Distribution of galling insects and their parasitoids on Caryocar brasiliense tree crowns

Distribuição de insetos galhadores e seus parasitoides em copas de pequizeiros (Caryocar brasiliense)

Abstract

Caryocar brasiliense Camb. (Malpighiales: Caryocaraceae) is widely distributed in the Brazilian savanna and its fruits are used by humans for food, production of cosmetics, lubricants, and in the pharmaceutical industry. This plant is damaged by galling insects. Number of these galling insects and their parasitoids was recorded, in the field (galls) and in the laboratory (adults emerged from the galls), from three C. brasiliense crown heights, during three years. Numbers of adults of Eurytoma sp. (Hymenoptera: Eurytomidae), galling insect (younger attack) and Sycophila sp. (Hymenoptera: Eurytomidae) (a parasitoid of Eurytoma sp.), were greater on the apical parts of C. brasiliense tree crowns. Numbers and groups of Eurytoma sp. globoid galls (older attack) were higher in the median and basal crown parts. The numbers of Eurytoma sp. galls were higher on apical part of C. brasiliense tree crown and also of their parasitoids.

Keywords:
Cerrado; Eulophidae; Eurytoma sp.; Sycophila sp

Resumo

Caryocar brasiliense Camb. (Malpighiales: Caryocaraceae) é, amplamente, distribuída no cerrado brasileiro e seus frutos são utilizados para alimentação humana, produção de cosméticos, lubrificantes e na indústria farmacêutica, no entanto, é danificada por insetos galhadores. O número de insetos galhadores e seus parasitoides foram avaliados, em campo (galhas) e em laboratório (emergência de adultos das galhas), em três alturas do dossel de C. brasiliense, durante três anos. Os números de adultos Eurytoma sp. (Hymenoptera: Eurytomidae), inseto galhador (galhas novas) e de Sycophila sp. (Hymenoptera: Eurytomidae), parasitoide de Eurytoma sp., foram maiores na parte apical do dossel da copa de árvores de C. brasiliense. A quantidade de galhas globoides de Eurytoma sp., isoladas ou em grupo (galhas velhas), foi maior na parte mediana e basal da copa. Os números de adultos do galhador Eurytoma sp. e de seus parasitoides, que os seguem, foram maiores na parte apical da copa de árvores de C. brasiliense.

Palavras-chave:
Cerrado; Eulophidae; Eurytoma sp.; Sycophila sp

1. Introduction

Caryocar brasiliense Camb. (Malpighiales: Caryocaraceae) trees are important to traditional people as food and production of cosmetics, lubricants, and in the pharmaceutical industry (Santos et al., 2018). Isolated C. brasiliense trees (i.e. pasture or gardening) are subjected to higher incidence of galling insects than in forest formations (i.e. cerrado) (Leite et al., 2017). Caryocar brasiliense leaves have four main galling insects (Hymenoptera) with distinct shape and morphology: i) Eurytoma sp. (Hymenoptera: Eurytomidae) with globoid galls; ii) Bruchophagus sp. (Hymenoptera: Eurytomidae) with vein galls; iii) Eulophidae (Hymenoptera) with spherical galls; and iv) hymenopteran discoid galls (Leite, 2014). Eurytoma sp., the main C. brasiliense leaf galler, has the parasitoids Sycophila sp. (Hymenoptera: Eurytomidae) and Ablerus magistretti Blanchard, 1942 (Hymenoptera: Aphelinidae) and an inquiline (Alycaulini (Diptera). Quadrastichus sp. (Hymenoptera: Eulophidae), is a hyperparasitoid of Sycophila sp. (Leite, 2014). Information and photos of the galling insects, their distribution within leaf and branch, the community of gall parasitoids, hyperparasitoids, and predator insects may be consulted on Leite (2014).

The number of galling insects in the C. brasiliense tree crowns varies with branch position and wind direction (Leite, 2014). The numbers of Eurytoma sp. and hymenopteran galls on C. brasiliense leaves were highest on the eastern slope, and those of Bruchophagus sp. and Eulophidae galls on the northern slope (Leite, 2014). These leaves, on these slope orientations, received more wind and sunlight in the north of Minas Gerais State, with low relative humidity and high temperature (Leite, 2014). These harsher ecophysiological conditions favor galling insects (Price et al., 1998). The vertical distribution of galling insects in the crown of C. brasiliense needs further studies due to the increase in the commercial monocultures of C. brasiliense. Eurytoma sp., as an example, can heavily damage the leaves of C. brasiliense seedlings and trees, having potential to become a pest of this plant (Leite et al., 2006, 2007). Studies on the vertical distribution of herbivorous insects and their natural enemies are important for sampling plans and pest management on forest and agricultural systems (Lamien et al., 2008).

