Arthropods biodiversity index in Bollgard[R] cotton (CrylAc) in Brazil/Indice de biodiversidad de artropodos en algodon Bollgard[R] (CrylAc) cultivado en la region de cerrado en Brasil/Indice de biodiversidade de artropodes em algodao Bollgard[R] (CrylAc) no Brasil.
Shannon-Wiener's diversity index (SWI) was used under untreated conditions of a cotton field during the 2006/2007 crop season in the Cerrado region, Brazil. Comparison was carried out between the transgenic NuOpal[R] (BollgarcF)(CrylAc) and the non-transgenic isogenic variety DeltaOpaP. SWI was calculated for target pests, non-target herbivores and predators groups. Two sampling methods were used: whole plant observation and beat sheet. As expected, the mean number of target pests, especially Pectinophora gossypiella (Sound.) and Alabama argillacea (Hubner), was significantly smaller in Bt cotton. In the whole plant method sampling the SWI for non-tar get herbivores was significantly higher in Bt-cotton. The mean number of Anthonomus grandis (Boh.) and Edessa meditabunda (Fabr.) adults were significantly higher in NuOpal[R] with the whole plant sampling method. However, such differences were not observed with the beat sheet method. For the natural enemies, SWI and mean number of larvae and adults of the dominant predators did not show any significant difference between Bt and non-Bt cotton. These results confirm the conservation of some tritrophic interactions inside the Bt (untreated) cotton and contributes to a better sustainable management of nontarget pests by enhancement of their natural biological control.
El indice de biodiversidad de Shannon-Wiener's (ISW) fue utilizado en areas dedicadas al cultivo de algodon no tratadas insecticidas. El trabajo se realizo en areas algodoneras localizadas en la region de Cerrado, Brasil. Se comparo el algodon transgenico NuOpal[R] (BollgarcPjjCrylAc) con la isolinea no transgenica DeltaOpaP. El indice de biodiversidad fue calculado para todos los insectos presentes en el agroecosistema algodonero, incluyendo los insectos plagas de la variedad Bt, convencionales y enemigos naturales. Los metodos de muestreo utilizados fueron el uso del pano de sacudida y la planta entera. Como era previsible, el valor promedio calculado de las plagas, especificamente Pectinophora gossypiella (Sound.) and Alabama argillacea (Hiibner), fue significativamente menor en el algodon Bt. El ISW para los insectos plagas fue significativamente mayor en algodon Bt con el metodo de planta entera, en tanto que la media poblacional de adultos de Anthonomus grandis (Boh.) y Edessa meditabunda (Fabr.) fue mayor en NuOpal[R] usando el mismo metodo. No obstante, esta diferencia no fue observada con el metodo de pano de sacudida. Por otra parte, el ISW, para los enemigos naturales y el valor de la media poblacional de larvas y adultos de los predadores dominantes no presentaron diferencia significativa entre el algodon Bt y el convencional. Estos resultados corroboran la conservacion de las interacciones tritroficas en el algodon Bt (no tratado con insecticidas) y aporta nuevos elementos tecnicos para manejo integrado de insectos con enfasis en su control biologico natural.
O indice de diversidade de Shannon-Wiener (ISW) foi utilizado em condicoes de cultivo de algodoeiro nao tratado, sem aplicacao de inseticidas durante a safra 2006/2007 no Cerrado, Brasil. Foi realizada comparacao entre NuOpal[R] (BollgarcP)(CrylAc) e sua isolinha nao transgenica. O indice foi calculado para pragas-alvo do algodao Bt, pragas nao-alvo e inimigos naturais. Foram utilizados dois metodos de amostragem: planta inteira e pano de batida. Como esperado, o numero medio de pragas-alvo, especialmente Pectinophora gossypiella (Sound.) e Alabama argillacea (Hiibner), foi significativamente menor em algodao Bt. Na amostragem por planta inteira, o ISW para herbivoros nao-alvo foi significativamente maior em algodao Bt. O numero medio de adultos de Anthonomus grandis (Boh.) e Edessa meditabunda (Fabr.) foi significativamente maior em NuOpal[R] utilizando o metodo de amostragem de planta inteira. Entretanto, esta mesma diferenca nao foi observada com o metodo do pano de batida. Para inimigos naturais, o ISW e o numero medio de larvas e adultos de predadores dominantes nao apresentou diferenca signficativa entre algodao Bt e nao-Bt. Estes resultados confirmam a conservacao de algumas interacoes tritroficas dentro do sistema algodao Bt (nao pulverizado) e contribui para um manejo de herbivoros nao-alvo sustentavel pelo incremento do seu controle biologico natural.
KEYWORDS / Bt-cotton / CrylAc / Diversity / Herbivores Non-Target / Predators / Shannon-Wiener's Index /
Biological communities have a degree of organization that is represented by their specific abundance distribution or relative frequency of the species present in the environment. The biological diversity in one biological community has two components: species richness (existing species number) and homogeneity, which depends on the larger or smaller uniformity of the distribution frequency of existing species (Hurlbert, 1971). The importance of the use of diversity indexes is their application in monitoring studies of biological communities dynamics and structural change detection, when the community environment is modified and the species have to adapt to the modifications, so as to contribute with the conservation of biodiversity in agroecosystems (Southwood, 1995).
Genetically modified (GM) cotton varieties expressing the Bacillus thuringiensis (Bt) CrylAc protein (NuOpal[R] and DP90B) were introduced commercially in Brazil during the 2006/2007 crop season. Knowledge about the non-target species (herbivores and natural enemies) present in the Bt-cotton in different field conditions is still incipient in Latin America, in spite of the economic importance of knowing the biological diversity and maintaining a biological control during the introduction of GM crops (Romeis et al., 2008; Lovei et al., 2009; Adenle, 2012).
Pest resistant GM varieties were initially grown in countries such as the USA, Argentina, Australia, China, Mexico and South Africa, allowing fewer insecticide applications, reduction in production costs and reduction of the risks to human health (Shelton et al., 2002; Naranjo, 2009). Another aspect is the promotion and the preservation of natural enemies, contributing to integrate pest management systems with a strong biological control component and assessment of risk of Bt-cotton to non-target arthropods, leading to a sustainable production and preserving the environment (Romeis et al., 2006; 2008; Sarvjeet, 2012).
