African Journal of
Agricultural Research

  • Abbreviation: Afr. J. Agric. Res.
  • Language: English
  • ISSN: 1991-637X
  • DOI: 10.5897/AJAR
  • Start Year: 2006
  • Published Articles: 6712

Full Length Research Paper

Diversity of insects in conventional and organic tomato crops (Solanum lycopersicum L., solanaceae)

Rubens Pessoa de Barros
  • Rubens Pessoa de Barros
  • Department of Biological Sciences, State University of Alagoas, Brazil.
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Ligia Sampaio Reis
  • Ligia Sampaio Reis
  • Center for Agricultural Sciences, Federal University of Alagoas, Brazil.
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Isabelle Cristina Santos Magalhaes
  • Isabelle Cristina Santos Magalhaes
  • Department of Biological Sciences, State University of Alagoas, Brazil.
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Miriany de Oliveira Pereira
  • Miriany de Oliveira Pereira
  • Department of Biological Sciences, State University of Alagoas, Brazil.
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Ana Cleia Barbosa de Lira
  • Ana Cleia Barbosa de Lira
  • Department of Biological Sciences, State University of Alagoas, Brazil.
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Claudio Galdino da Silva
  • Claudio Galdino da Silva
  • Department of Biological Sciences, State University of Alagoas, Brazil.
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Jaciara Maria Pereira e Silva
  • Jaciara Maria Pereira e Silva
  • Department of Biological Sciences, State University of Alagoas, Brazil.
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João Gomes da Costa
  • João Gomes da Costa
  • Rio Largo Research Unit Technical-Scientific Area, EMBRAPA - Rio Largo-AL, Brazil.
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Elio Cesar Guzzo
  • Elio Cesar Guzzo
  • Rio Largo Research Unit Technical-Scientific Area, EMBRAPA - Rio Largo-AL, Brazil.
  • Google Scholar


  •  Received: 20 January 2018
  •  Accepted: 07 February 2018
  •  Published: 08 March 2018

 ABSTRACT

This study aims to compare the diversity and relative abundance of insect families collected in organic and conventional tomato production systems located in Alagoas, Northeast Brazil (09°81'76"S and 36°59'42"W). In this region, the visible spectrum is quite broad with sunlight throughout the year. Between rows of tomato plants, we set up a system of colored traps colored blue, yellow, white, green, red, and transparent. The experiment was between September 2015 and January 2017. The experimental design was completely randomized with six experiments and with five replicates. The data collected were analyzed using the Scott-Knott test at 5% probability. Analysis of the various diversity indices was made using DivEs software. A total of 56,955 insects from 25 families were collected from the organic system, and 10,660 from 22 families in the conventional system. We observed that, in the conventional system, insect diversity and relative abundance (AR) were significantly greater than those of the organic system. The averages of the indices were as follows: For the organic system: Shannon-Wiener, 2.97; Simpson, 0.79; Simpson Dominance, 0.19; Margalef, 5.13; and Pielou, 2.27, respectively. For the conventional system, the indices were 3.49; 0.86; 0.12; 6.93; and 2.56; respectively. Several families of insect orders collected in the colored traps showed significant mean values for families of pollinator insects, predators, parasitoids, and pests. This may aid in decision making for the protection of plants and other agroecosystems. The collected insects did not differ significantly in terms of diversity of families. Colored traps may be exploited for pest control and for conservation of insect.
 
Key words: Vegetables, agricultural management, agroecology, plant protection.


 INTRODUCTION

Tomato is very important in Brazil, being the second most important vegetable crop. However, disease and pest infestation in crop have caused significant damage to tomato production. These insects’ damages generate morphological and physiological derangements in the tomato, causing them to ripen irregularly (Santos et al., 2008b). Environmental variation contributes diversity of species in natural ecosystems and in agroecosystems, where farm managers follow procedures aimed at causing the least impact to the environment. This applies regardless of whether the system is conventional or organic (Alencar et al., 2013). When the agroecosystem is managed with chemicals and the control of insects is done by insecticides, the diversity is damaged. Unlike the organic system, the diversity is represented by several families of insects (Letourneau and Goldstein, 2001). Plants protect themselves through the visible portion of the electromagnetic spectrum because colors motivate insects to search for food, locate mating sites, lay eggs, and pollinate (Skorupski and Chittka, 2010; Wanga et al., 2013). Paula et al. (2015) point out that colored traps may provide a potential alternative for insect control and integrated pest management. It may be possible to use such a system to monitor fluctuations in insect species and richness.
 