The hypothesis tested is that galling insects, and their parasitoids, would be more abundant on the apical part of C. brasiliense tree crowns (i.e. harsher ecophysiological conditions).

2. Material and Methods

The study was developed in the campus of the “Instituto de Ciências Agrárias” of the “Universidade Federal de Minas Gerais” (16°40’54,5”S, 43°50’26,8”W, 633m altitude) in the municipality of Montes Claros, Minas Gerais State, Brazil from Jun 2009 to Jun 2012. This region has dry winters and rainy summers with Aw climate: tropical savanna according to Köppen (Alvares et al., 2013). An area of 6,800 m² and 272 C. brasiliense trees with 10-years old (monoculture), spaced 5 × 5 m with gardens in the surrounding ~300 m was used. These trees were 3.85 ± 0.18 m high with 1.81 ± 0.15 m crown width (average ± standard error). The weeds between plant rows were cut by manual weeding.

A completely randomized design, with 15 replications (one tree/replication) and crown heights represented the treatments considered for the statistical analysis. Fifteen trees were selected and marked. Galling insects and their parasitoids (i.e., including rare ones) were collected during three consecutive years. Average number of individuals per crown part/tree were analyzed. The distribution of galling insects and their galls, leaves with galls, and parasitoids were recorded on four fully expanded leaves per C. brasiliense crown part [basal (0 to 33% of total plant height), medium (33 to 66% of total plant height) and apical (66 to 100% of total plant height)] on 15 C. brasiliense trees per month (36 months).

Evaluations in the three crown parts accounted for a total of 6,480 leaves (each leaf had three leaflets, all evaluated) during the 3 year or 12 leaves/tree/month. Caryocar brasiliense leaves were collected and transported to the laboratory. Gall size was measured with a digital caliper (accurate to the nearest 0.1mm). The leaves were scanned and the total leaf area and that per galling species calculated using SigmaScan Pro software (Sigma Scan Pro). Subsequently, these leaves were placed inside a white plastic pot (temperature of 25 °C), and the emergence of galling insects, parasitoids, hyperparasitoids, and inquilines were evaluated, per sample, every two days, during a 30-day period. The insects that emerged were collected and preserved in vials with 70% alcohol for identification by taxonomists. Alycaulini was identified by Dr. V.C. Maia and Eurytoma sp. and Quadrastichus sp. by Dr. M.A.P. Azevedo (Museu de História Natural, Universidade Federal do Rio de Janeiro, Rio de Janeiro State, Brazil); and A. magistretti, Bruchophagus sp., Eulophidae, Hymenoptera, and Sycophila sp. by Dr. O.H.H. Mielke (CDZOO, Universidade Federal do Paraná, Paraná state, Brazil) (voucher number: 1595/02).

The insect number means per crown tree part were used. The effect of crown height in the number of galling insects and parasitoids was evaluated with the statistical model: y_ij= m + a_i + b_j + e_ij, where y_ij is the observed value of the i-th plant part (i= 1, 2, ..., 3) of the j-th plant (j= 1, 2, ..., 15), m is the general average analyzed; a_i the effect of the i-th plant part (i= 1, 2, ..., 3); e_ij the effect of the experimental error associated with i-th part of the j-th plant. R software was used for statistical analysis. The aov function was used in the analysis of variance. The normality and homogeneity of the residual variances were identified by the tests Kruskal-Wallis and Bartlet, respectively. The means were compared using Tukey test (P≤ 0.05) with the aid of the glht function of the multcomp package.

3. Results

Number of Eurytoma sp. adults and length and width of their globoid galls were higher on the apical part of C. brasiliense tree crowns. However, Eurytoma sp. globoid gall groups were higher in the median and basal parts of the crown. The percentage of leaflets galled by all galling insects, leaflet area with Eurytoma sp. globoid galls and height and diameter of their globoid galls, numbers of Bruchophagus sp. vein galls, Eulophidae spherical galls, and Hymenopteran discoid galls did no differ between tree crown parts (Table 1).

