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Distance from the edge of forest fragments influence the abundance of aphidophagous hoverflies (Diptera: Syrphidae) in wheat fields/A distancia da borda de fragmentos florestais infuencia a abundancia de sirfideos afidofagos (Diptera: Syrphidae) em lavouras de trigo.


Hoverflies (Diptera: Syrphidae) are notably important insects because they act as pollinators (Jun, Yibo, Jin, Fazhi, & Zhenhai, 2009; Blaauw & Isaacs, 2014) and biological control agents (Irshad, 2014). In wheat crops (Triticum aestivum L.), the agronomic importance is at the larval stage, where aphid predators (Schmidt et al., 2003; Bugg, Colfer, Chaney, Smith, & Cannon, 2008) can consume up to 2,000 aphids (Dib, Simon, Sauphanor, & Capowiez, 2010; Hogg, Bugg, & Daane, 2011). Meanwhile, adult hoverflies feed on nectar and pollen, whose energy (Van Rijn, Kooijman, & Wackers, 2013) increases the reproductive rate (Laubertie, Wratten, & Hemptinne, 2012) and longevity (Pinheiro, Torres, Raimundo, & Santos, 2015). Because of the importance of floral resources to hoverflies, many studies have been conducted to promote the action of this natural enemy in crop fields using landscape management (Hickman & Wratten, 1996; Bokina, 2012; Amaral et al., 2013; Gontijo, Beers, & Snyder, 2013; Martinez-Una, Martin, Fernandez-Quintanilla, & Dorado, 2013; Haenke et al., 2014).

Moreover, the remaining forest fragment may act as an area of refuge to natural enemies during little abundance of pests in crop fields (Koh & Holland, 2015). In Brazil, although several studies have shown that natural enemies are highly efficient in suppressing aphid infestation in wheat crops (Salvadori & Salles, 2002; Alves, Prestes, Zanini, Dalmolin, & Menezes Jr., 2005; Bortolotto, Menezes Jr., Sampaio, & Hoshino, 2012; Bortolotto, Menezes Jr., & Hoshino, 2015), have no investigation about the influence of non-crop fields on these natural enemies. Among the conservative management strategies, the maintenance of non crop habitats has been studied to understand the importance of natural enemies (Barbosa, 1998; Walton & Isaacs, 2011; Letourneau, Bothwell, & Stireman, 2012; Fahrig et al., 2015). However, it is important to consider that most studies were developed in temperate regions. Hence, the importance of the remaining forest fragment near crop fields and its contribution to natural enemies are unavailable for the Neotropical agroecosystem. In adittion, some investigations were reported a devastation of native forest fragments in Brazil reducing non-crop areas (Fearnside, 2001; Nassar, 2009), and this practice caused impact on biodiversity (Vieira, Toledo, Silva, & Higuchi, 2008). In this sense, it is important to develop research to increase understanding about the importance of remaining forest fragments for natural biological control, and to encourage growers to maintain refuge areas in their farms. Thus, this study investigates the effect of the distance from the edge of a forest fragment on aphidophagous hoverflies in wheat fields.

Material and methods

Study site

The study was performed in four commercial wheat crops in northern Parana State, Brazil, during the 2009 crop season (usually in approximately April/May to August/September). The sites located in the municipalities of Ibipora-Santo 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) (23[degrees] 23' 59" S 5[degrees] 19' 01" W), and Londrina (23[degrees] 19' 49" S 51[degrees] 08' 12" W) (Table 1).

In all of the studied fields, wheat was sown in succession to soybean [Glycine max (Merrill) L.] in no tillering soil. The fields were sown on April 29 (Rolandia-GF), May 6 (Ibipora-FBS), May 8 (Ibipora SAF), and May 11 (Londrina). In general, the landscape complex around each farm (with an approximately 2 km radius) was primarily composed of wheat crops (32 to 47%), followed by non-crop area [Atlantic forest fragment (compound majority by Aspidosperma polyneuronand; Ficus spp.; Euterpe edulis; Orchidaceae and grasses) and pasture] (26.2 to 39%), maize (7 to 26.5%) and cofee crops (2.9 to 20.5%). Expeptionally in Ibipora-SAF oleraceous, fruits and fallow areas (predominantly infested with wild radish) were reported.

