by direct visual observation once a month. Insects were collected with tweezers, brushes, or aspirators and preserved in vials with 70 % alcohol for identification by taxonomists. The leaves were collected and transported to the laboratory. Gall size was measured by using a digital caliper (accurate to the nearest 0.1 mm). Leaves were scanned and the leaf area and that occupied by each galling species calculated using the Sigma Scan Pro software (SPSS 1999). Subsequently, the leaves were placed inside a white plastic pot (temperature 25 °C) and the emergence of galling insects, parasitoids, hyperparasitoids and inquilines were evaluated per sample every two days during 30 days. The emerged insects were collected and preserved as described for identification. The voucher number for spiders and insects are IBSP 36921-36924 (Instituto Butantan, São Paulo state, Brazil) and 1595/02 - 1597/02 (CDZOO, Universidade Federal do Paraná, Paraná state, Brazil), respectively.
Statistical analyses
Averages were used to reduce the data per leaflet/tree in each area. Correlations between the number of galling insects and their galls with floristic diversity (number of trees/ha) (see Leite et al. 2006) were subjected to variance (ANOVA) (P < 0.05) and simple regression analysis (P < 0.05). The richness and species diversity of galling insects and their parasitoids and predators were calculated per tree and habitat. The diversity was calculated using Hill´s formula (Hill 1973), and the species richness with Simpson indices (Lazo et al. 2007). The effect of the habitat on the numbers of galling insects and their galls, natural enemies and inquilines (transformed to √x + 0.5 or arcsine for percentage data) was determined with ANOVA (P < 0.05), with subsequent mean separation by Tukey’s test (P < 0.05).
Results
The richness of galling insects per leaflet was greater on the C. brasiliense trees in the Cerrado and pasture habitats than on the urban habitat and diversity of galling insects higher in the Cerrado habitat (Table 1). The highest richness and diversity for both parasitoids and predators of the galling insects were higher on C. brasiliense trees in the pasture and urban areas (Table 1). The numbers of trees/ha (floristic diversity) was negatively correlated with the percentages of leaflets, the total number of all kinds of galls/leaflets, of leaflet area with total number of all kinds of galls/leaflets, area of globoid galls, and length and width of the conglomerate of globoid galls and positively with the area of discoid galls (Fig. 1).
Table 1 Ecological indexes of galling insects and their natural enemies per leaflet on Caryocar brasiliense, Montes Claros, Brazil, during autumn 2008 to autumn 2011.
| Indexes | Cerrado | Pasture | Urban | F | P |
|---|---|---|---|---|---|
| Richness of galls* | 2.75 ± 0.25 a | 2.33 ± 0.22 a | 1.00 ± 0.00 b | 27.77 | 0.00000 |
| Diversity of galls* | 4.10 ± 0.57 a | 2.30 ± 0.18 b | 1.44 ± 0.00 b | 16.83 | 0.00004 |
| Richness of parasitoids* | 0.25 ± 0.13 b | 1.33 ± 0.18 a | 1.58 ± 0.22 a | 20.06 | 0.00001 |
| Diversity of parasitoids* | 0.36 ± 0.18 b | 1.77 ± 0.24 a | 1.75 ± 0.25 a | 1.97 | 0.00006 |
| Richness of predators* | 1.92 ± 0.37 b | 4.58 ± 0.48 a | 3.08 ± 0.25 a | 19.30 | 0.00001 |
| Diversity of predators* | 3.20 ± 0.73 b | 8.15 ± 1.35 a | 5.52 ± 0.74 ab | 8.64 | 0.00171 |
Means followed by the same letter (± standard error) per line do not differ by the test of Tukey (* = P < 0.01).
Figure 1 Relationships between number of trees/ha with percentages of leaflets and with total number of all kinds of galls and leaflet area with total number of all kinds of gall/leaflet, areas (mm2) of globoid and discoid galls, lengths and widths (mm) of conglomerate globoid galls on Caryocar brasiliense trees in Montes Claros, Minas Gerais State, Brazil.
The total numbers of adults emerged per area, in laboratory, were: a) Cerrado: Eurytoma sp. (globoid galls)= 12, Bruchophagus sp. (vein galls)= 1, Eulophidae (spherical galls)= 1, and Hymenopteran (discoid galls)= 22, respectively; b) pasture: Eurytoma sp. (globoid galls)= 499, Eulophidae (spherical galls)= 1, and Hymenopteran (discoid galls)= 2; and urban area: only Eurytoma sp. (globoid galls)= 3,328. The numbers of Eurytoma sp. adults emerged from galls induced on C. brasiliense in the urban habitat was five times higher than in the other two habitats. The numbers of Bruchophagus sp. galls, Eulophid and hymenopteran gallers were highest on C. brasiliense leaflets in the Cerrado habitat. The C. brasiliense trees in the urban environment were exclusively galled by Eurytoma (Tables 2-3).