There are few published studies conducted about the impact of the Bt-cotton varieties on the diversity of arthropods, especially with respect to the values found in diversity indexes, like the Shannon-Wiener's index. Using this index, no difference in arthropod biodiversity between Bt and non-Bt cotton was shown by Li et al. (2002), or an increase in the arthropod communities diversity and pest sub-communities (Men et al., 2003). In Brazil, Ramiro and Faria (2006) observed no significant differences in the total predator specimens collected from Bollgard[R] cotton as compared to treatments with Delta Pine Acala 90, with or without chemical control of caterpillars.
The objective of this research was to study the arthropod biodiversity associated with Bt-cotton (NuOpal[R]), as compared to the non-transgenic isogenic DeltaOpal[R] in the absence of insecticide sprays, promoting the knowledge of structural changes in arthropod communities in the Bt and non-Bt cotton, constituting a basis for the regulation of population dynamics of insect pests and the damage caused by such pests. This paper presents the first study of biodiversity of non-target herbivores and natural enemies (mainly predators) sampled with two methods: whole plant and beat sheet, in the Brazilian Cerrado Biome (Savannah) region, Mato Grosso do Sul State, Brazil. A faunistic analysis of the genera and species found on Bt-cotton compared with non Bt-cotton using the Shannon-Wiener's index is discussed.
Materials and Methods
This research was conducted at the Faculdade de Ciencias Agrarias (FCA), Universidade Federal da Grande Dourados, in Dourados, Mato Grosso do Sul,, Brazil, between February and June 2007. An irrigation system was installed in order to facilitate crop development during the experiment. Basic and side dressing fertilizations were performed with 400kg x [ha.sup.-1] NPK (8-20-20). Conventional planting system was adopted. Soil tillage was accomplished on February 14, 2007, before seeding by plowing and harrowing,. Seeds of the NuOpal[R] (Bt) and DeltaOpal[R] (non-Bt) varieties used in the experiment were provided by MDMSeeds of Cotton[R], and were pre-treated with the fungicides Euparen[R] (tolylfluanid) (200g/100kg seeds), Monceren[R] (pencycuron) (200g/100kg seeds), and Baytan[R] (triadimenol) (40ml/20Kg seeds), in order to control diseases that cause damping-off. Both varieties were manually seeded on February 15, 2007, at a density of 13 seeds/m and a row spacing of 0.90m. Emergence occurred 4 days later. Weed control was performed by hand-weeding during the entire cycle for both varieties. Blitz[R] baits (fipronil) were applied at the beginning of the crop cycle on the surroundings of the experimental area to control leaf-cutting ants of the genera Atta and Acromyrmex.
The total experimental area was 18x72m (0.12ha) with 32 sub-areas (plots) that were demarcated by random drawing, 16 for each treatment: DeltaOpal[R] and NuOpal[R]. Each Each sub-area comprised five rows of the treatment variety, measuring 4.5x9m. The three central rows were sampled; one row at each end of each subarea was the border of the sampling unit. In order to reduce the incidence of Anthonomus granais (Boheman, 1843) during the experiment, 23 traps were installed containing grandlure pheromone + insecticide, to capture boll weevils in the vicinity of the experiment area.
The sampling and quantification of the Bollgard[R] technology target insects, non-target pests, and natural enemies found were performed every seven days during the entire evaluation period, from the crop's VE stage (emergence), on February 21, until June 13. Two visual sampling methods were used: 'beat sheet', recommended by (Degrande et al., 2003), and 'whole plant'. Seventeen whole plant samplings and 8 beat sheet samplings were made for each treatment, preparing 272 replicates for the whole plant method and 128 for the beat sheet method in each treatment over the experimental period.
In the beat sheet method, samplings were taken in the crop inter-row between the three central rows of each sub area, at a random point, totaling 16 points per treatment and observation date. The beat sheet was white to facilitate insect visualization; sheet width matched the crop row spacing (0.9m), had a lm length, and was adjusted so as to cover the inter-rows. Then, both rows were vigorously shaken, causing the insects, either immature or adult, to fall onto the sheet, allowing them to be visualized, counted, and identified at the family and/or species level while still in the field. The presence of the parasitoid Catolaccus granais (Burks, 1954) and the target lepidopteran Pectinophora gossypiella was quantified in this method by the number of damaged reproductive structures (bolls) fallen onto the beat sheet. The bolls were then opened to reveal individuals of those insects.
In the whole plant evaluation method, ten plants were evaluated separately on the three central rows of each sub area, i.e., 160 plants per treatment and observation date, by quantifying and identifying the insects sampled at the family and/or species level while still in the field.
In both methods, when necessary, those insects that could not be identified in the field were collected and placed in a recipient with 70% ethanol and taken and after taken to the laboratory for later identification. Samplings for Heliothis virescens and Alabama argillacea eggs were made with the whole plant method.
The diversity in Bt and nonBt cotton with both sampling methods was based on calculations of frequency indices, constancy, abundance, and dominance (Silveira-Neto et al., 1976), considering the number of small (<1.0cm) and large caterpillars (>1.0cm), larvae, nymphs, and adults. Absolute frequency was defined as the total number of specimens observed in the various sampling conditions.
Constancy was defined as the percentage of samples in which a given species was present (Uramoto et al., 2005). After the constancy percentages over the sampling periods were obtained, the species were grouped into three categories: 'constant' (w), present in more than 50% of the weekly observations; 'accessory' (y), present in 25 to 50% of the observations; and 'accidental' (z), present in less than 25% of the observations.
Abundance is the number of individuals of a given species divided by the surface or volume unit, and may vary in space and time (Silveira-Neto et al., 1976). In order to estimate abundance, the limits established by the confidence interval (Cl) at 5 and 1% probabilities were used, and the following five classes were determined: 'rare' (r) with a number of individuals in the species smaller than the lower Cl limit at 1% probability; 'dispersed' (d) with a number of individuals between the lower limits of the confidence intervals at 1% and 5% probability; 'common' (c) within the confidence interval at 5%; 'abundant' (a), between the upper limits of the confidence intervals at 5% and 1% probability; and 'very abundant' (va) with a number of individuals greater than the upper Cl limit at 1% probability.
An organism is considered dominant when it receives impact from the environment and becomes adapted to it (Silveira-Neto et al., 1976). In the present study, a species was considered 'dominant' when its relative frequency was >1/S, where S: total number of species found in the sampling period.