Hoverfly survey

Hoverflies were assessed in two transects (90 m in length) that demarcated each field (adapted from Murta, Ker, Costa, Espirito-Santo, & Faria, 2008). The transects were set up immediately after the emergence (phenological stage V1) of wheat crops in all fields except Londrina, which was demarcated one day after sowing. In this sense, the assessment of hoverflies began on the same day that the transect was demarcated. To compare the "edge effect", one transect was demarcated at 25 m from the edge (near), and the other was at 525 m from the forest edge (far).

The hoverfly abundance was monitored using Malaise traps (Petanidou, Vuji, & Ellis, 2011), which were placed at the center of each transect (n = two traps field-1). The traps were made of a synthetic material and shaped like a tent, with an opening at the bottom that intercepted the insects during flight after they collided with one of the trap's septa. The traps were installed and positioned to face north, where the most sunlight was received. Each trap was approximately 1.80 m high X 1.80 m long. The collecting bottle contained 70% alcohol, which was changed weekly on the day that the number of aphids was counted. In the laboratory, the collected material was screened, and the hoverflies were identified using a stereoscope microscope according to an identification guide (Marinoni, Morales, & Spaler, 2007; Borges & Couri, 2009; Mengual, Ruiz, Rojo, Stahl, & Thompson, 2009).

Aphids survey

Aphid assessment was made for both distances (25 and 525 m from the edge of the forest). Each transect contained 10 evaluation points, where 20 tillers at each point were randomly evaluated (n = 400 tillers assessment in each field). All aphids were quantified and identified to the species level. To reduce interference, insecticides were not applied to a distance of 5 m from the evaluation points.

Similar to the hoverfly assessment, the aphis infestation survey began on the same day that the transect was demarcated, except in Londrina (seven days after the transect was demarcated). The assessments were performed on a weekly basis, and the aphid species were identified using a guide developed by Salvadori and Tonet (2001).

Statistical analysis

The aphid means were subjected to exploratory analyses to assess the assumptions of the normality of residuals, homogeneity of variance of the treatments, and additivity of the model to allow for parametric tests. The aphid abundance near (25 m) and far (525 m) the edge of the forest was compared using Student's t-test.

To compare the hoverfly abundance, the specimens were summed at each growth stage (except Rolandia-GF because of low abundance) and compared using a [chi square] (Chi-square) test. In adittion, the relationship between aphid and hoverfly abundance (density-dependence) was estimated using a quadratic regression model. The difference was considered significant only when the significance level was p < 0.05.

Results and discussion

In total, 1,845 adult hoverflies were captured, which represented 15 species and three genera (Table 2). The most abundant aphidophagous hoverfly species were Allograpia exoiica (60.43%), Toxomerus dispar (17.78%) and Toxomerus waisoni (26.7%) (Diptera: Syrphidae). The reported major abundance of Allograpia and Toxomerus genus in the present study is consistent with that obtained in a previous report in the Neotropical region (Thompson, 1999), which indicates the adaptation of these hoverflies.

Interestingly, during the wheat tillering stage, consistently higher hoverfly abundance was reported near (25 m) the forest edge than far (525 m) from the edge of the forest (Figure 1). In this period, the predominant species was A. exoiica (58%), which was followed by Pseudodorus clavaius (12%) (Diptera: Syrphidae). In Rolandia-GF farm, a low hoverfly abundance was captured (n total = 74), which did not allow us to perform a statistical test at each growth stage. However, the total abundance was higher near the forest edge (25 m) than far (525 m) from the edge of the forest fragment (Figure 1).


The highest abundance of A. exotica indicates a nice stablishment of this specie in wheat crop. In a study developed by Greco (1995) the authors reported A. exotica strongly associated with the aphid abundance in wheat fields, reforceing the importance of this specie for aphid supression. In the current study, the aphids were represented by only two species: Sitobion avenae, which exibited greater abundance (85%) (Hemiptera: Aphididae), and Rhopalosiphum padi (15%) (Hemiptera: Aphididae). The highest aphid abundance was reported during the wheat grain stage (Figure 2), which can be explained by the largest occurrence of S. avenae.