Vrdoljak and Samways (2012) argue that yellow color, compared with other colors, leads to a higher number of insects captured, with yellow traps catching insects from various groups in several growing areas and natural systems. Campos (2008) showed that various trap colors attract insects in agricultural settings and forests.  Predator insects are important in the agricultural context because they feed on other insects and control their populations. Predators are abundant in agricultural environments that have adequate management for pest control (Harterreiten- Souza et al., 2011).  Therefore, it is necessary to know which groups of insects associated with the tomato crop are attracted by what colors, in order to define a strategy for the use of colored adhesive traps for the attraction and capture of insect pests, or only attraction of beneficial insects without catching them and eliminating them from the environment. We hypothesized that colored traps would reveal similar indices of insect diversity in conventional and organic production systems. The objective was to compare the diversity and richness indices of insect families collected in conventional and organic production systems for the tomato (Solanum lycopersicum L.), for the management of insects pests in crops.


 MATERIALS AND METHODS

Research area
 
The study was carried out in two commercial tomato growing farms, both in Alagoas, (09°81'76"S and 36°59'42’’W) in Northeast Brazil, with an altitude of 264 m. One farm was conventional and another was organic. The two agricultural areas cultivated several vegetables, in addition to tomato. The experiment was created 45 days after emergence (DAE) of the seedlings between September 2015 and January 2017. The conventional and organic systems had the same distribution of tomatoes, with single rows spaced 1.5 and 25 m long. Each plot occupied an area of 1.5 ha, with approximately 6,000 ft of tomato. Organic farming has natural product management and conventional management uses synthetic products. The planted varieties were TY-2006 and Santa Clara. In both areas, the soil was predominantly eutrophic yellow Red Latosol (Embrapa, 2009). The climate is Köppen type As', that is, tropical and warm, with minimum average temperatures of 23°C and maximum average temperature 32°C. Rainfall in autumn/winter is between 500 mm and 1,000 mm (Alagoas, 2017).
 
Trap set-up and monitoring
 
The traps were made from plastic bottles, type Polyethylene Terephthalate (PET) with capacity of 2.5 L. Eighteen bottles were painted blue, yellow, white, green, red, and unpainted (transparent), three bottles for each color. To monitor insects in each experimental area, the colored PET bottles were installed randomly, mounted with the mouth fitted onto a 1.2 m bamboo stalk, close to the height of tomato plants. We applied entomological glue over a 75.00 cm2 area of the bottle body (Fig. 1A, B, C, D, and F.). The traps were initially placed in the field as pre-test and positive results were obtained regarding the use and adaptation for experimental design (Figure 1).
 
 
 
 
Experimental design and statistical analysis
 
The experimental design was a randomized block with six treatments: PET0 - colorless, PET1 - yellow, PET2 - green, PET3 - red, PET4 - white, PET5 – blue. The experiment was carried out over four crop cycles. The traps were randomly arranged. For comparison purposes, insect data collected and identified at the family level were analyzed using analysis of variance - ANOVA and the Scott-Knott test at 5% probability using Assistat Software Version 7.7 (Silva and Azevedo, 2016).
 
Methodological procedures
 
The insects caught in the traps were counted and removed in the field with the aid of a clamp and organic solvent, every five days. Insects were placed in jars containing 70% alcohol and that were deposited in the Laboratory of Ecology and Biodiversity of the State University of Alagoas/Campus I, for screening and identification. Insect identification was carried out by stereoscopic binocular microscopy (Opton®) at 80x. Identifications were made with the aid of arthropod pictorial identification keys and with images from entomological taxonomies (Seltmann, 2004; Carrano-Moreira, 2015; Rafael et al., 2012).
 
Analysis of insect family diversity indices
 
 
For the analysis of diversity, the following indices were considered: diversity (Shannon-Wiener, Simpson), richness (Margalef), dominance (Simpson), and evenness (Pielou). These parameters were analyzed using DivEs software (Rodrigues, 2016). Relative abundance (AR) for insect families was described by the formula AR (%) = n / N x 100, where AR = abundance percentage, n = number of specimens of the order and family, and N = total number of specimens captured in each system (Soares et al., 2016).

 


 RESULTS AND DISCUSSION

During the period of the research (2015 to 2017), we collected 56,955 insects in the organic system and 10,660 in the conventional system. We considered for analysis only insects that are ≥ 1 were captured. The traps attracted 22 families to the conventional system and 25 in the organic system. Amaral et al. (2010) describe densely wooded areas with well-adapted insect diversity, some attracted by colors more than the others. The control of insects in agricultural systems with agroecological management, diversity is sustainable (Letourneau and Bothwell, 2008). Table 1 displays comparison data for the conventional system using the Scott-Knott test at 5% probability, for 22 families collected in the colored traps. The order Diptera was most prominent, with the Agromizidae and Tabanidae families being most collected in the blue and white traps. Santos et al. (2008a) reported that yellow most attracted the Agromizidae family. This order is second highest in terms of number of species, accounting for a very varied niche, including hematophagous insects, phytophagous insects, miners, predators, parasitoids, and pollinators (Azevedo et al., 2015). The Tabanidae family are dipterans of veterinary and medical interest.
 