In order to compare the mean differences between groups of target pests, nontarget pests, natural enemies and individuals of dominant species within each group, the development stage of the specimens was taken into consideration. The comparison between Bt and non-Bt treatments was calculated based on the mean of each treatment throughout the entire sampling period. The Student's t test was later used at a significance level [alpha]=5%. The original data were not normally distributed, and the test was applied to the data transformed to [square root of X+0.5], thus meeting the assumptions associated with the model.
Target pest, non-target pest and natural enemy diversity in Bt and non-Bt-cotton environments were studied using Shannon-Wiener's index with a correction factor and natural logarithm (Poole 1974), by means of specimen frequency. This index measures the degree of uncertainty in predicting to which species will belong a randomly selected individual, from a sample with S species and N individuals (Silveira-Neto et al., 1976).
The smaller the Shannon-Wiener's index value, the smaller the degree of uncertainty, therefore reflecting the low diversity of a sample. Diversity tends to be higher for higher index values (Uramoto et al., 2005). Student's t test was used to check whether the species diversity difference between those environments was significant at [alpha]=5%. Data were analyzed using the statistical software package SPSS[R] (SPSS, 2006).
Results and Discussion
A total of 55 species were observed, distributed among 11 orders and 32 families, and were divided into three groups: target pests, non-target pests, and natural enemies (Table I). The very abundant (va) species of non target herbivores, both in NuOpal[R] and DeltaOpal[R] cotton with the whole plant and beat sheet methods, were Horciasoides nobilellus (Bergston, 1883) and Dysdercus sp. The species Bemisia tabaci (Gennadius, 1889) and Agallia albidula (Uhler, 1895) were very abundant in Bt and nonBt cotton only with the whole plant method. The species Edessa meditabunda (Fabr., 1794), however, was very abundant in both varieties, but only with the beat sheet method. The non-target species Anthonomus grandis (Boheman, 1843) was found to be abundant in Bt cotton with both sampling methods.
The fact of B. tabaci was observed as the most abundant species with similar population densities between Bt and non-Bt cotton in the whole plant method (Naranjo, 2005) can be attributed to the behavior of this insect. Its quick flight when the plant is touched, made it difficult to be sampled by beat sheet, demonstrating the importance of selecting the adequate sampling method to monitor non-target insects with an economic importance in transgenic varieties in the field (Naranjo et al., 2005; Wade et al., 2006). Another point that will be considered is the differences in 'leaf hair' between the cotton varieties and in the mode of action of Bt toxins inserted in these genetically modified cotton varieties, which can influence the abundance of insects, as observed in Australia (Whitehouse et al., 2007), with high numbers of whitefly in Bt cotton (VipCotton).
Dominance was found in the target pest group for the species A. argillacea and P. gossypiella in non-Bt cotton, with both sampling methods. The presence of the species H. virescens was also detected, but at a low frequency when compared with the other two target pests, i.e., one caterpillar in DeltaOpal[R] with both sampling methods. The non-target herbivores species, A. grandis, H. nobilellus, Euschistus heros (Fabr., 1798) and Dysdercus sp. were dominant in both varieties with both sampling methods, while B. tabaci and A. albidula were dominant in both NuOpal[R] and DeltaOpal[R] only with the whole plant method. For the pentatomid species Nezara viridula (L., 1758) and E. meditabunda, the dominance was observed in both varieties, but only with the beat sheet method. In the whole plant sampling, the sucking herbivore species E. meditabunda was dominant in NuOpal[R] only, while the chewing herbivore Diabrotica speciosa (Germar, 1824) was dominant only in the Bt variety, with the beat sheet sampling (Table I).
These dominance results showed the reduction in feeding competition between nontarget herbivores and target insects controlled by the Bollgard[R] technology, as a reduction in competition for food resources with target caterpillars controlled by the CrylAc toxin and the sucking herbivores like the pentatomids and mirids. They show the importance of the knowledge of bioecology interaction between insects in an agroecosystem.
Also, the sampling method used can influence the quantification of each insect species affecting the Bt and non-Bt varieties, considering the behavior of each species and their migration from soybean varieties to cotton (Lu et al., 2010), as in the case of some pentatomids, searching food resources in the cotton-soybean agroecosystem. The correct selection of the sampling method leads to real interpretations about the effect of the GM plant on the arthropod population, and consequently on the biological control, which may be potentiated with the adoption of Bt crops.
Considering the constancy throughout the sampling period, A. argillacea had constant incidence only in non-Bt cotton with the whole plant method. The constant non-target herbivore species in both NuOpal[R] and DeltaOpal[R] in both samplings were D. speciosa, H. nobilellus, E. meditabunda, E. heros, N. viridula (L., 1758) and Dysdercus sp., while B. tabaci, A. albidula, Piezodorus guildini (Westwood, 1837), Jansonius boggianii subaeneus and Frankliniella sp. were constant in both Bt and non-Bt cotton with the whole plant sampling, and A. grandis and Pseudoplusia includens (Walker, 1857) were constant in both types of cotton with beat sheet sampling. The non-target herbivores species Lagria villosa (Fabr., 1783), Astylus variegatus (Germar, 1824), Neomegalotomus parvus (Westwood, 1842), A. albidula, Piezodorus guildini (Westwood, 1837) and Spodoptera eridania (Cramer, 1782) were constant only in Bt cotton with the whole plant method (Table I).
With regard to non-target herbivores diversity, the Shannon-Wiener's index with the whole plant method for Bt cotton showed statistically significant differences, being higher than non-Bt, thus demonstrating that the NuOpal[R] variety showed higher diversity of non-target herbivores than the DeltaOpal[R] variety with the whole plant sampling. However, in the beat sheet method, the index did not show significant difference (Table II). This result in the diversity index can be explained by fact that the mean number of the non-target herbivores A. grandis
and E. meditabunda adults in the whole plant method was significantly different between Bt and non-Bt cotton, being higher in Bt cotton than non-Bt (Table III). Yet, such difference was not observed with the beat sheet method (Table IV). The mean number of target pest individuals observed with both sampling methods was significantly smaller in NuOpal[R] than in DeltaOpal[R].