Unlike the present study, Alves et al. (2005) reported highest aphid infestation before the reproductive growth of wheat. However, in that case, R. padi was the predominant species. Therefore, the higher infestation of S. avenae in the present study is probably associated with decreased abundance of R. padi related to wheat growth. This promotes competition among the species, favouring S. avenae development during grain stage of wheat (Gianoli, 2000).

In general, the infestation of aphids was not associated with the distance from the forest fragmente and varies according to the study site. For example, differences were observed only in the grain stage, and in Ibipora (SAF), a higher abundance of aphids was recorded far (525 m) from the edge of the forest, whereas in Londrina, a higher infestation of the pest was reported near (25 m) to the edge of the forest (Figure 2). This fact indicates that aphids are not dependent of refuge area, as opposed of the initial abundance of hoverflies reported in this study.

Is important to emphasize that both aphid species present in wheat fields, R. padi and S. avenae are prey to A. exotica (Rojo, Gilbert, Marcos-Garcia, Nieto, & Durante, 2003; Bokina, 2012), which can contribute to highest abundance of this hoverfly specie in wheat fields (Table 1). In addition, some studies have reported that the hoverflies T. watsoni and T. dispar usually occur less frequently than A. exotica in open fields (Greco, 1995; Arcaya, Mengual, Banon-Perez, & Rojo, 2013), and that this species are probably less adapted to agroecosystems. One important factor that needs attention is that A. exotica has been reported in the Brazilian agroecosystem to prey on many aphids in oleraceuous and fruit gardens (Resende et al., 2006; Sturza, Dorfey, Poncio, Dequech, & Bolzan, 2011) and to have other prey, such as mites, thrips and newly hatched caterpillars (Rojo et al., 2003). Thus, we believe that the wide spectrum of preys of A. exotica is likely the main reason for its widespread occurrence in all areas and its adaptability to local agroecosystems because of food availability during the larval and adult stages. Secondly, it is necessary to consider the influence of climatic factors on hoverflies, because the microclimate in wheat fields can favour A. exotica in relation to other hoverflies species. However, there is very little information about the bioecology of these aphid predators and additional studies are necessary to verify this hypothesis.

Although flowers cultivated efficiently increases aphidophagous hoverflies around crop fields (Amaral et al., 2013; Gontijo et al., 2013; Martinez Una et al., 2013; Haenke et al., 2014), in the present work, is important to emphasize that we did not sow strip flowers; thus, our data strongly indicate the relevance of preserving native forest fragments to the survival of aphidophagous hoverflies during low aphid infestation in wheat crops. This report is supported by another study in Parana State, which was developed by Marinoni, Miranda, and Thompson (2004). Their study found a larger abundance of Allograpta and Toxomerus in hedge forest than open fields (pasture), which indicates the availability of benefical resources to aphidophagous hoverflies.

The other factor is probably the presence of alternative prey for hoverfly larvae near the hedge. In this sense, this relation was previously reported by Koh and Holland (2015), which showed that Anthocoridae predators were in soybean crops before aphid infestation and survived because of the presence of alternative prey and floral resources or weeds. In the present study, during wheat tillering in Londrina, for example, only four aphids were quantified in the wheat fields, which indicates that the larvae of aphidophagous hoverflies can survive by feeding on other insects such as other aphid species and catepillars, in some cases, according to other studies (Rojo et al., 2003; Sturza et al., 2011). This fact reinforces the hypothesis of the importance of forest fragments to increase or mantain hoverfly abundance near the hedge during low aphid infestation in the fields.

Furthermore, the beneficial effect of forest fragments or refuge areas can vary according to the studied taxa or the local climate. In this sense, Raymond et al. (2015) reported a higher abundance of non-aphidophagous hoverflies in the hedge forest, whereas aphidophagous hoverflies were more abundant in crops, which are associated with a high availability of prey. However, in this study, we found a prevalence of aphidophagous predators in general, which was associated with the aphid abundance, but they were initially more abundant near the hedge forest fragment. Thus, the hedge "effect" on hoverflies was reported only in wheat tillering, and the distribution varied among the fields after this wheat growth stage, likely because of the expected relation with aphid infestation (Table 3). The exception was found near (25 m) the edge in one field (Londrina) (Table 3). Although this result is not clear, we hypothesized that another wheat field, which was sown later than the assessed field at approximately a distance far (525 m) from the edge, affected the hoverfly behavior and likely contained better-quality available aphids for consumption.