 
 
Those that are ectoparasites of horses, prefer dark brown and reddish brown animals (Bassi et al., 2000; Mikuška et al., 2016). Santos et al. (2008b) points out that insects can be attracted by different colors. For example, Lyriomiza trifolii (Burgess, 1880) (Diptera: Agromyzidae) is attracted by yellow, and Thrips tabaci (Lindeman, 1889) (Thysanoptera: Thripidae) by blue. However, Vrdoljak and Samways (2012) highlight that yellow and black may be repellent to some families and attractive to others. The Apidae family, who is important for tomato pollination in the conventional system, comprised 46.66% of insects collected in the yellow traps. Barbosa et al. (2016) reported the presence of Apis mellifera (Linnaeus, 1758) and Trigona spinipes (Fabricius, 1793), of the Apidae family. Freitas et al. (2006) commented that bees of the genus Exomalopsis, Epicharis and Centris were good tomato pollinators. Nanotrigona pirilampoides (Cresson, 1878) (Hymenoptera: Apidae), use a mechanism involving wing vibration that results in cross-pollination of heavier fruits with more seeds (Cauich et al., 2004; Castro et al., 2006) (Table 1). Table 2 displays 25 insect families in the organic system by the Scott-Nott average comparison test, at 5% probability.
 
 
 

The number of insects was higher in the organic system than in the conventional system. As for the diversity of insect families, the organic system was slightly larger than the conventional system. Santos et al. (2008a) suggested that yellow attracted adults of Diabrotica speciosa (Germar, 1824), (Coleoptera: Chrysomelidae), Bemisia tabaci (Gennadius, 1889) (Hemiptera: Aleyrodidae), Liriomyza trifolii (Burgess, 1880) (Diptera: Agromyzidae), Myzus persicae (Sulzer, 1776), and Macrosiphum euphobiae (Thomas, 1878) (Hemiptera: Aphididae). The diversity of families and the number of insects can serve as bioindicators of diversified management, indicating polyculture areas where shrub and tree plants such as the neem (Azadirachta indica A. Juss.; Meliaceae) function as wind barriers. In addition, the growing area includes cashew (Anacardium occidentale L.; Anacardiaceae), guava (Psidium guajava L.; Myrtaceae), mango (Mangifera indica L.; Anacardiaceae), coconut (Cocos nucifera L.; Arecaceae), jocote (Spondias purpúrea L.; Anacardiaceae), mulberry (Morus nigra L.; Moraceae), acerola (Malpighia emarginata DC; Malpighiaceae), orange (Citrus sinensis L.; Rutaceae), lime (Citrus limon L.; Rutaceae), and various weeds. Cardozo (2007) reports that these trees, when maintained in the agroecosystem, serve to protect plants, both from pesticide drift from neighboring areas, and from the spores and/or invasive propagules.

 

The presence of pollinators, predators, and parasitoids in the area guarantees stability of the families of insects collected in the various colored traps. Campos (2008), in an open field study, listed 22 species of tomato pollinators distributed among the families Apidae, Halictidae and Andrenidae. Insects can be attracted to colors, by means of their long photoreceptor fibers (Skorupski and Chittka, 2010; Wanga et al., 2013). Albuquerque et al. (2006) highlight melitophilia as a common pollination among the various solanaceous species, it is particularly attracted by floral structure, as is the case of the tomato in this study (Del Sarto, 2005). To pollinate the tomato, the bee’s anthers need to vibrate in order to the release pollen. This fact reduces the number of effective pollinators, since such species as Trigona spinipes (Fabricius, 1793) (Hymenoptera: Apidae) cannot vibrate (Vianna et al., 2007). Santos and Nascimento (2011), in a study of diversity indices in organic crops, reported that the most abundant family was Apidae, representing 48.76% of the total sample (Table 2). Table 3 displays various ecological indices (Shannon-Wiener and Simpson for diversity, Simpson for dominance, Margalef for richness, and Pielou for evenness) with respect to the colors of the PET traps. The data show differences in terms of diversity and richness of the insect families, highlighting the indices for the conventional system. 

 

 
The collected insects were attracted by the colors in each visited habitat, and foraging occurred on the basis of this attraction. We found that yellow, blue, and white attracted more insects than did green, red, and colorless.  The diversity indices of the insects collected in the colored traps revealed a tendency of attraction for the colors. This study highlighted the α (alpha) diversity that is constituted in the number of species (richness) in homogeneous fragments of a particular habitat type (Whittaker et al., 2001; Tuomisto, 2010; Chi et al., 2014). For both systems, the Jaccard similarity index was 0.88. The Jaccard index varies between 0 for different communities regarding the composition of species and 1 in similar communities regarding species composition (Zanzini, 2005). In both systems, the Margalef indices were greater than 5.0, suggesting considerable families richness. Higher values of the Margalef index suggest proportional value for rare species. The Shannon-Wiener and Simpson indices were significantly different in each system. The Pielou index revealed a balance between the number of families in the two systems. According to Pielou (1966, 1975), values of the index vary between 0 for minimum uniformity, and 1 for maximum uniformity. In this study, the values were higher than 1.5.
 