The results of the faunistic analysis of non-target species of CrylAc (Bollgard[R] cotton) sampled between the NuOpal[R] and DeltaOpal[R] environments demonstrate that abundance, dominance and constancy of the species can be attributed to several factors, such as the lack of insecticidal activity of the transgenic variety (CrylAc) on non-target herbivores and predators in NuOpal[R], which can affect directly the diversity and trophic interactions of these insects, promoting the knowledge of these tritrophic interactions and the integration of Bt cotton use and biological control (Li et al., 2002; Romeis et al., 2008).
Among the natural enemies sampled, predators were mainly present. The predators Araneae, Cycloneda sanguinea (L., 1763) and Scymnus sp. were very abundant both in NuOpal[R] and DeltaOpal[R] with both sampling methods. With the beat sheet method, the parasitoid species C. grandis was abundant both in NuOpal[R] and DeltaOpal[R], and the predator bug Orius sp. was abundant in non Bt cotton only.
Dominant natural enemies both in Bt and non-Bt cotton, with both the whole plant and beat sheet methods, were Araneae, C. sanguinea, Scymnus sp., Geocoris sp. and C. grandis. On the other hand, the predator Orius sp. was dominant in both NuOpal[R] and DeltaOpal[R] with the beat sheet method. However, this bug was only dominant in DeltaOpal[R] with the whole plant sampling. The beneficial arthropods Araneae, C. sanguinea, Scymnus sp. and Geocoris sp. Did not vary in both Bt and non-Bt cotton with both sampling methods. However, in the beat sheet, the predators Doru luteipes (Scudder, 1876) and Zelus longipes (L., 1767) were constant in DeltaOpal[R] only, while Chrysoperla sp. was constant in both Bt and nonBt cotton (Table I).
The faunistic analysis for the natural enemies is mainly correlated with the tritrophic interactions and the direct and indirect effects of Bt toxin plants on the preys and hosts of these benefical insects (Shelton et al., 2002). Another point to be considered is the traits adopted in the transgenic varieties (Wan et al., 2002; Yang et al., 2005), like the application or not of insecticides with regard to the control level to the non-target herbivores of Bt plants (Degrande, 2004; Thomazoni et al., 2010), the use of selective insecticides, and the sampling method adopted correlated with the behavior and bioecology of the natural enemy, which can be influence the diversity of these insects (Men et al., 2003), as demonstrated in this study, in the beat sheet method for Orius sp., which was dominant in both NuOpal[R] and DeltaOpal[R] and was only dominant in DeltaOpal[R] with the whole plant sampling.
With regard to natural enemies diversity in both sampling methods, the Shannon-Wiener's index and also the mean number of natural enemies was not significantly different between cotton varieties using both sampling methods (Table II). The mean number of larvae and adults in the dominant genera and species of the predators C. sanguinea, Scymnus sp., Chrysoperla sp., Geocoris sp., Orius sp., Araneae and C. granais did not show significant differences between Bt and non-Bt cotton in any of the sampling methods (Table V).
The dominance of predator Chrysoperla sp. in Bt cotton with both sampling methods, may indicate that this insect possibly did not suffer a negative impact from the Bt toxin present in the transgenic variety (Hilbeck et al., 2006). In contrast to our results, a small difference in Geocoris sp. population density between Bt and non-Bt cotton, both without chemical control application, was observed by Naranjo (2005). In the case of Orius sp. populations, the lack of chemical control application during the entire development cycle of both varieties can influence predator abundance, and influenced this genus, which was abundant in both Bt and nonBt cotton. This result was confirmed by the measure of the mean number of individuals of Orius sp., and the same result was observed with Araneae in both sampling methods. But other studies have shown a higher mean number of these predators in Bt cotton than in non Bt cotton (Wan et al., 2002; Hagerty et al., 2005).
The similarity in the mean number of individuals of the Chrysopidae family between Bt and non-Bt cotton was also observed in Australia (Whitehouse et al., 2005), and the presence of individuals of this family was also observed in Bt cotton (Sisterson et al., 2004). However, Hagerty et al. (2005) found that chrysopid populations belonging to the Chrysopidae and Hemerobiidae families were more abundant in Bollgard[R] cotton when compared with non-Bt cotton, showing a negative effect of Bt cotton on the diversity of these natural enemies.
A lack of significant difference in the mean number of sampled Coccinellidae was also observed in China (Yang et al., 2005). However, in other countries (Hagerty et al., 2005; Hofs et al., 2005) differences in the mean number of specimens from this family of predators have been observed. Such difference in results can be attributed to the number of prey sampled between Bt and nonBt cotton, whose development was favored by the lack of action of insecticides (Marvier et al., 2007) that are otherwise commonly applied for their control, showing the importance of integrating pest management tactics (Romeis et al., 2006, 2008), in this case, Bt cotton and biological control.
This biodiversity study was conducted to better understand the biology and ecology of the predator/pest interactions in Bt and non-Bt cotton varieties without application of insecticides, in a savannah agroeco-system in Brazil, being relevant because the arthropods play an important part in the structure and operation of the ecosystems and the maintenance of the biological diversity (Tscharntke and Clough, 2007; Scherr and McNeely, 2008; Sarvjeet, 2012). With the crescent introduction of the Bt cotton varieties in Brazil, it is crucial to quantify the diversity of insect communities present in Bt and non-Bt cotton plots and to determine how these communities are influenced by environmental changes provoked by natural causes or by human activity, like agronomic practices such a insecticide control for non-herbivores insects, and how these affect the biodiversity by tritrophic interactions that can contribute with the reduction of target pests, as natural enemies are the main cause of insect mortality in agroecosystems (Parra, 2000; Peixoto et al., 2007). In this way, this research can show how to integrate natural control with the transgenic plants, promoting the conservation of the beneficial insects, using the different monitoring sampling and diversity indexes.
NuOpal[R] (CrylAc) is efficient in the control of target species (P. gossypiella, H. virescens and A. argillacea) under cultivation conditions of the Brazilian Cerrado biome (savannah) without insecticide sprays.
The whole plant sampling method, as detected by the diversity indexes, has a higher diversity of the non-target herbivores A. granais and E. meditabunda in Bt cotton (CrylAc).
The natural enemies diversity on the non-sprayed Bt cotton (CrylAc) shows tritrophic interactions, and the conservation potential and benefits on that agroecossystem.
Moreover, this research demonstrated that the faunistic analysis and the diversity index of Shannon-Wiener can be used in studies of risk assessment of Bt varieties in non-target arthropod populations in Brazil.