Table 1
Percentage of leaflet galled by all galling insects (Leafgalls), numbers of total Eurytoma sp. globoid galls per leaflet (Leafgloboid), Eurytoma sp. globoid gall height (Ggheight), Eurytoma sp. globoid gall diameter (Gg. diam.), Eurytoma sp. groups of globoid gall area (Area (cm²) of ggg.), Eurytoma sp. groups of globoid gall length (Len. ggg.), Eurytoma sp. groups of globoid gall width (mm) (Wid. ggg), Eurytoma sp. globoid gall number (Gg. num.), Eurytoma sp. groups of globoid gall number (Num. ggg), Bruchophagus sp. vein galls (Num. vg), Eulophidae spherical galls (Num. sg), hymenopteran discoid galls (Num. dg), adults of Eurytoma sp., Sycophila sp. (parasitoid of Eurytoma sp.), Ablerus magistretti (parasitoid of Eurytoma sp.), Alycaulini (inquiline of Eurytoma sp. galls), and Quadrastichus sp. (hyperparasitoid of Sycophila sp.) per 12 leaflets/crown part of Caryocar brasiliense tree.

	Crown part			ANOVA
Galls and insects	Apical	Median	Basal	F	P
Leaf gallsn.s.	51.90 ± 1.49	48.70 ± 0.95	52.95 ± 1.18	3.23	0.05
Leaf. globoidn.s.	57.07 ± 7.48	46.73 ± 5.20	44.94 ± 3.77	2.43	0.10
Gg. height (mm)n.s.	2.22 ± 0.07	2.23 ± 0.04	2.36 ± 0.05	2.04	0.14
Gg.diam. (mm2)n.s.	1.83 ± 0.11	1.67 ± 0.04	1.79 ± 0.03	1.83	0.17
Area (cm2) of ggg*	3.35 ± 0.39a	2.06 ± 0.20b	2.11 ± 0.19b	12.75	0.00
Len. ggg (mm)*	33.47 ± 2.21a	26.96 ± 1.60b	27.08 ± 1.52b	7.58	0.00
Wid. ggg (mm)*	9.54 ± 0.55a	7.43 ± 0.32b	7.62 ± 0.32b	13.01	0.00
Gg. num.*	333.96 ± 23.06b	431.10 ± 17.84a	415.80 ± 8.88a	14.29	0.00
Num. ggg*	218.91 ± 8.75b	292.80 ± 12.02a	274.58 ± 10.41a	13.97	0.00
Num. vgn.s.	0.30 ± 0.08	0.60 ± 0.26	0.50 ± 0.15	0.69	0.51
Num. sgn.s.	0.13 ± 0.05	0.07 ± 0.03	0.03 ± 0.02	3.30	0.05
Num. dgn.s.	0.93 ± 0.17	0.61 ± 0.09	0.63 ± 0.13	1.79	0.18
Eurytoma sp.*	445.04 ± 15.25a	266.51 ± 9.50c	330.09 ± 12.96b	50.05	0.00
Sycophila sp.*	59.54 ± 2.91a	40.17 ± 2.78b	39.25 ± 1.51b	21.25	0.00
Ablerus magistretti n.s.	0.79 ± 0.12	0.85 ± 0.28	0.93 ± 0.23	0.11	0.89
Alycaulini*	0.27 ± 0.09a	0.00 ± 0.00b	0.00 ± 0.00b	7.52	0.00
Quadrastichus sp.n.s.	2.55 ± 0.38	3.24 ± 0.34	2.29 ± 0.36	1.84	0.17

• Means ± standard error followed by the same letter per row do not differ by the Tukey test (*= P< 0.01 and **= P< 0.05). Values of F and P were obtained by ANOVA. ^n.s. = non-significant by ANOVA. df’s of treatments, blocks, and errors were 2, 14, and 28, respectively.

Number of Sycophila sp. adults (parasitoid of Eurytoma sp.) and Alycaulini adults (inquiline of Eurytoma galls) was higher on the apical tree parts. Number of A. magistretti adults, parasitoid of Eurytoma sp., and Quadrastichus sp. adults, hyperparasitoid of Sycophila sp., was similar (P> 0.05) between tree crown parts (Table 1).