Virginio et al. (2016) argue that the greater the knowledge regarding the fauna of an area, the more effective are the strategies for its conservation. This is especially true for northeastern ecosystems, where there is a shortage of studies. Wilsey et al. (2005) suggest that species richness is dependent on sample size. In the conventional system, there was greater dominance index compared with the organic system. However, the samples collected during the study showed a balance in terms of evenness index. We observed that the more homogeneous the number of individuals per species, the greater the evenness and uniformity.Following this reasoning, a given diversity index may indicate that community A is more diverse than B, while another index indicates the opposite (Mendes et al., 2008). Diversity is defined as a set of multivariate statistical procedures that inform various characteristics of the structure of biological communities (Ricotta, 2005).  According to Medeiros et al. (2011), it is essential to understand the interactions between insects and plants in order to understand biodiversity, since the resources provided by the plants are fundamental for the adaptive spread of the animals (Gaertner and Borba, 2014). Similarly, Ribeiro (2005) and Ferraz et al. (2009) emphasize that higher values of these indices suggest greater dominance and the lower diversity (Table 3).
 
Table 4 displays relative abundance - AR (%) of insect families and orders in both systems. The highest relative abundance of individuals collected in the traps were from the order diptera, 40.19% for the organic system and 37.45% for the conventional system. The Agromizydae family (AR = 24.92% organic) featured prominently, obtaining greater significance for yellow, blue, white, and red. Lima and Serra (2008) affirm that this order has a wide range of niches and diversity of families. Some families in Table 4 represent predatory insects, phytophagous, natural enemies, and pollinators in the agroecosystem. Even with the systematic application of insecticides three times a week, these insects acquire resistance and remain active. Moura et al. (2014) point out that the most common predators found are wasps, ants, the neuropteran Chrysoperla externa (Hagen, 1861) (Neuroptera: Chrysopidae), spiders and bedbugs of the Reduviidae, Pentatomidae and Nabidae families. According to Togni et al. (2010), this abundance and diversity of families is mainly due to the greater availability of spaces protected from intra-species predation and access to alternative food resources. The presence of the leafminer Liriomyza trifolii (Burgess, 1880) (Diptera: Agromizydae) in tomato crops suggests that integrated pest management requires greater attention, since this insect causes direct damage to the tomato leaf, reducing its productivity. Gusmão (2004) found abundant leafminer larvae in tomato leaves. In this study, we performed a random survey of ten plants and found two leafminer nests larvae on leaves of each tomato plant examined.
 
 
 

The order Coleoptera had an AR of 45.63% in the organic system and 13.95% in the conventional system. The Scarabaidae family had an AR of 32.05% in the organic system and 5.66% in the conventional system. Lima et al. (2013) studied diversified environments and found a significant number of this family. Matta et al. (2017) report predatory activity of the Carabidae family on weeds in cotton fields. The Carabidae family had and AR of 8.53% in the organic system and 0.41% in the conventional system. Al-Attal et al. (2003) found 36% of the total number of insects identified as specimens of this family, with diversified functions in the agroecosystem. According to Cividanes et al. (2003), specimens of the Carabidae family spread by walking or flying. In this niche, they contribute to the pollination and decomposition of particulate matter. The order Hymenoptera, generally abundant in vegetable environments, in the collections had an AR of 14.98% in the conventional system and 1.09% in the organic system. Alencar et al. (2007) and Kaminski et al. (2009) observed that this order has a diverse behavior in the agroecosystem. They are associated with specific ecological interactions as detritivores, predators, granivores, and herbivores. The Apidae family achieved an AR of 3.29% in the conventional system and 0.28% in the organic system. This is notable because these insects are important pollinators (Vianna et al., 2007).

 

The order Hemiptera had an AR of 19.78% in the organic system and 1.23% in the conventional system. The Cicadelidae family had a higher presence with an AR of 18.74% in the conventional system and 0.71% in the organic system. These are phytophagous insects, vectors of Xylella fastidiosa (Wells et al., 1987) (Table 4). Table 5 shows the significant results of the orders of insects collected in the colored traps. Seven orders of insects were attracted, including many of agricultural interest. The red traps attracted the orders Coleoptera and Lepidoptera, which are useful for plant pollination in both tomato growing systems. Paz and Pigozzo (2012) investigated mangrove, Atlantic Forest and Restinga, using traps with colored water. They report the most attractive colors to the insects were green, white, and blue. They show that Atlantic Forest was the environment with the greatest abundance of individuals and orders of insects, being a biome with a greater diversity of plants than other areas. The colors of the flowers and or plants serve as an attraction to insects, who visit in order to feed and lay eggs. In so doing, they pollinate as well.