The authors thank Sergio Vanin (Universidade de Sao Paulo) for identifying the chrysomelid Jansonius boggianii subaeneus, Rogerio Silvestre and Manoel Fernando Demetrio (Universidade Federal da Grande Dourados) for identifying the ants (Solenopsis invicta e Atta sp.), MDM-Sementes de Algodao[R] for the seeds of both varieties used in the experiment and CNPq for the grant awarded to the first author.
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Received: 25/09/2012. Modified: 09/12/2013. Accepted: 12/12/2013.
Danielle Thomazoni. Biologist and Ph.D. in Sciences (Entomology), Universidade Federal de Grande Dourados (UFGD), Brazil. Research Entomologist, Instituto Mato-grossense do Algodao (IMAmt), Brazil. Address: Rodovia BR 070 Km 265, Campo Experimental, Zona Rural, Primavera do Leste, MT, Brazil. 78850-000. e-mail: daniellethomazoni@ imamt.com.br
Miguel Ferreira Soria. Agronomist and Ph.D. in Vegetal Production, UFGD, Brazil. Research Entomologist, IMAmt, Brazil.
Paulo Eduardo Degrande. Agronomist and Ph.D. in Sciences (Zoology), Universidade de Sao Paulo, Brazil. Professor, UFGD, Brazil.
Odival Faccenda. Mathematician and Ph.D. in Agronomy (Energy in Agriculture), Universidade Estadual Paulista Julio de Mesquita Filho, Brazil. Professor, Universidade Estadual de Mato Grosso do Sul, Brazil.
Pierre Jean Silvie. Biologist and Ph.D. in Entomology, Centre de Cooperation Internationale en Recherche Agronomique Pour le Development (ORAD), France. Research Entomologist, CIRAD, Montpellier, France.
TABLE I FAUNISTIC ANALYSIS OF GROUPS OF TARGET PESTS, NON-TARGET PESTS, AND NATURAL ENEMIES BY ORDER, FAMILY, AND SPECIES, SAMPLING METHOD, AND TYPE OF COTTON Group Order/Family Species Stage (1) Target Lepidoptera/ Alabama SC+LC pests Noctuidae argillacea Lepidoptera/ Heliothis SC+LC Noctuidae virescens Lepidoptera/ Pectinophora Cat Gelechiidae gossypiella Total Non-target Coleoptera/ Cerotoma Ad pests Chrysomelidae arcuata Coleoptera/ Chrysomelidae Ad Chrysomelidae sp.l Coleoptera/ Diabrotica Ad Chrysomelidae speciosa Coleoptera/ Jansonius Ad Chrysomelidae boggianii subaeneus Coleoptera/ Maecolaspis Ad Chrysomelidae sp. Coleoptera/ Megascelis sp. Ad Cicindellidae Coleoptera/ Anthonomus L+Ad Curculionidae granais Coleoptera/ Lagria villosa Ad Lagriidae Coleoptera/ Astylus Ad Melyridae variegatus Hem iptera/A Bemisia tabaci Ad leyroidade Hemiptera/ Neomegalotomus Ad Alydidae parvus Hemiptera/ Agallia Ad Cicadellidae albidula Hemiptera/ Hypselonotus Ad Coreidae sp. Hemiptera/ Oxycarenus sp. Ad Lygaeidae Hemiptera/ Horciasinus Ad Miridae signoreti Hemiptera/ Horcias Ad Miridae nobilellus Hemiptera/ Chinavia spp. N+Ad Pentatomidae Hemiptera/ Edessa N+Ad Pentatomidae meditabunda Hemiptera/ Euschistus N+Ad Pentatomidae heros Hemiptera/ Nezara N+Ad Pentatomidae viridula Hemiptera/ Piezodorus N+Ad Pentatomidae guildini Hemiptera/ Dysdercus sp. N+Ad Pyrrhocoridae Lepidoptera/ Spodoptera SC+LC Noctuidae eridania Lepidoptera/ Spodoptera SC+LC Noctuidae frugiperda Lepidoptera/ Pseudoplusia SC+LC Noctuidae indudes Orthoptera/ Gryllus sp. Ad Gryllidae Orthoptera/ Tettigoniidae Ad Tettigoniidae sp.l Thysanoptera/ Frankliniella Ad Thripidae sp. Total Natural Araneae Araneae Ad enemies Coleoptera/ Callida sp. Ad Carabidae Coleoptera/ Lebia concinna Ad Carabidae Coleoptera/ Cycloneda L+Ad Coccinellidae sanguinea Coleoptera/ Eriopsis L+Ad Coccinellidae connexa Coleoptera/ Hyperaspis Ad Coccinellidae festiva Coleoptera/ Olla v-nigrum Ad Coccinellidae Coleoptera/ Scymnus sp. L+Ad Coccinellidae Dermaptera/ Doru luteipes Ad Forficulidae Diptera/ Condylostylus Ad Dolichopodidae sp. Diptera/ Toxomerus sp. L+Ad Syrphidae Hemiptera/ Orius sp. Ad Anthocoridae Hemiptera/ Geocoris sp. Ad Lygaeidae Hemiptera/ Nabis sp. Ad Nabidae Hemiptera/ Podisus sp. N+Ad Pentatomidae Hemiptera/ Repipta sp. Ad Reduviidae Hemiptera/ Zelus Ad Reduviidae armillatus Hemiptera/ Zelus longipes Ad Reduviidae Hymenoptera/ Solenopsis Ad Formicidae invicta Hymenoptera/ Catolaccus L Pteromalidae grandis Mantodea/ Mantidae sp.l Ad Mantidae Neuroptera/ Chrysoperla L Chrysopidae sp. Neuroptera/ Nusulala sp. L Hemerobiidea Neuroptera/ Mantispidae Ad Mantispidae