4. Discussion

The higher number of adults of Eurytoma sp. globoid galls in the apical part (n = 6676) of the C. brasiliense trees, in the semiarid northern Minas Gerais State, agrees with the preference of galling insects by the upper crown, as observed for tropical rainforest trees (Ribeiro and Basset, 2007), probably because this crown part receives more solar radiation than the basal one (total emerged = 4952) (Ribeiro and Basset, 2007). That is, the apical part shadows the basal part of the C. brasiliense trees and, therefore, the leaves at this last part receive lower solar radiation. This would explain the thermal comfort provided by large trees used in parks, gardens, and sidewalks in cities (Richards and Edwards, 2017). Higher sclerophylly with a suitable ecosystem for gall-forming insects on taller tree crown in wet tropical rainforests was attribute to nutrient stress in meristems of this part (Ribeiro and Basset, 2007). The Amazonian forest upper canopy has similar conditions as those of the Mediterranean vegetation habitats: hygrothermically stressed environments and the leaves with high levels of leaf sclerophylly and temperature at lethal limits (Juliao et al., 2014). Higher galling insect's survival in more sclerophilous leaves (i.e. tree tops) was found in the Panama wet rainforest (Neotropical) and Australia subtropical forest (Australian) (Ribeiro et al., 2014). The harsher environment favors oviposition, survivorship, distribution, diversity, and abundance of galling insects in sclerophyllous vegetation (Fernandes and Price, 1988, 1992; Ribeiro and Basset, 2007).

The higher number of Sycophila sp. adults, most important Eurytoma sp. parasitoid (Leite et al., 2013), in the apical part (total emerged = 894) than in the basal part (total emerged = 589) of the C. brasiliense tree crown, associated with galls of this insect, agrees with the natural enemy’s pattern – parasitoids follow their hosts (Leite et al., 2017). For this reason, natural enemies in high populations may reduce the numbers of galling insects (Leite et al., 2013). The indole butyric acid (phytohormone) and numbers of Eurytoma sp. adults, and of their galls, and Sycophila sp. on C. brasiliense trees were ppositively correlated (Leite et al., 2007).

The numbers of Eurytoma sp. galling insect and of its parasitoid Sycophila sp. and inquiline Alycaulini were higher on the apical C. brasiliense crowns. with the latter following the first one.

Acknowledgements

This research was supported by the “Programa Cooperativo sobre Proteção Florestal (PROTEF) do Instituto de Pesquisas e Estudos Florestais (IPEF)”.