 

 
In this niche, there are also predators and parasitoids (Skorupski and Chittka, 2010; Wanga et al., 2013). According to Vasconcellos et al. (2010), the seasonality in the Caatinga region favors the presence of the insect orders found. They found 20 orders belonging to the Insecta class, of which seven are found in the table collected in this study: Blattodea, Coleoptera, Diptera, Hemiptera, Hymenoptera, Lepidoptera, and Thysanoptera. The order Hymenoptera, with a mean of between 10.0 and 129.0 individuals in both systems, represents a good part of the collections as social insects, a result corroborated in Dutra and Machado (2001), Santos and Nascimento (2011), Souza (2011), and Rocha et al., 2010). In this study, the red trap was significantly superior to the others, attracting a greater number of insects of the order Coleoptera. We hypothesize that these insects are attracted to red, since electromagnetic waves have wavelength ≥ 700 nm (Table 5).
 
 


 CONCLUSION

The use of colored traps is an efficient strategy to know the diversity of insects of the agricultural environments, allowing an integrated pest management planning. The insect family diversity indexes collected were different in the colored traps for the two cropping systems.


 CONFLICT OF INTERESTS

The authors have not declared any conflict of interests.


 ACKNOWLEDGEMENTS

The authors want to thank: The University of Alagoas State – UNEAL, through the Undergraduate Program of Scientific Research Initiation - PIBIC.



 REFERENCES

Al-Attal YZ, Kasrawi MA, Nazer IK (2003). Influence of Pollination Technique on Greenhouse Tomato Production. Agric. Marine Sci. 8(1):21-26.

 

Alagoas (2017). Secretaria de Estado do Meio Ambiente e dos Recursos Hídricos – AL.Diretoria de Meteorologia. Boletim anual de dados climatológicos. 2017. Disponível em: 

View. Acesso em 23 abr. 2017.

 
 

Albuquerque LB, Velázquez A, Vasconcellos-Neto J (2006). Composição florística de solanaceae e suas síndromes de polinização e dispersão de sementes em florestas mesófilas neotropicais. Interciencia 31(011):807-816.

 
 

Alencar GV, Mendonça ES, Oliveira TS, Jucksch I, Cecon PR (2013). Percepção ambiental e uso do solo por agricultores de sistemas orgânicos e convencionais na Chapada da Ibiapaba, Ceará. Rev. de Econ. e Sociologia Rural 51(2):217-236.
Crossref

 
 

Alencar IDCC, Fraga FB, Tavares MT, Azevedo CO (2007). Perfil da fauna de vespas parasitóides (Insecta, Hymenoptera) em uma área de Mata Atlântica do Parque Estadual de Pedra Azul, Domingos Martins, Espírito Santo, Brasil. Arquivos do Instituto Biológico, São Paulo 74(2):111-114.

 
 

Amaral DS, Venzon M, Pallini A, Lima PC, Desouza O (2010). A diversificação da vegetação reduz o ataque do bicho-mineiro-do-cafeeiro Leucoptera coffeella (Guérin-Mèneville) (Lepidoptera: Lyonetiidae)? Neotrop. Entomol. 39(4):543-548.
Crossref

 
 

Azevedo FR, Azevedo RA, Santos CAM, Moura ES, Nere DR (2015). Análise Faunística e Flutuação Populacional da Dipterofauna de Ecossistemas da Área de Proteção Ambiental do Araripe, Barbalha, CE. EntomoBrasilis 8(2):117-124.
Crossref

 
 

Barbosa BC, Paschoalini M, Maciel TT, Prezoto F (2016). Visitantes florais e seus padrões temporais de atividade em flores de Dombeya wallichii (Lindl.) K. Schum (Malvaceae). Entomotropica 31(16):131-136.

 
 

Bassi RMA, Cunha MCI, Coscaron AS (2000). Study of behavior of tabanids (Diptera, Tabanidae) from Brazil. Acta Biol. Par., Curitiba 29 (1, 2, 3, 4):101-115.

 
 

Bustillo AE, Cárdenas R, POSADA FJ (2002). Natural Enemies and Competitors of Hypothenemus hampei (Ferrari) (Coleoptera: Scolytidae) in Colombia. Neotrop. Entomol. 31(4) :635-639.
Crossref

 
 

Campos MJ (2008). Landscape management and pollinator richness in tomato (Lycopersicon esculentum Mill., Solanaceae) crops in Southeastern Brazil. In: Pollinators Management in Brazil. MMA: Brasília 41p.

 
 

Carrano-Moreira AF (2015). Insetos: manual de coleta e identificação. 2ª ed. Rio de Janeiro: Technical Books 369p.

 
 

Cardozo AII (2007). Produção de pimentão com vibração das plantas. Ciênc. agrotec. Lavras 31(4):1061-1066.