sp.l Total Grand total Sampling method Whole plant Group Order/Family Species NuOpal[R] DeltaOpal[R] FC(A)D (2) FC(A)D (2) Target Lepidoptera/ Alabama 9 yn 55 w(c)s pests Noctuidae argillacea Lepidoptera/ Heliothis 0 1 z(c)n Noctuidae virescens Lepidoptera/ Pectinophora 0 39 y(c)s Gelechiidae gossypiella Total 9 95 Non-target Coleoptera/ Cerotoma 5 z(d)n 2 z(d)n pests Chrysomelidae arcuata Coleoptera/ Chrysomelidae 2 z(d)n 2 z(d)n Chrysomelidae sp.l Coleoptera/ Diabrotica 52 w(c)n 45 w(c)n Chrysomelidae speciosa Coleoptera/ Jansonius 37 w(c)n 38 w(c)n Chrysomelidae boggianii subaeneus Coleoptera/ Maecolaspis 19 y(d)n 10 y(d)n Chrysomelidae sp. Coleoptera/ Megascelis sp. 1 z(d)n 2 z(d)n Cicindellidae Coleoptera/ Anthonomus 235 y(ma)s 154 y(c)s Curculionidae granais Coleoptera/ Lagria villosa 2 z(d)n 3 z(d)n Lagriidae Coleoptera/ Astylus 26 y(c)n 10 z(d)n Melyridae variegatus Hem iptera/A Bemisia tabaci 903 w(ma)s 856 w(ma)s leyroidade Hemiptera/ Neomegalotomus 0 3 z(d)n Alydidae parvus Hemiptera/ Agallia 315 w(ma)s 261 w(ma)s Cicadellidae albidula Hemiptera/ Hypselonotus 0 0 Coreidae sp. Hemiptera/ Oxycarenus sp. 5 z(d)n 2 z(d)n Lygaeidae Hemiptera/ Horciasinus 1 z(d)n 1 z(d)n Miridae signoreti Hemiptera/ Horcias 611 w(ma)s 549 w(ma)s Miridae nobilellus Hemiptera/ Chinavia spp. 5 z(d)n 2 z(d)n Pentatomidae Hemiptera/ Edessa 129 w(c)s 74 w(c)n Pentatomidae meditabunda Hemiptera/ Euschistus 114 w(c)s 93 w(c)s Pentatomidae heros Hemiptera/ Nezara 63 w(c)n 61 w(c)n Pentatomidae viridula Hemiptera/ Piezodorus 38 w(c)n 17 w(c)n Pentatomidae guildini Hemiptera/ Dysdercus sp. 217 w(a)s 219 w(ma)s Pyrrhocoridae Lepidoptera/ Spodoptera 5 z(d)n 9 y(d)n Noctuidae eridania Lepidoptera/ Spodoptera 4 y(d)n 6 y(d)n Noctuidae frugiperda Lepidoptera/ Pseudoplusia 4 y(d)n 13 y(d)n Noctuidae indudes Orthoptera/ Gryllus sp. 3 z(d)n 4 z(d)n Gryllidae Orthoptera/ Tettigoniidae 0 1 z(d)n Tettigoniidae sp.l Thysanoptera/ Frankliniella 50 w(c)n 43 w(c)n Thripidae sp. Total 2846 2480 Natural Araneae Araneae 152 w(va)s 185 w(va)s enemies Coleoptera/ Callida sp. 13 z(c)n 16 z(c)n Carabidae Coleoptera/ Lebia concinna 3 z(d)n 5 z(d)n Carabidae Coleoptera/ Cycloneda 74 w(va)s 74 w(va)s Coccinellidae sanguinea Coleoptera/ Eriopsis 4 z(d)n 5 z(d)n Coccinellidae connexa Coleoptera/ Hyperaspis 9 z(c)n 7 y(d)n Coccinellidae festiva Coleoptera/ Olla v-nigrum 3 z(d)n 5 z(d)n Coccinellidae Coleoptera/ Scymnus sp. 191 w(va)s 174 w(va)s Coccinellidae Dermaptera/ Doru luteipes 7 y(c)n 12 y(c)n Forficulidae Diptera/ Condylostylus 1 z(d)n 1 z(d)n Dolichopodidae sp. Diptera/ Toxomerus sp. 7 y(c)n 8 y(d)n Syrphidae Hemiptera/ Orius sp. 27 y(c)n 45 y(c)s Anthocoridae Hemiptera/ Geocoris sp. 42 w(c)s 53 w(c)s Lygaeidae Hemiptera/ Nabis sp. 2 z(d)n 0 Nabidae Hemiptera/ Podisus sp. 2 z(d)n 3 z(d)n Pentatomidae Hemiptera/ Repipta sp. 1 z(d)n 2 z(d)n Reduviidae Hemiptera/ Zelus 1 z(d)n 3 z(d)n Reduviidae armillatus Hemiptera/ Zelus longipes 12 y(c)n 10 y(c)n Reduviidae Hymenoptera/ Solenopsis 25 y(c)n 17 y(c)n Formicidae invicta Hymenoptera/ Catolaccus 45 z(c)s 39 z(c)s Pteromalidae grandis Mantodea/ Mantidae sp.l 2 z(d)n 1 z(d)n Mantidae Neuroptera/ Chrysoperla 28 y(c)s 21 y(c)n Chrysopidae sp. Neuroptera/ Nusulala sp. 2 z(d)n 8 y(d)n Hemerobiidea Neuroptera/ Mantispidae 1 z(d)n 0 Mantispidae sp.l Total 654 694 Grand total 3509 3269 Sampling method Beat sheet Group Order/Family Species NuOpal[R] DeltaOpal[R] FC(A)D2 FC(A)D (2) Target Lepidoptera/ Alabama 0 31y(c)s pests Noctuidae argillacea Lepidoptera/ Heliothis 0 lz(c)n Noctuidae virescens Lepidoptera/ Pectinophora 0 35y(c)s Gelechiidae gossypiella Total 0 67 Non-target Coleoptera/ Cerotoma 0 0 pests Chrysomelidae arcuata Coleoptera/ Chrysomelidae 0 1 z(d)n Chrysomelidae sp.l Coleoptera/ Diabrotica 35 w(c)s 26 w(c)n Chrysomelidae speciosa Coleoptera/ Jansonius 13 y(c)n 21 y(c)n Chrysomelidae boggianii subaeneus Coleoptera/ Maecolaspis 0 0 Chrysomelidae sp. Coleoptera/ Megascelis sp. 0 1 z(d)n Cicindellidae Coleoptera/ Anthonomus 47 w(a)s 45 w(c)s Curculionidae granais Coleoptera/ Lagria villosa 8 w(d)n 8 y(d)n Lagriidae Coleoptera/ Astylus 19 w(c)n 13 y(c)n Melyridae variegatus Hemiptera/A