Use of flower strips to attract pollinator insects and natural enemies in tomato crops

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The study was conducted using commercial tomatoes (6.200 m²) in the Brazilian Cerrado. The experimental outline was completely randomized with 15 plots of 5 x 4 meters, constructed with 16 tomato plants, in two treatments: 1) tomato plants without attractive flower strips (control) and 2) tomato plants with attractive flower strips of cilantro and sorghum. The sampling of pollinator insects and natural enemies was performed using trap-type bee bowls and active collection. Data were analyzed by generalized linear models (GLM) to compare insect diversity and abundance between treatments. As a result, the richness (p = 0.040) and abundance (p = 0.030) of pollinating insects were significantly higher in tomatoes with sorghum flowers than in the control. The effect of mixing strips of intercropped flowers (cilantro and sorghum) increased the abundance (p = 0.007) and richness (p = 0.005) of the total natural enemies and pollinators in richness (p = 0.030) and abundance (p = 0.020) in the tomato plants with the flower strips compared to the tomato plants without the strips. Our results clearly show that the use of attractive flower strips of the mix of cilantro and sorghum in interleaved periods with tomato plants contributes to the permanence of the services provided by insects to the crop field. Environmental service floral resource sorghum mix of sorghum flowers and cilantro Figures Figure 1 Figure 2 Figure 3 Figure 4 Figure 5 INTRODUCTION The intensified land use, pesticide use, climate change, and fragmentation of habitats have driven the decline in populations of beneficial insects like pollinators and natural enemies (Grubisic et al. 2018 ). These changes reduce the areas of native vegetation and ecological corridors that interfere with the availability of food and nesting sites for insects (Kremen et al. 2007 ; Oliveira and Maruyama 2014 ). Furthermore, the use of pesticides can cause lethal or sublethal effects to exposed insects, which affects behavior, performance, and neurophysiology (Desneux et al. 2007 ; Freitas and Pinheiro 2010 ; Gierer et al. 2019 ). Insects are the most diverse and abundant organisms on Earth and are providers of important ecosystem services essential for humanity, such as pollination and biological control of plagues (Garibaldi et al. 2016 ; Schowalter et al. 2018 ; Stork 2018 ; Togni et al. 2019 ). Biotic pollination, exercised by animals, is of utmost importance for the reproduction of plants, resulting in the formation of fruits and seeds (Biesmeijer et al. 2006 ; Klein et al. 2007 ; Ollerton et al. 2011 ; Roubik 2018 ). In tropical regions, approximately 94% of plants are pollinated by animals. From the studies about pollination, 72% are from temperate regions, and Brazil represents from 2–5% of the studies, indicating a lack of information, according to Bartholomée and Lavorel ( 2019 ). In agriculture, bees are the most abundant group of pollinators, visiting more than 90% of the 107 main agricultural crops in the world (Klein et al. 2007 ). In Brazil, of 141 agricultural crops, 85 depend on pollinators. The economic contribution made by the pollination ecosystem service represented 30% of the total annual agricultural income of the dependent crops (Giannini et al. 2015a ). The absence of pollinators causes a decrease of 3–8% in agricultural production, affecting the diversity and quantity of agriculture (Maués 2014 ). Besides, the biological control of agricultural pests is a service carried out by natural enemies that are fundamental for the regulation and suppression of pests from the agroecosystem. Biological control collaborates to reduce the use of pesticides due to the maintenance of the pests at a below action level, contributing to the increment of agricultural production (Ghosh 2011 ; Naranjo et al. 2015 ). Therefore, pollination ecosystem services, as well as biological controls, contribute to food production (Steward et al. 2014 ) and are directly related to the richness of pollinators and natural enemies in the field (Dainese et al. 2019 ). The maintenance of the areas surrounding agricultural crops is of utmost importance for the permanence