Table 2 Average number of adult galling insects, their natural enemies, and inquilines per leaflet on Caryocar brasiliense at Montes Claros, Minas Gerais, Brazil (2008 to 2011).
| Kinds of insects | Cerrado | Pasture | Urban | F | P |
|---|---|---|---|---|---|
| Galling insects | |||||
| Eurytoma sp.* | 0.01 ± 0.01 b | 0.19 ± 0.09 ab | 1.03 ± 0.48 a | 5.95 | 0.009 |
| Bruchophagus | 0.001 ± 0.001 | 0.0 ± 0.0 | 0.0 ± 0.0 | 1.00 | 0.390 |
| Eulophidae | 0.0006 ± 0.0005 | 0.0003 ± 0.0002 | 0.0 ± 0.0 | 1.00 | 0.390 |
| Hymenoptera | 0.017 ± 0.016 | 0.001 ± 0.001 | 0.0 ± 0.0 | 0.97 | 0.388 |
| NE/inquilines | |||||
| Ablerus magistretti | 0.0 ± 0.0 | 0.0 ± 0.0 | 0.001 ± 0.001 | 2.57 | 0.099 |
| Alycaulini | 0.0 ± 0.0 | 0.0 ± 0.0 | 0.001 ± 0.001 | 1.00 | 0.390 |
| Epipolops sp.** | 0.001 ± 0.001 b | 0.02 ± 0.01 a | 0.0 ± 0.0 b | 15.39 | 0.000 |
| Holopothrips sp. | 0.003 ± 0.001 | 0.01 ± 0.01 | 0.01 ± 0.01 | 2.84 | 0.080 |
| Quadrastichus sp. | 0.001 ± 0.001 | 0.004 ± 0.002 | 0.002 ± 0.001 | 1.52 | 0.241 |
| Spiders | 0.01 ± 0.01 | 0.01 ± 0.01 | 0.02 ± 0.01 | 1.90 | 0.174 |
| Sycophila sp.** | 0.001 ± 0.001 b | 0.04 ± 0.01 ab | 0.09 ± 0.03 a | 3.58 | 0.045 |
| Total ants* | 0.06 ± 0.01 ab | 0.10 ± 0.02 a | 0.02 ± 0.01 b | 9.70 | 0.001 |
| Trybonia spp.** | 0.003 ± 0.001 b | 0.09 ± 0.04 a | 0.0 ± 0.0 b | 4.36 | 0.025 |
| Zelus armillatus** | 0.002 ± 0.001 b | 0.01 ± 0.01 ab | 0.08 ± 0.03 a | 4.74 | 0.019 |
Means followed by the same letter (± standard error) in each row are not different by the test of Tukey (* = P < 0.01 and ** = P < 0.05).
Table 3 Galling insects and their damage per leaflet on Caryocar brasiliense, Montes Claros, Brazil, during autumn 2008 to autumn 2011.
| Indexes | Cerrado | Pasture | Urban | F | P |
|---|---|---|---|---|---|
| Leaflet galled (%) | 14.74 ± 2.56 b | 45.11 ± 2.33 a | 52.98 ± 4.48 a | 39.22 | 0.000 |
| Leaflet area taken by all galls (%) | 0.48 ± 0.21 b | 3.63 ± 0.50 b | 17.01 ± 3.98 a | 14.16 | 0.000 |
| Leaf area occupied by Eurytoma globoid galls (mm2) | 0.92 ± 0.30 b | 2.23 ± 0.21 ab | 3.68 ± 0.74 a | 8.40 | 0.002 |
| Leaf area occupied by Bruchophagus vein galls (mm2) | 4.08 ± 1.23 a | 0.72 ± 0.50 b | --- | 9.82 | 0.010 |
| Leaf area occupied by Eulophid spherical galls (mm2) | 0.12 ± 0.06 | 0.48 ± 0.23 | --- | 2.49 | 0.143 |
| Leaf area occupied by hymenopteran discoid galls (mm2) | 2.40 ± 0.63 | 1.75 ± 0.32 | --- | 1.42 | 0.256 |
| Length (mm) of conglomerate of globoid galls* | 12.63 ± 1.49 b | 28.73 ± 3.12 a | 25.31 ± 1.15 a | 17.11 | 0.000 |
| Width (mm) of conglomerate of globoid galls** | 4.24 ± 0.58 b | 8.15 ± 0.81 a | 7.05 ± 0.38 a | 10.09 | 0.001 |
Means followed by the same letter (± standard error) per line do not differ by the test of Tukey (* = P < 0.01 and ** = P < 0.05).