The importance of hoverflies in wheat fields can be atribute due female hoverflies strongly respond to aphid infestation and can locate even small colonies of the pest (Almohamad, Verheggen, & Haubruge, 2009). In this sense, several studies have shown that hoverflies are highly affected by the presence of infochemicals. For example, Leroy et al. (2014) found that the honeydew excreted by Acyrtosiphum pisum (Hemiptera: Aphididae) increased the oviposition of Epysirphus balteatus (Diptera: Syrphidae). In addition, other studies have shown that even in the absence of honeydew, the presence of aphids stimulates hoverfly oviposition and cairomone emission from the infested plants (Francis, Martin, Lognay, & Haubruge., 2005; Harmel et al., 2007; Verheggen, Arnaud, Bartram, Gohy, & Haubruge, 2008). Thus, although forest fragments can aid in hoverfly survival during low aphid infestation in the field, our data indicate that when the aphid infestation increases in wheat fields, these infochemical signals stimulate aphidophagous hoverflies to forage preys and those floral resources can be less important at this time.

Is important to consider that many natural enemies are present in agroecossystem and contribute with aphid suppression. Although the present study showed hoverflies associated with aphid abundance (Table 3), other biological control agents acted against aphid infestation also. In Brazil, after implementation of biological control of aphids of wheat (BCAW) program, parasitoids are mainly responsible for reducing aphid infestation (Salvadori & Salles, 2002; Bortolotto et al., 2012). In the present work, we report an average parasitism between 6.8 and 16.9% among the fields. Another natural enemy associated with reduced aphid abundance was the predator Dolichopodidae ([R.sup.2] = 0.37 to 0.56; p < 0.05), supporting the importance of natural biological control against this pest in wheat fields. So, these natural enemies reported in this study can justify the weak influence of hoverflies on aphid abundance.

Although this subject is not the main objective of the study, the forest fragment quality was not associated with the abundance and richness of hoverflies. This result was observed in Ibipora (SAF), which had the largest number of individuals and the largest richness, although it contained a forest section with intermediate biotic quality (Table 1). Our data indicate that the abundance can be explained by the fact that this area also had the highest infestation of aphids, which suggests a density-dependent relationship. However, the hoverfly richeness must be linked to other factors that were not measured in the study, such as the diversity of plants on site in the agroecosystem, environmental complexity on a regional scale (Fahrig et al., 2015) and historical management of crops (input of pesticides) (Bokina, 2012). Thus, these factors must be investigated in other studies to better understand the relation between hoverflies and the environment.

Finally, this study reports for first time the importance of preserving areas of forest fragments as a refuge and likely source of supplies for aphidophagous hoverflies in Brazilian agroecosystems. There is currently a great necessity for similar studies in developing tropical regions because of the lack of such information. Thus, other aspects should be considered for further studies, such as identifying the weeds in the vicinity of the crop to select potential plants to be grown to attract these natural enemies in regions with poor natural biodiversity.


Hoverfly abundances are initially higher near the edge of the forest fragment. After the aphid abundance in wheat fields increases, the hoverfly population depends on the prey infestation.

Doi: 10.4025/actasciagron.v3812.27711


We are grateful to Dra Mirian Morales for assisting in identification of insects and Capes and CNPq for providing the post-graduate scholarship.


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Received on May 7, 2015. Accepted on August 10, 2015.

Orcial Ceolin Bortolotto *, Ayres de Oliveira Menezes Junior, Adriano Thibes Hoshino and Thiago Augusto Campos

Universidade Estadual de Londrina, Rua Celso Garcia Cid, s/no., 86057-970, Campus Universitario, Londrina, Parana, Brazil. * Author for correspondence. E-mail:
Table 1. Farm description and climatic data during the study. Parana
State, crop season (May to September of 2009).