 
 

Cárcamo MC, Brandão RK, Costa VA, Ribeiro PB (2009). Ocorrência de Aprostocetus hagenowii (Hymenoptera, Eulophidae), parasitoide de ootecas da barata americana, no Rio Grande do Sul. Ciência Rural 39(9):2649-2651.
Crossref

 
 

Castro MS, Koedam D, Contrera FAL, Venturieri GC, Nates-Parra G, Malagodi-Braga KS, Campos LO, Viana M, Cortopassi-Laurino M, Nogueira-Neto P, Peruquetti RC, Imperatriz-Fonseca VL (2006). Stingless bees. In: Imperatriz-Fonseca, V.L., Saraiva, A.M. & De Jong, D. Bees as pollinators in Brazil: assessing the status and suggesting best practices. Ribeirão Preto: Holos pp. 75-88.

 
 

Cauich O, Quezada-Euán JJG, Macias-Macias JO, Reyes-Oregel V, Medina-Peralta S, Parra-Tabla V (2004). Behavior and pollination efficiency of Nannotrigona perilampoides (Hymenoptera: Meliponini) on greenhouse tomatoes (Lycopersicon esculentum) in Subtropical Mexico. Hortic. Entomol. 97(2):475-481.

 
 

Cividanes FJ, Souza VP, Sakemi LK (2003). Composição faunística de insetos predadores em fragmento florestal e em área de hortaliças na região de Jaboticabal, Estado de São Paulo. Acta Scientiarum. Biological Sciences. Maringá 25(2):315-321.

 
 

Chi Chun-Huo, Lou JOST, Chao ANNE (2014). Phylogenetic beta diversity, similarity, and differentiation measures based on Hill numbers. Ecol. Monogr. 84(1):21-44.
Crossref

 
 

Cunha ASD, Nóbrega MAS, Antonialli Junior WF (2014). Insetos Polinizadores em Sistemas Agrícolas. Ensaios e Ciência: Ciênc. Biol. Agrár. Saúde 18(4):185-194.

 
 

Del Sarto MCL (2005). Avaliação de Melipona quadrifasciata Lepeletier (Hymenoptera: Apidae) como Polinizador da Cultura do Tomateiro

 
 

Dutra J, Machado VL (2001). Flowering entomofauna in Stenolobium stans (Juss.) Seem (Bignoniaceae). Neotrop. Entomol. 30(1):43-53.
Crossref

 
 

Embrapa (2009). Mapa exploratório do reconhecimento do solo em Arapiraca-AL. Disponível em:  

View Acesso em 17 mar. 2017.

 
 

Fernandes DRR, Bená DC, Lara RIR, IDE S, Perioto NW (2012). Nitidulidae (Coleoptera) associados a frutos do café. Coffee Sci. Lavras 7(2):135-138.

 
 

Ferraz ACP, Gadelha BQ, Aguiarcoelho VM (2009). Análise faunística de Calliphoridae (Diptera) da Reserva Biológica do Tinguá, Nova Iguaçu, Rio de Janeiro. Rev. Bras. de Entomologia, São Paulo 53(4):620-628.

 
 

Freitas BM, Martins CF, Schlindwein CP, Wittman D, Santos IA, Cane JH, Ribeiro MF, Gaglianone MC (2006). Bumble bees and Solitary bees. In: Imperatriz- Fonseca, V.L., Saraiva, A.M. & De Jong, D. Bees as pollinators in Brazil: assessing the status and suggesting best practices. Ribeirão Preto: Holos pp. 55-62.

 
 

Gaertner C, Borba RS (2014). Diferentes cores de armadilhas adesivas no monitoramento de pragas em alface hidropônica. Rev. Thema 11(01).

 
 

Gullan PJ, Cranston OS (2008). Os insetos: um resumo de entomologia. São Paulo: Rocca, 2008.

 
 

Gusmão MR (2004). Amostragem de Liriomyza trifolii (Burguess) (Diptera: Agromizydae) no Tomateiro. 2004. 83 f. (Tese de Doutorado). Tese de Doutorado apresentado à Universidade Federal de Viçosa – Programa de Pós-Graduação em Entomologia. Viçosa-MG.

 
 

Harterreiten-Souza ES, Pires CSS, Carneiro RGC, Sujii ER (2011). Predadores e Parasitoides: aliados do produtor rural no processo de transição agroecológica. Brasília, DF: Emater, Embrapa Recursos Genéticos e Biotecnologia, CNPq. 92p.