The percentages of leaflets, the total number of galls/leaflet (4 galling species) and the length and width of the conglomerate globoid galls (Eurytoma sp.) were greater on C. brasiliense leaflets in the pasture and urban habitats than in the Cerrado. The numbers and size of globoid galls (Eurytoma sp.), the percentages of leaflet area and the total number of galls/leaflets were greater in the urban habitat. The numbers of vein galls (Bruchophagus sp.) of the largest size and discoid galls (Hymenopteran galls) were highest on C. brasiliense leaflets in the Cerrado. The size of discoid galls (Hymenopteran) and the number of spherical galls (Eulophidae) were similar (P > 0.05) in the pasture and Cerrado habitats; however, the vein galls (Bruchophagus sp.) on C. brasiliense leaflets were larger in the Cerrado habitat (Table 3).
The numbers of the parasitoid Sycophila sp. (Hymenoptera: Eurytomidae) and of the predator, Zelus armillatus (Hemiptera: Reduviidae) were 2.5 and 8 times higher on C. brasiliense leaflets in the urban habitat compared to the other ones (Table 2). The numbers of the hyperparasitoids of Sycophila sp., Ablerus magistretti Blanchard, 1942 (Hymenoptera: Aphelinidae), and Quadrastichus sp. (Hymenoptera: Eulophidae), and adults of the Eurytoma gall inquiline (Alycauline: Diptera) were similar between habitats (P > 0.05; Table 2).
The numbers of the predators Epipolops sp. (Hemiptera: Geocoridae), Trybonia spp. (T. intermedius Bagnall 1910 and T. mendesi Moulton 1933: Thysanoptera: Phlaeothripidae), the ants (Hymenoptera: Formicidae) and the sap-sucking hemipterans were larger on C. brasiliense trees in the pasture habitat and those of the predators Holopothrips sp. (Thysanoptera: Phlaeothripidae) and spiders similar between habitats (Table 2).
Discussion
Caryocar brasiliense trees can reach over 10 m in height and 6 m in canopy width in the Cerrado (Leite et al. 2006). Its fruits have an internal mesocarp rich in oil, vitamins and proteins, and contain many compounds of medicinal importance. Moreover, it is used by humans for food, production of cosmetics, lubricants and in the pharmaceutical industry (Bezerra et al. 2015).
The diversity of leaf-galling species (all kinds of galls) on C. brasiliense trees increased with the floristic diversity, as higher numbers of trees, shrubs and herbs were found in the Cerrado and pasture habitats than on the university campus (the urban area). The galling species are not linearly distributed among the habitats with trends in their distribution and impacts between them (Leite et al. 2006). The density of Eurytoma sp. (globoid gall), the most abundant species, and consequently, the richness and diversity of its natural enemies (i.e. Sycophila sp. and Z. armillatus) was highest in an environment with the lowest floristic diversity (i.e., the urban area).
The emergence and percentage of survival of Eurytoma sp. were higher in the urban area and lowest in the Cerrado area. This galling insect colonized up to 70 % of the leaf area of C. brasiliense trees in an urban area (Leite et al. 2009). On the other hand, a positive correlation between floristic diversity and the area of discoid galls was observed, and these galls showed the highest emergence of adults per this gall type in the Cerrado area. Discoid galls species were not observed in the urban area. This shows that changing the environment promotes a complete change in the structure of galling insect communities, with a single species completely dominating the available resources. The increase in the environmental simplification positively influenced the most common species, Eurytoma sp., corroborating to report that plant species richness is one of the most important factors explaining the variation in galling richness on the regional scale (Araújo et al. 2013). The combination of plant richness and plant abundance, on the regional level, is the best model to explaining galling insect richness (Araújo et al. 2014).
The higher richness and diversity of natural enemies of the galling insects in C. brasiliense trees in the pasture and urban areas, including that of Eurytoma sp., confirms the natural enemies’ patterns - their populations depend on their prey/hosts and follow those of the herbivorous insects (Oberg et al. 2008; Venturino et al. 2008). These natural enemies, such as spiders, predatory bugs and Sycophila sp., are important in C. brasiliense and other ecosystems (Oberg et al. 2008; Venturino et al. 2008; Leite et al. 2012a, 2012b, 2012c, 2013).
Conclusions
Greater environmental diversity (i.e. floristic diversity) favored the diversity of galling insect species and of their natural enemies, but decreased that of Eurytoma sp. and their natural enemies numbers, with the habitat impact having different effects in the structure of galling insect communities. Eurytoma sp. is the galling insect species with greatest potential to become a pest in commercial C. brasiliense plantations, based on the abundant and premature abscission caused to C. brasiliense leaves.