Bemisia tabaci 0 0 leyroidade Hemiptera/ Neomegalotomus 1 w(r)n 1 z(d)n Alydidae parvus Hemiptera/ Agallia 11 w(c)n 12 z(c)n Cicadellidae albidula Hemiptera/ Hypselonotus 1 z(r)n 0 Coreidae sp. Hemiptera/ Oxycarenus sp. 3 y(r)n 2 y(d)n Lygaeidae Hemiptera/ Horciasinus 7 y(d)n 7 y(d)n Miridae signoreti Hemiptera/ Horcias 142w(ma)s 150 w(ma)s Miridae nobilellus Hemiptera/ Chinavia spp. 6 y(d)n 2 y(d)n Pentatomidae Hemiptera/ Edessa 61 w(ma)s 75 w(ma)s Pentatomidae meditabunda Hemiptera/ Euschistus 40 w(c)s 31 w(c)s Pentatomidae heros Hemiptera/ Nezara 40 w(c)s 31 w(c)s Pentatomidae viridula Hemiptera/ Piezodorus 6 w(d)n 6 y(d)n Pentatomidae guildini Hemiptera/ Dysdercus sp. 99 w(ma)s 165 w(ma)s Pyrrhocoridae Lepidoptera/ Spodoptera 9 w(d)n 11 y(c)n Noctuidae eridania Lepidoptera/ Spodoptera 0 4 z(d)n Noctuidae frugiperda Lepidoptera/ Pseudoplusia 7 w(d)n 12 w(c)n Noctuidae indudes Orthoptera/ Gryllus sp. 0 1 z(d)n Gryllidae Orthoptera/ Tettigoniidae 2 y(r)n 0 Tettigoniidae sp.l Thysanoptera/ Frankliniella 0 0 Thripidae sp. Total 557 625 Natural Araneae Araneae 58 w(va)s 72 w(va)s enemies Coleoptera/ Callida sp. 1 z(d)n 1 z(r)n Carabidae Coleoptera/ Lebia concinna 1 z(d)n 2 y(r)n Carabidae Coleoptera/ Cycloneda 44 w(va)s 44 w(va)s Coccinellidae sanguinea Coleoptera/ Eriopsis 0 0 Coccinellidae connexa Coleoptera/ Hyperaspis 1 z(d)n 0 Coccinellidae festiva Coleoptera/ Olla v-nigrum 2 z(d)n 1 z(r)n Coccinellidae Coleoptera/ Scymnus sp. 92 w(va)s 82 w(va)s Coccinellidae Dermaptera/ Doru luteipes 4 y(d)n 7 w(d)n Forficulidae Diptera/ Condylostylus 0 0 Dolichopodidae sp. Diptera/ Toxomerus sp. 1 z(d)n 0 Syrphidae Hemiptera/ Orius sp. 23 y(c)s 41 y(a)s Anthocoridae Hemiptera/ Geocoris sp. 20 w(c)s 28 w(c)s Lygaeidae Hemiptera/ Nabis sp. 1 z(d)n 0 Nabidae Hemiptera/ Podisus sp. 3 y(d)n 5 y(d)n Pentatomidae Hemiptera/ Repipta sp. 0 0 Reduviidae Hemiptera/ Zelus 0 0 Reduviidae armillatus Hemiptera/ Zelus longipes 3 y(d)n 6 w(d)n Reduviidae Hymenoptera/ Solenopsis 1 z(d)n 1 z(r)n Formicidae invicta Hymenoptera/ Catolaccus 45 z(va)s 39 z(a)s Pteromalidae grandis Mantodea/ Mantidae sp.l 0 1 z(r)n Mantidae Neuroptera/ Chrysoperla 26 w(c)s 20 w(c)n Chrysopidae sp. Neuroptera/ Nusulala sp. 2 y(d)n 5 y(d)n Hemerobiidea Neuroptera/ Mantispidae 0 0 Mantispidae sp.l Total 328 355 Grand total 885 1047 (1) SC: small caterpillar, LC: large caterpillar, Cat: caterpillar, L: larva, N: nymph, Ad: adult. (2) F: total number observed in different sampling conditions; C (constancy): w: constant, y: accessory, z: accidental; A (abundance): va: very abundant, a: abundant, c: common, d: dispersed, r: rare; D (dominance): s: dominant, n: non-dominant. TABLE II SHANNON-WIENER'S DIVERSITY INDEX, (VARIANCE), AND NUMBER OF NON-TARGET PEST SPECIES AND NATURAL ENEMIES PRESENT IN THE BT- AND NON-BT COTTON ENVIRONMENTS Bt cotton (1) Non-Bt cotton (1) Whole plant (n=272) (n=272) t-Student P Non-target 2.11(0.004)(25) a 2.04(0.005)(27) b 1.98 0.047 pests Natural 2.17(0.002X24) 2.21(0.001)(22) -0.558 0.576 enemies Bt cotton (1) Non-Bt cotton (1) Beat sheet (n=128) (n=128) t-Student P Non-target 2.32(0.001)(20) 2.23(0.001)(22) 1.643 0.100 pests Natural 2.04(0.002)(18) 2.12(0.002)(16) -1.053 0.292 enemies (1) Different letters in a row represent non-significant values at 5%, assuming equal variances by Levene's test. TABLE III MEAN NUMBER OF ARTHROPOD SPECIMENS (SD) PER TYPE OF COTTON AND SAMPLING METHOD Bt cotton (1) Non-Bt cotton (1) t-Student P Whole plant (n=272) (n=272) (2) Target pests 0.03 (0.19) a 0.35 (0.76) (b) 7.029 (3) 0.000 Non-target pests 10.45 (6.94) a 9.11 (6.68) (b) 2.626 0.009 Natural enemies 2.36 (2.67) 2.50 (2.78) 0.817 0.414 Bt cotton (1) Non-Bt cotton (1) t-Student P Beat sheet (n=128) (n=128) (2) Target pests 0.00 (0.00) a 0.52 (0.96) (b) 6.777 (3) 0.000 Non-target pests 4.35 (3.09) 4.87 (4.28) 0.498 (3) 0.619 Natural enemies 2.50 (2.38) 2.71 (2.21) 1.209 0.228 (1) Different letters in a row represent non-significant values at 5%, assuming equal variances by Levene's test. (2) Original data transformed to [square root of X+0.5] for statistical analysis purposes. (3) Different variances. TABLE IV MEAN NUMBER (SD) OF