Printer Friendly

Influencia de la distancia de fragmentos forestales adyacentes en el parasitoidismo de afidos (Hemiptera: Aphididae) de trigo en Parana, Brasil.

Influence of distance from adjacent forest fragments on aphids (Hemiptera: Aphididae) parasitoidism in wheat fields in Parana State, Brazil


Biological control services in agricultural landscapes are enhanced by natural and semi-natural habitats adjacent to arable fields (Holland et al. 2008; Thomsom and Hoffman 2013). Shelter, floral resources and alternative preys and hosts for natural enemies are provided by these non-crop habitats (Tscharntke et al. 2005), but several studies showed that crop pests can be benefited by these habitats (Bianchi et al. 2006). Investigations on effects of non-crop habitats on the occurrence of crop pests and their natural enemies have mostly been performed in the northern hemisphere (Bianchi et al. 2006; Thies et al. 2008; Caballero-Lopez et al. 2012), while there is scarce information for Neotropical region. In this context, the aim of this study is to investigate the effects of tropical forest fragments on aphid abundance and parasitoidism rates in adjacent wheat fields in agricultural landscapes of Parana State, southern Brazil. On the basis of the studies highlighted above we hypothesized that aphid parasitoids benefit from forest fragments and will be higher abundance near the forest fragment than in center of the crops.

Material and methods

It was carried out a study during wheat cropping season 2009 (from April to September) at four commercial wheat fields, all located in northern Parana State, Brazil. The sites were located in the municipalities of Ibipora-San Antonio Farm (SAF, 23[degrees]14'34"S, 51[degrees]27'07"W), Ibipora-Bonsucesso Farm (BF, 23[degrees]12'26"S, 51[degrees]03'51"W), Rolandia-Gioconda Farm (GF, 23[degrees]23'59"S, 5[degrees]19'01"W), and Londrina (23[degrees]19'49"S, 51[degrees]08'12"W). The study region is characterized by a humid subtropical climate with rainfall concentrated in the summer months and an average annual temperature and precipitation of 21 [degrees]C and 1600 mm, respectively (IAPAR 2015). The size of wheat fields varied from 2.3 to 20.9 ha and adjacent forest (Atlantic) fragments varied from 24.5 to 380 ha. In general, the landscape complex around each farm (considering 2 Km radius) was compound majority by wheat crops (39.2 to 47.4%), follow by non-crop area (forest fragment and pasture) (26.2 to 39%), maize (7 to 26.5%) and coffee crops (2.9 to 20.5%).

Population dynamics of the cereal aphids were monitored weekly from wheat emergence to physiological maturity of winter wheat (from April to September, 2009). All aphids were identified to the species level, by means of a visual inspection (Salvadori and Tonet 2001). The number of healthy and parasitized aphids (mummies) in the edge (25 m) and centre (525 m) of the wheat fields were concomitantly estimated. In each field, aphid counts were conducted in two 100m linear transects fixed at two distances apart from the adjacent forest fragments. The linear transects were composed with 10 assessment points with a spacing of 10m between points. Each assessment point comprised 20 wheat shoots/tillers summing to 400 shoots/tillers per field. All parasitized aphids were collected and reared in plastic microtubes until parasitoid emergence. Parasitoids were identified to species level using the identification key (Kavallieratos et al. 2006).

To detect differences in parasitoidism rates between the crop edge (25 m) and centre (525 m) t test was used. Also, aphid abundance was correlated with the number of mummies using Pearson rank correlation test. To check if the data residuals are normally distributed the Shapiro & Wilk (1965) test was used. All analyses were performed using the statistical software SAS (SAS Institute 2001).


In total were recorded 8,392 aphids, compound by two species Sitobion avenae (Fabricius, 1794) (85%) followed by Rhopalosiphum padi (Linnaeus, 1758) (15%) (Hemiptera: Aphididae). It was recorded 4,668 and 317 mummies in Ibipora-SAF and 3, 257 aphids and 250 mummies Londrina. In Ibipora-SAF and Rolandia-GF were reported low densities of aphids and mummies (n= 360 aphids and 10 mummies; 107 aphids and 11 mummies, each field, respectively).