of beneficial pollinators (Garibaldi et al. 2014 ; Oliveira and Maruyama 2014 ; Kremen and M’Gonigle 2015 ; Aizen et al. 2019 ). In fact, the addition of flowering plant species favors an increase in the multifunctionality of the environment, attracting pollinator species and natural enemies (Wratten et al. 2012 ; Gontijo et al. 2013 ; Garibaldi et al. 2014 ; Blaauw and Isaacs 2015 ; Sidhu and Joshi 2016 ). Flowering plants can provide resources for pollinators beyond the flowering interval of adjacent crops (Rosas-Ramos et al. 2019 ) or shorten the flight distance of these species, especially in large areas of cultivation (Garibaldi et al. 2014 ). Thus, the surrounding crops can improve the reproduction rate (Carvell et al. 2015 ), increasing the abundance and richness of species of beneficial insect pollinators (Jönsson et al. 2015 ; Scheper et al. 2015 ). In addition, the provision of floral resources close to agricultural landscapes benefits natural enemies, which increases or maintains pest suppression (Isbell et al. 2011 ; Kremen and Miles 2012 ; Araj and Wratten 2015 ; Tschumi et al. 2016 ; Garratt et al. 2017 ; Rand et al. 2019 ; Rosas-Ramos et al. 2019 ). Attractive flowers are classified by their function within habitat management and are known as floral plants, trap crops, habitat plants, and attractive flower strips (Frank 2010 ; Parolin et al. 2014 ). Recent studies have shown the efficiency of flowering species in the management of natural enemies within crops, such as the use of sweet alyssum Lobularia maritima (L.) Desv., Coriandrum sativum L. (Pineda and Marcos-García 2008 ), Fagopyrum esculentum Moench. (Balzan and Wäckers 2013 ; Rijn et al. 2013 ), and Calendula officinalis L. (Zhao et al. 2016 ). In addition, other studies have demonstrated the efficiency of flowering plants in increasing the diversity and abundance of pollinators (Sutter et al. 2017 ; Eeraerts et al. 2019 ; Timberlake and Vaughan 2019 ; Urbanowicz et al. 2020 ). The tomato ( Solanum lycopersicum L.) is considered an autogamous plant; however, the morphologic characteristic of the genus presents anthers with a poricidal opening, which requires the agitation of its flowers by the wind or pollinators for fertilization (Kevan et al. 1991 ; Morandin et al. 2001 ; Córdoba and Cocucci 2011 ). The pollination dependency rate in this crop is considered to be modest from 10–40%. This rate is set according to the effect of pollinators on the increase in crop production (Klein et al. 2007 ; Giannini et al. 2015a ). However, recent results show that the pollination carried out by bees (pollination by buzzing) increases the productivity and quality of the tomato fruit (Gaglianone et al. 2018 ). In 2019, world tomato production was 37.38 million (M kg) (Tomato News Sas 2020 ). In Brazil, Solanaceae is considered to be of great economic importance, with an annual production of 4.3 M kg, representing 57.4% of all the vegetables cultivated in the country (Instituto Brasileiro De Geografia E Estatística – IBGE 2019). The present study aimed to assess the effect of attractive flower strips on the regulation of environmental services by insects (pollination and biological control) in the tomato crop S. lycopersicum . Thus, the following hypotheses were tested: (H1) the diversity of pollinator insects and natural enemies increases with the attractive flower strips of cilantro and sorghum in corn fields; and (H2) the production of tomato fruits increases according to the attractive flower strips of cilantro and sorghum. MATERIALS AND METHODS Study Area The research was conducted on a rural property (15° 37’ 38’’ S 58° 10’ 55’’ W; 284 masl) in the municipality of São José dos Quatro Marcos (Mato Grosso, Brazil). The rural property is in proximity to a remnant of secondary vegetation of 10.4 acres and cultivates species of tomato crop fields of different planting ages, banana ( Musa paradisiaca L.), cucumber ( Cucumis sativus L.), and corn ( Zea mays L.) in different flowering periods. The commercial tomato production used in our study corresponds to an autumn-winter planting, with an area of approximately 6.200 m² and spacing of 1.25 m between rows and 1 meter between the plants (double rows of planting separated by 2.5 meters). The experimental parcel was 5 x 4 