INDIVIDUALS FROM DOMINANT NON-TARGET PEST SPECIES PER TYPE OF COTTON AND SAMPLING METHOD Bt-cotton (3) Non-Bt cotton (3) Whole plant Stage 2 (n=272) (n=272) Horciasoides nobilellus Ad 2.25 (3.28) 2.02 (3.29) Anthonomus grandis Ad 0.86 (1.62) a 0.57 (1.19) b Agallia albidula Ad 1.16 (1.47) 0.96 (1.33) Nezara viridula N 0.06 (0.25) 0.03 (0.17) Nezara viridula Ad 0.17 (0.59) 0.19 (0.56) Euschistus heros N 0.04 (0.23) 0.03 (0.19) Euschistus heros Ad 0.38 (0.84) 0.31 (0.95) Edessa meditabunda N 0.04 (0.38) 0.03 (0.20) Edessa meditabunda Ad 0.43 (1.08) a 0.24 (0.73) b Dysdercus sp. N 0.06 (0.27) 0.07 (0.38) Dysdercus sp. Ad 0.74 (1.41) 0.73 (1.33) Diabrotica speciosa Ad 0.19 (0.47) 0.17 (0.45) Whole plant t-Student (1) P Horciasoides nobilellus 0.848 0.397 Anthonomus grandis 2.267 0.024 Agallia albidula 1.703 0.089 Nezara viridula 1.345 0.179 Nezara viridula 0.594 0.553 Euschistus heros 0.787 0.431 Euschistus heros 1.017 0.309 Edessa meditabunda 0.319 0.750 Edessa meditabunda 2.451 0.015 Dysdercus sp. 0.316 0.752 Dysdercus sp. 0.121 0.903 Diabrotica speciosa 0.679 0.498 Bt-cotton (3) Non-Bt cotton (3) Beat sheet Stage 2 (n=128) (n=128) Horciasoides nobilellus Ad 1.11 (1.43) 1.17 (1.52) Anthonomus grandis Ad 0.37 (0.79) 0.35 (0.78) Agallia albidula Ad 0.09 (0.28) 0.09 (0.50) Nezara viridula N 0.08 (0.29) 0.06 (0.27) Nezara viridula Ad 0.23 (0.55) 0.18 (0.46) Euschistus heros N 0.00 (0.00) 0.02 (0.12) Euschistus heros Ad 0.31 (0.64) 0.23 (0.53) Edessa meditabunda N 0.01 (0.08) 0.00 (0.00) Edessa meditabunda Ad 0.47 (1.37) 0.59 (1.97) Dysdercus sp. N 0.02 (0.15) 0.06 (0.62) Dysdercus sp. Ad 0.75 (1.23) 1.23 (2.03) Diabrotica speciosa Ad 0.27 (0.64) 0.20 (0.49) Beat sheet t-Student (1) P Horciasoides nobilellus 0.250 0.803 Anthonomus grandis 0.209 0.834 Agallia albidula 0.219 0.827 Nezara viridula 0.463 0.644 Nezara viridula 0.812 0.418 Euschistus heros 1.420 0.157 Euschistus heros 1.111 0.268 Edessa meditabunda 1.000 0.318 Edessa meditabunda 0.241 0.810 Dysdercus sp. 0.438 0.662 Dysdercus sp. 1.821 0.070 Diabrotica speciosa 0.859 0.391 (1) Original data transformed to [square root of X+0.5] for statistical analysis purposes. (2) N: nymph, Ad: adult. (3) Different letters in a row represent non-significant values at 5%, assuming equal variances by Levene's test. TABLE V MEAN NUMBER OF SPECIMENS (SD) OF INDIVIDUALS FROM DOMINANT NATURAL ENEMY SPECIES PER TYPE OF COTTON AND SAMPLING METHOD Bt-cotton Non-Bt cotton Whole plant Stage (2) (n=272) (n=272) Cycloneda sanguinea L 0.20 (0.58) 0.21 (0.82) Cycloneda sanguinea Ad 0.07 (0.31) 0.07 (0.29) Scymnus sp. L 0.56 (1.29) 0.46 (1.15) Scymnus sp. Ad 0.15 (0.41) 0.18 (0.58) Chrysoperla sp. L 0.10 (0.51) 0.08 (0.28) Geocoris sp. Ad 0.15 (0.44) 0.19 (0.53) Orius sp. Ad 0.10 (0.45) 0.17 (0.62) Araneae Ad 0.56 (0.93) 0.68 (1.00) Catolaccus grandis L 0.14 (0.62) 0.12 (0.64) Whole plant t-Student (1) P Cycloneda sanguinea 0.231 0.817 Cycloneda sanguinea 0.235 0.815 Scymnus sp. 0.771 0.441 Scymnus sp. 0.425 0.671 Chrysoperla sp. 0.332 0.740 Geocoris sp. 0.951 0.342 Orius sp. 1.326 0.185 Araneae 1.629 0.104 Catolaccus grandis 0.533 0.594 Bt-cotton Non-Bt cotton Beat sheet Stage (2) (n=128) (n=128) Cycloneda sanguinea L 0.27 (0.70) 0.27 (1.09) Cycloneda sanguinea Ad 0.07 (0.31) 0.08 (0.26) Scymnus sp. L 0.61 (1.13) 0.56 (0.91) Scymnus sp. Ad 0.11 (0.36) 0.08 (0.26) Chrysoperla sp. L 0.20 (0.71) 0.16 (0.38) Geocoris sp. Ad 0.16 (0.40) 0.22 (0.46) Orius sp. Ad 0.18 (0.63) 0.32 (0.84) Araneae Ad 0.45 (0.85) 0.56 (0.81) Catolaccus grandis L 0.29 (0.88) 0.25 (0.93) Beat sheet t-Student (1) P Cycloneda sanguinea 0.577 0.564 Cycloneda sanguinea 0.367 0.714 Scymnus sp. 0.063 0.950 Scymnus sp. 0.694 0.489 Chrysoperla sp. 0.258 0.797 Geocoris sp. 1.160 0.247 Orius sp. 1.518 0.130 Araneae 1.343 0.180 Catolaccus grandis 0.546 0.585 (1) Original data transformed to [square root of X+0.5] for statistical analysis purposes. (2) L: larva, Ad: adult.
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|Author:||Thomazoni, Danielle; Soria, Miguel Ferreira; Degrande, Paulo Eduardo; Faccenda, Odival; Silvie, Pier|
|Date:||Dec 1, 2013|
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