 
 

Kaminski LA, Sendoya SF, Freitas AVL, Oliveira P (2009). Ecologia comportamental na interface formiga-planta-herbívoro: interações entre formigas e lepidópteros. Oecologia Brasiliensis, 13(1):27-44.
Crossref

 
 

Letourneau DK, Goldstein B (2001). Pest damage and arthropod community structure in organic vs. conventional tomato production in California. J. Appl. Ecol. 38:557-570.
Crossref

 
 

Letourneau DK, Bothwell SG (2008). Comparison of organic and conventional farms: challenging ecologists to make biodiversity functional. Front Ecol. Environ. 6(8):430-438.
Crossref

 
 

Lima VP, Serra AL (2008). Análise morfológica comparada da venação de asas da ordem Diptera (Linnaeus, 1758- Arthropoda, Insecta). Conscientia e Saúde, São Paulo 7(4):525-533.
Crossref

 
 

Lima IMM (2002). Registro da ocorrência de Cybocephalus sp. (Coleoptera: Nitidulidae) predando espécies-praga de Diaspididae (Hemiptera), no estado de Alagoas. Neotrop. Entomol. 31(1):157-159.
Crossref

 
 

Lima MGA, Silva RPA, Sousa MDF, Costa EM (2013). Diversidade de Scarabaeinae (Coleoptera: Scarabaeidae) no Parque Botânico do Ceará, Caucaia - CE, Brasil. Revista [email protected] On-line 7(1):89-94.

 
 

Matta DH, Cividanes FJ, Silva RJ, Batista MN, Otuka AK, Correia ET, Matos STS (2017). Feeding habits of Carabidae (Coleoptera) associated with herbaceous plants and the phenology of coloured cotton. Acta Scientiarum. Agron. Maringá 39(2):135-142.

 
 

Medeiros MA, Harterreiten-Souza ES, Togni PHB, Milane PVGN, Pires CSS, Carneiro RG, Sujii ER (2011). Princípios e práticas ecológicas para o manejo de insetos praga na agricultura (livreto). Brasília: Emater-DF / Embrapa. 1:44.

 
 

Mendes RS, Evangelista LR, Thomaz SM, Agostinho AA, Gomes C (2008). A unified index to measure ecological diversity and species rarity. Ecography 31(4):450-456.
Crossref

 
 

Mikuška A, Mlinarić S, Begović L, Curran E (2016). Comparative efficiency of traps for horse fly (Diptera: Tabanidae) survey in riparian oak-ash forests in Danube floodplain. Eur. J. Entomol. 113:531–536.
Crossref

 
 

Moura AP, Michereff Filho M, Guimarães JA, Liz RS (2014). Manejo integrado de pragas do tomateiro para processamento industrial. EMBRAPA – Circular Técnica –nº 129, Fevereiro.

 
 

Noubissié JBT, Yadji HT, Baldena I (2012). Screening Sorghum Populations for Resistance to Striga hermonthica (Del.) Benth in Northern Cameroon. Ann. Biol. Res. 3(5):2357-2364.

 
 

Parra JRP, Botelho PSM, Correa-Ferreira BS, Bento JMS (2002). Controle biológico no Brasil: parasitóides e predadores. São Paulo: Editora Manole 609p.

 
 

Paula DP, Andow DA, Pires SCS, Sujii ER (2015). Impacto da Introdução de Pragas sobre a Biodiversidade. Cap. 3. In: Sugayama, R. L.; Lopes-Da-Silva, M.; Silva, S. X. B.; Ribeiro, L. C.; Rangel, P. L.E. Defesa vegetal: fundamentos, ferramentas, políticas e perspectivas. 1ª ed. Belo Horizonte; SBDA-Sociedade Brasileira de Defesa Agropecuária 544p.

 
 

Paz JRL, Pigozzo CM (2012). Comparação da Entomofauna Coletada por Armadilhas Coloridas de Água em um Fragmento de Mata Atlântica e Dois Ecossistemas Associados, Bahia. Candombá – Revista Virtual 8(1):63-72.

 
 

Pielou EC (1975). Ecological Diversity. Wiley Interscience, New York.

 
 

Pielou EC (1966). The measurement of diversity in different types of biological collections. J. Theor. Biol.13:131-144.
Crossref

 
 

Rafael JA, Melo GAR, Carvalho CJB, Casari AS (2012). Insetos do Brasil: Diversidade e Taxonomia. Ribeirão Preto: Holos, Editora 810p.

 
 

Ramalho M (2004). Stingless bees and mass flowering trees in the canopy of Atlantic Forest: a tight relationship. Acta Bot. Bras., 18(1):37-47.
Crossref

 
 

Ribeiro FV (2005). Biodiversidade e distribuição geográfica de Anastrepha spp. (Diptera: Tephritidae) no Alto e Médio Rio Solimões, Amazonas. 2005. 106f. Dissertação (Mestrado em Agricultura e Sustentabilidade na Amazônia) - Faculdade de Ciências Agrárias, Universidade Federal do Amazonas, Manaus.

 
 

Ricotta C (2005). Through the jungle of biological diversity. Acta Biotheor. 53(1):29-38.
Crossref

 
 

Rocha JF, Pimentel RR, Rosa MMT, Machado SR (2010). Anatomia e histoquímica dos nectários florais de Dombeya wallichii (Lindl.) K. Schum. e Dombeya natalensis Sond. (Malvaceae). Rev. Biol. Neotrop. 7(1):27-36.