m, consisting of 16 tomato plants arranged in the experimental area of two treatment schemes: 1) tomato plants without attractive flower strips (control) and 2) tomato plants with attractive flower strips of cilantro and sorghum (Fig. 1 ). The sample design was entirely randomized, consisting of 2 treatments: control (tomato plants without the attractive flower strips, T1-T5) and tomato plants with attractive flower strips (cilantro and sorghum, C1-C10) with 15 parcels, 5 repetitions for witness strips and 10 repetitions for the attractive flower strips. The parcels consisted of double rows of tomatoes, with 8 tomato plants per row, totaling 16 tomato plants per parcel (Fig. 1 ). The cilantro row flourished before sorghum, and the two attractive species did not flower simultaneously. The cilantro was distributed among the tomato plant rows in the experimental parcel, 60 days after transplanting the tomato seedlings. Thus, we sowed the cilantro in a seedling tray with substrate, and after 7 days, we transplanted it into permanent pots that were distributed in the experimental area. Cilantro flowering occurred between 60 and 68 days after tomato transplantation. The graniferous sorghum was planted 48 days after transplanting the tomato seedlings to the study plot, to the border of the area, in a single strip with a line of 67 linear meters. Sorghum flowered between 72 and 80 days after the tomato transplant. Sampling of pollinators and natural enemies The sampling of the pollinator insects and natural enemies was carried out during the 8 days of the flowering period of the attractive flower strips. Two methods were used for sampling: active trapping (sweep netting) and passive trapping (pan traps, i.e., bee bowls). In the active trapping, the insects were sampled for 20 minutes in each parcel from 7:00 to 12:00 in the morning and captured with an entomological net. The total sampling effort was 40 hours at the end of the 8 days of sampling. The trap used was the bee bowl (BB), according to the methodology adapted from Wheelock and O’Neal ( 2016 ), which allocated 1 bee bowl per parcel. To collect natural enemies and pollinators together, the traps were installed every 2 days within the 8-day period for active sampling. The sampling of the insects occurred at two moments, the first from 60 to 68 days of tomato transplantation when the cilantro was flowering, and the second moment from 72 to 80 days of tomato transplantation when the sorghum was flowering. The collected insects were identified at the family level with the assistance of taxonomic identification keys and at the morph types. The insects were assigned to one of the following functional groups as “pollinators or natural enemies” based on specific literature (Rosas-Ramos et al. 2019 ). To evaluate the tomato production within the parcel, 8 tomato plants were evaluated per parcel. The green and ripe tomato fruits were harvested 90 days after transplantation of the tomato seedlings and weighed with an electronic balance. Statistical Analysis The generalized linear model (GLM) was used to model the number of beneficial insects (richness and abundance of pollinators and natural enemies) as a function of the attractive flower strip using the Poisson, Quasipoisson, or binomial negative distribution errors. The overdispersion, Q-Q plots, and Akaike's criterion (AIC) of each model were evaluated, and the better error function distribution was chosen. The explanatory variable (x) was composed of two levels, 1. tomato plants without an attractive flower strip (control) and 2. tomato plants with an attractive flower strip, and the response variables (y) were pollinator richness, pollinator abundance, richness of natural enemies, and abundance of natural enemies. The analyses were separated by the flowering time of each species of attractive flower strips, according to the flowering period, first for cilantro and second for sorghum. Therefore, the analysis of the variable responses was carried out in three different periods, corresponding to the effect of cilantro flowering from 60 to 68 days after tomato transplanting; the sorghum flowering strips from 72 to 80 days of tomato transplanting; and the sum of the richness in the two flowering periods (mix of cilantro flower and sorghum), for