Parasitoids were represented by six species: Lysiphlebus testaceipes (Cresson, 1880), Diaeretiella rapae (McIntosh, 1855), Aphidius colemani Viereck, 1912, Aphidius ervi Haliday, 1834, Aphidius uzbekistanicus Luzhetzki, 1960 and Aphidius rhopalosiphi De Stefani Perez 1902. All parasitoids emerged from mummies collected in Ibipora-SAF and Londrina (Table 1) therefore, the fields Ibipora-SAF and Rolandia-GF were excluded from parasitoidism analysis.

Pearson rank correlation showed that aphids were negatively correlated with parasitoidism in crop edge (r = - 0.67 in Ibipora-SAF and r = - 0.50 in Londrina; P [menor que o igual a] 0.01) and centre (r = - 0.50 in Ibipora-SAF and r = - 0.18 in Londrina; P [menor que o igual a] 0.05). Aphid abundance and parasitoidism rates in crop edge and interior were not affected by distance from adjacent forest edge (Fig. 1).


Aphid abundance was negatively correlated with parasitoidism rates in both distances (25 m and 525 m). On the other hand, aphid abundance and parasitoidism rates in crop edge and interior varied considerably among the fields and the hypothesis that crop edge presents higher parasitoidism rates than interior was not supported.

These findings contrast with studies conducted in temperate regions where cereal aphids and their parasitoids presented positive associations with non-crop habitats (Thies et al. 2005; Roschewitz et al. 2005). In temperate regions, aphids reproduce sexually in crop fields and eggs are laid on adjacent trees and herbaceous plants (overwintering sites) (Stary and Havelka 2008). However, under favorable climatic conditions aphids reproduce by thelytokous parthenogenesis (Simon et al. 2002). Thus, under the mild climate conditions in the Neotropics, aphids reproductiFon are done exclusively by thelytokous parthenogenesis and do not need to hibernate in trees of adjacent forest fragments. In addition, the crop rotation system adopted in the study region comprises soybean and corn in summer and wheat and corn in autumn and winter. Therefore, cereal crops are available throughout the year and crop associated species such as cereal aphids and their parasitoids probably spillover from adjacent cereal crops and not from forest fragments.

Here, first information is provided about aphid-parasitoid interactions in cereal crops and adjacent tropical forest fragments in a Neotropical region. Future studies should investigate how aphids and parasitoids interact with natural and managed ecosystems at multiple spatial and temporal scales. This information is essential to maintain and even enhance aphid biological control in agricultural landscapes.


In the present study, crop edges near forest fragments did not support higher aphid abundance and parasitoidism rates than interior. These results can be attributed to the diversity of host crops that probably allows aphids and their parasitoids spillover from other host plants to winter wheat fields and not from forest fragments. Finally is needed more studies in Neotropical region, for better understand this relationship between environment and aphid parasitoids.

Received: 28-May-2014 * Accepted: 19-Mar-2016


We are grateful to CAPES and CNPq that provided research grants to authors.

Literature cited

BIANCHI, F. J. J. A.; BOOIJ, C. J. H.; TSCHARNTKE, T. 2006. Sustainable pest regulation in agricultural landscapes: a review on landscape composition, biodiversity and natural pest control. Proceedings of the Royal Society 273 (1595): 1715-1727.

CABALLERO-LOPEZ, B., B.; BOMMARCO, R.; BLANCOMORENO, J. M.; SANS, F. X.; PUJADE-VILLAR, J.; RUNDLOF, M.; SMITH, H. G. 2012. Aphids and their natural enemies are differently affected by habitat features at local and landscape scales. Biological Control 63 (2): 222-229.

HOLLAND, J. M.; OATEN, H.; SOUTHWAY, S.; MOREBY, S. 2008. The effectiveness of field margin enhancement for cereal aphid control by different natural enemy guilds. Biological Control 47 (1): 71-76.

IAPAR (Instituto Agronomico do Parana). 2015. Available in: http:// [Review date: 22 May 2015].

KAVALLIERATOS, N. G.; TOMANOVICB, Z.; SARLISC, G. P.; FASSEASD, C.; EMMANOUELE, N. E. A. 2006. Review of the genus Aphidius Nees in Greece (Hymenoptera: Braconidae: Aphidiinae) with the description of a new species. Journal of Natural History 40: 1179-1197.