 
 

Rodrigues WC (2017). DivEs - Diversidade de Espécies v4.0. Software e guia do usuário. Disponível em:< http://dives.ebras.bio.br>. Acesso em 15 de jan. 2017.

 
 

Santos JP, Wamser AF, Becker WF, Mueller S, Suzuki A (2008). Captura de insetos sugadores e fitófagos com uso de armadilhas adesivas de diferentes cores nos sistemas de produção convencional e integrada de tomate em Caçador, SC. Hortic. Bras. 26: S157-S163.

 
 

Santos JPS, Wamser AF, Mueller WFBS, Romano F (2008). Atraidos pela cor. Tomate-Cultivar HF, Fevereiro / Março. pp. 18-19.

 
 

Santos AB, Nascimento FS (2011). Diversidade de visitantes florais e potenciais polinizadores de Solanum lycopersicum (Linnaeus) (Solanales: Solanaceae) em cultivos orgânicos e convencionais. Neotrop. Biol. Conserv. 6(3):162-169.

 
 

Seltmann K (2004). Building web-based interactive keys to the Hymenopteran families and superfamilies. Lexington, Kentucky, 2004. 73 p. Dissertação (Master of Science in Entomology in the College of Agriculture) - University of Kentucky.

 
 

Silva FF, Carvalho GA (2015). Espécies, número e frequência de visitantes florais em culturas agrícolas submetidas à aplicação de produtos fitossanitários. Arq. Inst. Biol., São Paulo 82:1-7.
Crossref

 
 

Silva FAS, Azevedo CAV (2009). The Assistat Software Version 7.7 and its use in the analysis of experimental data. Afr. J. Agric. Res. 11(39):3733-3740.

 
 

Skorupski P, Chittka L (2010). Photoreceptor Spectral Sensitivity in the Bumblebee, Bombus impatiens (Hymenoptera: Apidae). PLoS ONE 5(8): e12049.
Crossref

 
 

Soares JBC, Costa EM, Silva FEL, Araujo EL (2016). Insect diversity in an experimental vineyard in the State of Rio Grande do Norte, Brazil. Revista Caatinga, Mossoró, 29(1):239-245.

 
 

Souza DTM (2011). Comportamento forrageiro de insetos visitantes florais da romãzeira (L.). Magistra 23(3):122-128.

 
 

Susek A, Ivancic A (2006). Pollinators of Helleborus niger in Slovenian naturally occurring populations. Acta Agric. Slovenica pp. 205-211.

 
 

Togni PHB, Cavalcante KR, Langer LF, Gravina CS, Medeiros M, Pires CSS. Fontes EMG, Sujii ER (2010). Conservação de inimigo naturais (Insecta) em tomateiro orgânico. Instituto Biologico, 77(4):669-676.

 
 

Triplehorn CA, Johnson NF (2005). Borror and delong's introduction to the study of insects. Belmont: Thomson Brooks.

 
 

Vasconcellos A, Andreazze R, Almeida AM, Araujo HFP, Oliveira ES, Oliveira U (2010). Seasonality of insects in the semi-arid Caatinga of northeastern Brazil. Revista Brasileira de Entomologia, Curitiba, 54(3):471-476.
Crossref

 
 

Vianna MA, Marco-Junior P, Campos LA (2007). O. Manejo de polinizadores e o incremento da produtividade agrícola: uma abordagem sustentável dos serviços do ecossistema. Resumo do II Congresso Brasileiro de Agroecologia. Rev. Bras. Agroecologia. 2(1):144-147.

 
 

Virginio F, Maciel TT, Barbosa BC (2016). Novas contribuições para o conhecimento de vespas sociais (Hymenoptera: Vespidae) para Estado do Rio Grande do Norte, Brasil. Entomotropica 31(26):221-22.

 
 

Vrdoljak SM, Samways MJ (2012). Optimising coloured pan traps to survey flower visiting insects. J. Insect Conserv. 16:345-354.
Crossref

 
 

Wanga H, Conchou L, Bessière J, Cazals G, Schatz B, Imbert E (2013). Flower color polymorphism in Iris lutescens (Iridaceae): Biochemical analyses in light of plant–insect interactions. Phytochemistry 94:123-134.
Crossref

 
 

Wells JM BC, Raju H, Hung WG, Weinsberg L, Mandelco-Paul DJB (1987). Xylella fastidiosa gen. nov. sp.nov.: Gram-negative, sylem-limited fastidiosa bacteria related to Xanthomonas spp. Int. J. Syst. Bacteriol. 37:136-143.
Crossref

 
 

Wilsey BJ, Chalcraft DR, Bowles CM, Willig MR (2005). Relationships among indices suggest that richness is an incomplete surrogate for grassland biodiversity. Ecology 86(5):1178-1184.
Crossref

 
 

Zanzini ACS (2005). Descritores Quantitativos de Riqueza e Diversidade de Espécies Lavras: UFLA/FAEPE. 43p.

 

 




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