which the total richness denomination was used. Likewise, the total abundance was analyzed using the sum of the sampled insects in the two flowering periods (mix of flower cilantro and sorghum). This analysis was made from the sum of the morph types of insects in the attractive flower strips of cilantro and sorghum. To verify the hypothesis that the diversity of pollinator insects and natural enemies increases with the proximity of the corn field, which was in a productive phase during the study period, an F test was used. In the statistical model, the variable (x) was composed of the distance between the parcels of the tomato plant area and the corn field, and the variable response (y) was the richness in the pollinators. The same model was used for the other variable responses, such as the abundance of pollinators, the richness of natural enemies, and the abundance of natural enemies. This analysis was done because the corn field is located between the tomato field of the experiment and the fragment of native vegetation (Fig. 1 ). Therefore, it was possible to verify whether corn attracted the insect pollinators and natural enemies to the tomato plants or was a barrier between the tomato plants and the fragment of native vegetation. Jaccard similarity indices were used to compare associations between absence/presence data of insect and treatment (1. flower strips of cilantro, 2. flower strips of sorghum, and 3. without attractive flower strips - control). The indices ranged from 0 (no similarity) to 1 (identity) and were used in the free program PAST-Paleontological Statistics. Furthermore, to verify the relationship between the production of tomato fruits and the surrounding tomato plants and the diversity of the pollinator insects, multiple regression was used, with tomato production (kg) as the variable response (y). The explanatory variables were surrounding the tomato (x1) (1. without attractive flower strips and 2. with attractive flower strips of cilantro and sorghum), total richness of the pollinator morphotypes (x2), and total abundance of the pollinators (x3), in addition to the interaction between x1:x2 and x1:x3. The same model was used to verify whether there was a contribution from the natural enemies to the production of the tomato fruits. The analysis procedure was backward, and the model was simplified by removing the nonsignificant variables with an F test required to be below 5%. Statistical models were applied to critically appraise the final model with model-checking plots. All analyses were fitted in R (R Core Team 2019). The normality test was applied to verify the adjustment of the response variable to the distribution of errors. RESULTS The abundance of the sampled morph types was 216 insects distributed in 6 orders and 31 families. Among the pollinators, orders Diptera, Coleoptera, and Hymenoptera were identified. Order Hymenoptera was the most abundant (49.15%), represented mainly by bees from the Apidae family. Diptera was the most abundant order of the natural enemies sampled (18. 9%), represented mainly by flies Syrphidae and Tachinidae, followed by order Hymenoptera (7. 9%), Coleoptera (3. 2%), Odonata (1. 8%), and Neuroptera (0.5%). From the 31 families identified, 15 were classified as pollinators, 9 as natural enemies, and 7 as pollinators and natural enemies (Table 1 ). Table 1 Insects identified after active trapping (sweep netting and pan traps) in an experimental tomato crop field in southwestern Mato Grosso State. In the attractive flower strips: 1) Control (without stripe), 2) With cilantro flower stripe, and 3) With sorghum flower stripe. Family Attractive flower strips Functional groups Nº % Reference Diptera Syrphidae 1,2,3 Pollinator/Predator 16 5.9 (Morales and Köhler 2006 ) Stratiomyidae 1,2,3 Pollinator 4 1.5 (Roig-Juñent et al. 2015 ) Hermetia illucens (L.) 1,2 Pollinator 2 (Pujol-Luz, JR and Pujol-Luz CVA 2014) Hermetia albitarsis (Fabricius) 2 Pollinator 1 (Cusser et al. 2015 ) Sargus fasciatus (Valenciennes) 3 Pollinator 1 (Pujol-Luz, JR and Pujol-Luz CVA 2014) Tachinidae 1,2,3 Parasitoid 16 5.9 (De Groot et al. 2007 ) Bombyliidae 2 Pollinator/ Parasitoide/ Predator 6 2.2 (Deyrup MA 1988 ; Koptur et al. 2013 ; Oliveira and Maruyama 2014 ; Van Herk et al. 2015 ; Barbosa