ROSCHEWITZ, I., HUCKER, M., TSCHARNTKE, T., THIES, C. 2005. The influence of landscape context and farming practices on parasitism of cereal aphids. Agriculture, Ecosystems & Environment 108 (3): 218-227.

SALVADORI, J. R.; TONET, G. E. L. 2001. Manejo integrado dos pulgoes de trigo. Passo Fundo: EMBRAPA/CNPT. 52 p. (Circular Tecnica).

SAS, 2001. User's Guide: Statistics, Version 6e. Cary. 201 p.

SHAPIRO, S. S.; WILK, M. B. 1965. An analysis of variance test for normality. Biometrika 52: 591-611.

SIMON, J. C.; RISPE, C.; SUNNUCKS, P. 2002. Ecology and evolution of sex in aphids. Trends in Ecology and Evolution 17: 34-39.

STARY, P.; HAVELKA, J. 2008. Fauna and associations of aphid parasitoids in an up-dated farmland area (Czech Republic). Bulletin of Insectology 61 (2): 252-276.

THIES, C.; ROSCHEWITZ, I.; TSCHARNTKE, T. 2005. The landscape context of cereal aphid-parasitoid interactions. Proceedings of the Royal Society 272 (1559): 2003-2010.

THIES, C.; STEFFAN-DEWENTER, I.; TSCHARNTKE, T. 2008. Interannual landscape changes influence plantherbivore-parasitoid interactions. Agriculture Ecossystem and Environment 125 (2-4): 266-268.

THOMSON, L. J.; HOFFMANN, A. A. 2013. Spatial scale of benefits from adjacent woody vegetation on natural enemies within vineyards. Biological Control 64 (1): 57-65.

TSCHARNTKE, T., RAND, T. A.; BIANCHI, F. J. J. A. 2005. The landscape context of trophic interactions: insect spillover across the crop-noncrop interface. Annales Zoologici Fennici 42: 421-432.


(1) Ph. D. Universidade Estadual de Londrina, PR, Brazil., corresponding author.

(2) Ph. D. ayres@

(3) M. Sc.

(4) M. Sc.

Leyenda: Figure 1. Aphid abundance (A) and parasitoidism (B) in wheat fields, near (25 m) and far from (525 m) the edge of forest fragments. Parana State, 2009 cropping season (April to September). (ns = non-significant). * = (Student t test; * = P [less than or equal to] 0.05). Ps. Ibipora-Bonsucesso Farm (BF) and Rolandia-Gioconda Farm (GF) had a low parasitoidism (10 and 11 mummies, respectively) what avoid to compare this parameter near (25 m) and far (525 m) the forest edge.
Table 1. Parasitoids (Braconidae: Aphidiinae) emerged from mummies
collected in Ibipora-SAF and Londrina. Wheat cropping season 2009
(April to September).

                                   Parasitized aphids

Parasitoids emerged from   Rhopalosiphum   Sitobion     Total
the collected mummies          padi         avenae    abundance


Lysiphlebus testaceipes         68            --         68
Diaeretiella rapae               1            --          1
Aphidius colemani                2            --          2
Aphidius ervi                   --            2           2
Aphidius uzbekistanicus         --            11         11
Aphidius rhopalosiphi           --            1           1


A. ervi                          3            10         13
A. uzbekistanicus               --            16         16
A. colemani                      6            1           7
Total abundance                 80            41         121
COPYRIGHT 2016 Sociedad Colombiana de Entomologia
No portion of this article can be reproduced without the express written permission from the copyright holder.
Copyright 2016 Gale, Cengage Learning. All rights reserved.

Article Details
Printer friendly Cite/link Email Feedback
Title Annotation:Articulos de investigacion
Author:Bortolotto, Orcial Ceolin; De Oliveira Menezes, Ayres, Jr.; Hoshino, Adriano Thibes; Medeiros, Hugo
Publication:Revista Colombiana de Entomologia
Article Type:Ensayo
Date:Jan 1, 2016
Previous Article:Fe de erratas 40-1 (2014).
Next Article:Diagnostico de Leucoptera coffeella (Lepidoptera: Lyonetiidae) y sus parasitoides en el departamento de Antioquia, Colombia.

Terms of use | Privacy policy | Copyright © 2018 Farlex, Inc. | Feedback | For webmasters