References

• ALVARES, C.A., STAPE, J.L., SENTELHAS, P.C., GONÇALVES, J.L.M. and SPAROVEK, G., 2013. Köppen’s climate classification map for Brazil. Meteorologische Zeitschrift, vol. 22, no. 6, pp. 711-728. http://dx.doi.org/10.1127/0941-2948/2013/0507
  » http://dx.doi.org/10.1127/0941-2948/2013/0507
• FERNANDES, G.W. and PRICE, P.W., 1988. Biogeographical gradients in galling species richness: tests of hypotheses. Oecologia, vol. 76, no. 2, pp. 161-167. http://dx.doi.org/10.1007/BF00379948 PMid:28312192.
  » http://dx.doi.org/10.1007/BF00379948
• FERNANDES, G.W. and PRICE, P.W., 1992. The adaptive significance of insect gall distribution: survivorship of species in xeric and mesic habitats. Oecologia, vol. 90, no. 1, pp. 14-20. http://dx.doi.org/10.1007/BF00317803 PMid:28312265.
  » http://dx.doi.org/10.1007/BF00317803
• JULIÃO, G.R., VENTICINQUE, E.M., FERNANDES, G.W. and PRICE, P.W., 2014. Unexpected high diversity of galling insects in the amazonian upper canopy: the savanna out there. PLoS One, vol. 9, no. 12, pp. e114986. http://dx.doi.org/10.1371/journal.pone.0114986 PMid:25551769.
  » http://dx.doi.org/10.1371/journal.pone.0114986
• LAMIEN, N., TIGABU, M., DABIRE, R., GUINKO, S. and ODEN, P.C., 2008. Insect (Salebria sp.) infestation and impact on Vitellaria paradoxa CF Gaertn. fruit production in agroforestry parklands. Agroforestry Systems, vol. 72, no. 1, pp. 15-22. http://dx.doi.org/10.1007/s10457-007-9094-1
  » http://dx.doi.org/10.1007/s10457-007-9094-1
• LEITE, G.L.D., 2014. Galling insects on Caryocar brasiliense Camb. (Caryocaraceae). In: G.W. FERNANDES and J.C. SANTOS, eds. Neotropical insect galls Berlin: Springer-Verlag, pp. 179-192. https://http://dx.doi.org/10.1007/978-94-017-8783-3_12
  » http://dx.doi.org/10.1007/978-94-017-8783-3_12
• LEITE, G.L.D., VELOSO, R.V.S., CASTRO, A.C.R., LOPES, P.S.N. and FERNANDES, G.W., 2007. Effect of AIB on quality and phytosanity of Caryocar brasiliense Camb. (Caryocaraceae) air layering. Revista Árvore, vol. 31, no. 2, pp. 315-320. http://dx.doi.org/10.1590/S0100-67622007000200014
  » http://dx.doi.org/10.1590/S0100-67622007000200014
• LEITE, G.L.D., VELOSO, R.V.S., REDOAN, A.C.M., LOPES, P.S.N. and MACHADO, M.M.L., 2006. Arthropods associated to “piquizeiro” tree seedlings. Arquivos do Instituto Biológico, vol. 73, pp. 365-370.
• LEITE, G.L.D., VELOSO, R.V.S., ZANUNCIO, J.C., AZEVEDO, A.M., SILVA, J.L., WILCKEN, C.F. and SOARES, M.A., 2017. Architectural diversity and galling insects on Caryocar brasiliense trees. Scientific Reports, vol. 7, no. 1, pp. 16677. http://dx.doi.org/10.1038/s41598-017-16954-6 PMid:29192234.
  » http://dx.doi.org/10.1038/s41598-017-16954-6
• LEITE, G.L.D., VELOSO, R.V.S., ZANUNCIO, J.C., FERNANDES, G.W., ALMEIDA, C.I.M., PEREIRA, J.M.M., SERRÃO, J.E. and SOARES, M.A., 2013. Seasonal abundance of galling insects (Hymenoptera) on Caryocar brasiliense (Malpighiales: Caryocaraceae) trees in the cerrado. The Florida Entomologist, vol. 96, no. 3, pp. 797-809. http://dx.doi.org/10.1653/024.096.0313
  » http://dx.doi.org/10.1653/024.096.0313
• PRICE, P.W., FERNANDES, G.W., LARA, A.C.F., BRAWN, J., BARRIOS, H., WRIGHT, M.G., RIBEIRO, S.P. and ROTHCLIFF, N., 1998. Global patterns in local number of insect galling species. Journal of Biogeography, vol. 25, no. 3, pp. 581-591. http://dx.doi.org/10.1046/j.1365-2699.1998.2530581.x
  » http://dx.doi.org/10.1046/j.1365-2699.1998.2530581.x
• RIBEIRO, S.P. and BASSET, Y., 2007. Gall-forming and free-feeding herbivory along vertical gradients in a lowland tropical rainforest: the importance of leaf sclerophylly. Ecography, vol. 30, no. 5, pp. 663-672. http://dx.doi.org/10.1111/j.2007.0906-7590.05083.x
  » http://dx.doi.org/10.1111/j.2007.0906-7590.05083.x
• RIBEIRO, S.P., BASSET, Y. and KITCHING, R., 2014. Density of insect galls in forest understorey and canopy: neotropical, gondwana or global patterns? In: G.W. FERNANDES and J.C. SANTOS, eds. Neotropical insect galls Berlin: Springer-Verlag, pp. 129-141. https://http://dx.doi.org/10.1007/978-94-017-8783-3_8
  » http://dx.doi.org/10.1007/978-94-017-8783-3_8
• RICHARDS, D.R. and EDWARDS, P.J., 2017. Quantifying street tree regulating ecosystem services using Google Street View. Ecological Indicators, vol. 77, pp. 31-40. http://dx.doi.org/10.1016/j.ecolind.2017.01.028
  » http://dx.doi.org/10.1016/j.ecolind.2017.01.028
• SANTOS, P.H.R., GIORDANI, S.C.O., SOARES, B.C., SILVA, F.H.L., ESTEVES, E.A. and FERNANDES, J.S.C., 2018. Genetic divergence in populations of Caryocar brasiliense Camb. from the physical characteristics of the fruits. Revista Árvore, vol. 42, pp. e420116. http://dx.doi.org/10.1590/1806-90882018000100016
  » http://dx.doi.org/10.1590/1806-90882018000100016

Publication Dates

• Publication in this collection
  28 May 2021
• Date of issue
  2022

History

• Received
  20 Mar 2020
• Accepted
  28 Aug 2020