et al. 2016 ) Tachinidae 1,2,3 Parasitoid 16 5.9 (De Groot et al. 2007 ) Bombyliidae 2 Pollinator/ Parasitoide/ Predator 6 2.2 (Deyrup MA 1988 ; Koptur et al. 2013 ; Oliveira and Maruyama 2014 ; Van Herk et al. 2015 ; Barbosa et al. 2016 ) Poecilognathus spp. (Jaenicke) 2 Pollinator 3 Villa spp. (Lioy) 2 Parasitoid 3 Ceratopogonidae 2 Pollinator/ Ectoparasite 1 0.4 Asilidae 3 Pollinator/ Predator 1 0.4 (Berti Filho and Macedo 2011 ;; Kohler et al. 2013 ; Koptur et al. 2013 ; Wolowski et al. 2019 ) Mallophora calida (Fabricius) 3 Predator 1 Tabanidae 3 Pollinator/Parasitoid 1 0.4 Chrysops variegatus (De Geer) 3 Pollinator 1 (Tamayo-Cen 2020 ) Coleoptera Scarabaeidae 1,2,3 Pollinator 9 3.3 (Paulino-Neto 2014 ) Crysomelidae 1,2,3 Pollinator 13 4.8 Coccinellidae 2,3 Pollinator/Predator 4 1.5 (Berti Filho and Macedo 2011 ; Wolowski et al. 2019 ) Carabidae 1,3 Predator 3 1.1 (Berti Filho and Macedo 2011 ) Tenebrionidae 3 Pollinator 1 0.4 (Witt et al. 2004 ; Paulino-Neto 2014 ) Curculinonidae 3 Pollinator 1 0.4 Cerambycidae 3 Pollinator 1 0.4 (Wolowski et al. 2019 ) Elateridae 3 Pollinator 1 0.4 (Paulino-Neto 2014 ) Hemiptera Scutelleridae 1,2,3 Pollinator 8 2.9 (Berti Filho and Macedo 2011 ; Wolowski et al. 2019 ) Reduviidae 2 Predator 1 0.4 (Berti Filho and Macedo 2011 ) Coreidae 1,3 Pollinator 2 0.7 (Wolowski et al. 2019 ) Hymenoptera Apidae 1,2,3 Pollinator 95 35.1 (Oliveira and Maruyama 2014 ) Apis mellifera (Linnaeus, 1758) Polinizador (Santos et al. 2014 ; Giannini et al. 2015; Vinícius-Silva et al. 2017 ; Toni et al. 2021) Euglossa (Euglossa) carolina (Nemésio, 2009) Potencial Polinizador (Deprá et al. 2014 ) Bombus (Thoracobombus) brevivillus (Franklin, 1913) Polinizador (De Luca and Vallejo-Marin 2013) Tetragona clavipes (Fabricius, 1804) Visitante floral (Silva-Neto et al. 2017 ) Frieseomelitta varia (Lepeletier, 1836) Visitante floral . (Silva-Neto et al. 2017 ; Vinícius-Silva et al. 2017 ) Trigona dallatorreana (Friese, 1900) Polinizador (Santos et al. 2014 ; Vinícius-Silva et al. 2017 ) Oxytrigona aff. flaveola (Friese, 1900) ? - Ceratina (Calloceratina) chloris (Fabricius, 1804) ? - Florilegus (Euflorilegus) aff. affinis (Urban, 1970) ? - Vespidae 1,2,3 Pollinator/Predator 12 4.4 ( Berti Filho and Macedo 2011 ; Oliveira and Maruyama 2014 ) Halictidae 2,3 Pollinator 2 0.7 ( Berti Filho and Macedo 2011 ; Oliveira and Maruyama 2014 ) Augochloropsis sp. 22 Polinizador (Teppner 2005 ; Vinícius-Silva et al. 2017 ) Megachilidae 1,2,3 Pollinator 4 1.5 ( Berti Filho and Macedo 2011 ; Oliveira and Maruyama 2014 ) Megachile (Sayapis) sp. 1 Polinizador (Teppner 2005 ; Vinícius-Silva et al. 2017 ) Megachile (Leptorachis) sp. 1 Polinizador (Teppner 2005 ; Vinícius-Silva et al. 2017 ) Andrenidae 2 Pollinator 2 0.7 ( Berti Filho and Macedo 2011 ; Oliveira and Maruyama 2014 ) Oxaea flavescens (Klug, 1807) Potencial Polinizador (Deprá et al. 2014 ; Santos et al. 2014 ; Silva-Neto et al. 2017 ; Vinícius-Silva et al. 2017 ) Mellitidae 1 Pollinator 1 0.4 (Castro and Singer 2019 ) Formicidae 1 Pollinator 2 0.7 (Gómez and Zamora 1992 ) Evaniidae 2,3 Parasitoid 2 0.7 (Berti Filho and Macedo 2011 ) Ichneumonidae 3 Parasitoid 3 1.1 Odonata Coenagrionidae 2 Predator 2 0.7 (Siregar et al. 2016 ) Libellulidae 1,2 Predator 2 0.7 (Gorayeb and Pinger 1978 ) Neuroptera Chrysopidae 1 Predator 1 0.4 (Berti Filho and Macedo 2011 ) Total 216 100% Source: Ladeia, 2021 In the tomato plants without attractive flower strips (control), 43 insects (15.93%) were sampled; in the tomato plants with attractive flower strips of cilantro, 105 insects (38.89%) were sampled; and 122 insects (45.18%) were sampled in the treatment with attractive flower strips of sorghum. The similarities between the families of the beneficial insects (pollinators and natural enemies) in the cilantro flower strips and in the control were more homogeneous than the insect similarity in the sorghum flower strips (Fig. 2 ). During the flowering of cilantro, the pollinator insect and natural enemies in the tomato plants without the attractive flower strips did not differ from the tomato plants with the strips, both for richness of morph types (X 2 = 4.33, N = 8, p = 0.09) and abundance of natural enemies (X 2 = 4.33, N = 8, p = 0.09). The absence of the effect of the cilantro strip was observed