Description                          Farms

                           Ibipora   Ibipora   Rolandia   Londrina
                            (SAF)     (BF)       (GF)

Wheat field (size)         2.3 ha    16.2 ha   20.9 ha     11.4 ha
Forest fragment (size)      45 ha    24.5 ha    380 ha      25 ha
Rapid Ecological             34        28         48         50
  Assessment (1)
Ecological Integrity (1)   Medium     Poor       Good     Excellent
Climatic data                --        --         --         --
Temperature average         20.54     20.54       17        17.5
Rainfall total (mm)        461.00    461.00     351.7       585.9

(1) Methodology and classification according to Medeiros and Torezan

Table 2. Hoverflies (Diptera: Syrphidae) captured in Malaise trap
during the crop season of 2009 (May to September) in the Northest of
Parana State.


Syrphidae species         Ibipora   Ibipora   Rolandia
                           (SAF)     (BF)       (GF)

Allograpia annulipes         3         0         0
Allograpia exotica          794       169        40
Allograptafalcata            3         0         0
Allograpia hasiaia           3        10         0
Allograpia neoiropica        3         0         0
Allograpia obliqua           0         0         3
Pseudodorus clavaius         6         0         13
Ocypiamus dimidiaius         3         0         0
Ocypiamus gasirosiacius      0         9         0
Ocypiamus sp.1               3         0         0
Ocypiamus sp.2               0         0         0
Ocypiamus sp.3               0         0         0
Syrphus phaeosiigma          3         0         6
Toxomerus dispar            258       15         0
Toxomerusfloralis            0         0         3
Toxomerus lacrymosus         3         0         0
Toxomerus poliius            0         3         9
Toxomerus sp.               52        22         0
Toxomerus waisoni           134        0         0
Trichopsomyia sp.            3         0         0
Absolute abundance         1,271      228        74
Relative abundance        68.89%    12.36%     4.01%
Richness                    14         6         6


Syrphidae species         Londrina   Absolute   Relative

Allograpia annulipes         0          3        0.16%
Allograpia exotica          112       1,115      60.43%
Allograptafalcata            0          3        0.16%
Allograpia hasiaia           0          13       0.70%
Allograpia neoiropica        0          3        0.16%
Allograpia obliqua           3          6        0.33%
Pseudodorus clavaius         18         37       2.01%
Ocypiamus dimidiaius         9          12       0.65%
Ocypiamus gasirosiacius      0          9        0.49%
Ocypiamus sp.1               0          3        0.16%
Ocypiamus sp.2               3          3        0.16%
Ocypiamus sp.3               3          3        0.16%
Syrphus phaeosiigma          3          12       0.65%
Toxomerus dispar             55        328       17.78%
Toxomerusfloralis            12         15       0.81%
Toxomerus lacrymosus         0          3        0.16%
Toxomerus poliius            6          18       0.98%
Toxomerus sp.                48        122       6.61%
Toxomerus waisoni            0         134       7.26%
Trichopsomyia sp.            0          3        0.16%
Absolute abundance          272       1,845       100%
Relative abundance         14.74%       --        100%
Richness                     11         --         --

Table 3. Relationship between aphid abundance and hoverflies
near and far from the forest edge. Regression polinomial
quadratic test. Parana, wheat season (May to September of 2009).

Farm                                     Distance from edge

                       Near (25 m)                 Far (525 m)

                 F       p      [R.sup.2]    F       p      [R.sup.2]

Ibipora (SAF)   4.39   < 0.01     0.36      5.38   < 0.01     0.42
Londrina        0.56    n.s       0.08      6.24   < 0.01     0.48
Ibipora (BF)    2.26    0.03      0.20      2.51    0.03      0.25

* Rolandia (GF) was not possible for a statistical analysis because
of the low aphid and hoverfly abundances.
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Author:Bortolotto, Orcial Ceolin; Menezes, Ayres de Oliveira, Jr.; Hoshino, Adriano Thibes; Campos, Thiago
Publication:Acta Scientiarum. Agronomy (UEM)
Date:Apr 1, 2016
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