for the pollinator insects, where no difference was found for the richness of morph types (X 2 = 1.25, N = 11, p = 0.34), and for an abundance of pollinating insects, there was also no difference (X 2 = 3.86, N = 11, p = 0.19) with an increase in coriander flower strips in relation to the control. In sorghum flowering, natural enemies did not differ between tomato plants without strips of attractive flowers and tomato plants with strips, both for richness (X 2 = 2.36, N = 11, p = 0.14) and abundance (X 2 = 2.36, N = 11, p = 0.12). For pollinators, the morph-type richness was two times higher in the tomato plants with attractive flower strips of sorghum than in the tomato plants without the strips (with sorghum strips = 5.56, control = 2.5, X²=6.28, N = 11, p = 0.04) (Fig. 3 a). The abundance of the pollinating insects was three times higher in tomato plants with attractive strips of sorghum than in tomato plants without strips (with sorghum strips = 10.67, control = 3.5, X²=4.94, N = 11, p = 0.02) (Fig. 3 b). The effect of the two attractive flower strips intercropped (with mixed strips of cilantro and sorghum) increased the total abundance of natural enemies by more than three times in the tomato plants with strips of cilantro and sorghum compared to the tomato plants without the strips (mix of cilantro and sorghum = 6.56, control = 2.6, Χ2 = 7.16, N = 12, p = 0.007) (Fig. 4 a). The same effect was observed for the total richness of natural enemies (mix of cilantro and sorghum = 6.44, control = 2.4, Χ²=7.91, N = 12, p = 0.005) (Fig. 4 b). The total abundance of pollinators was three times higher in the mix of cilantro and sorghum than in the control (mix of cilantro and sorghum = 17.1, control = 5.8, Χ²=35.81, N = 12, p = 0.02) (Fig. 4 c). The mix of cilantro flower and sorghum increased the total richness of morph types by two times (mix of cilantro and sorghum = 10.4, control = 4.8, Χ²=13.29, N = 12, p = 0.03) (Fig. 4 d). The diversity of natural enemy insects increased with the distance from the corn field, which was observed for the morph type richness (p = 0.02, N = 12, r²=0.37) (Fig. 5 a) and abundance (p = 0.03, N = 12, r²=0.33) (Fig. 5 b). The distance from the corn field ,when combined with the attractive flower strips, had no effect on natural enemies or the interactions (corn field distance * attractive flower strips/species richness p = 0.4 and abundance p = 0.5). For the pollinators, the morph-type richness increased with distance from the corn field (p = 0.004, N = 12, r²=0.50) (Fig. 5 c), as did the abundance (p = 0.003, N = 12, r²=0.53) (Fig. 5 d). The interactions of the corn field distance and the attractive strips were not significant (corn field distance * attractive flower strips/species richness p = 0.48 and abundance p = 0.38). Tomato production was not influenced by the use of attractive flower strips (mix of cilantro flowers and sorghum; p = 0.26) in consortium with tomato plants or by the diversity of natural enemies (total morph-type richness with strips = 7 ± 3.68, control = 2 ± 1.14, p = 0.46, N = 8 and total abundance with strips = 7 ± 3.75, control = 3 ± 1.14, p = 0.13, N = 8). The diversity of pollinators did not influence tomato production (total morph-type richness with strips = 10 ± 4.39, control = 3 ± 3.63, p = 0.64, N = 8 and total abundance with strips = 15 ± 9.77, control = 5 ± 5.26, p = 0.52, N = 8), and the surroundings did not show an effect (p = 0.34) when combined with the pollinators. The diversity of pollinators did not influence tomato production (total morph-type richness with strips = 10 ± 4.39, control = 3 ± 3.63, p = 0.64, N = 8 and total abundance with strips = 15 ± 9.77, control = 5 ± 5.26,p = 0.52, N = 8), and the surroundings did not show an effect (p = 0.34) when combined with the pollinators. DISCUSSION The working hypothesis was that the consortium of tomato plants with cilantro and sorghum contributes to the increase in the abundance and richness of pollinator insects and natural enemies. In our tomato study, the hypothesis was accepted for the richness of pollinators due to sorghum and the abundance of natural enemies when using cilantro together with the crop planting. The heterogeneity of agricultural landscapes provides complementary resources over time and space, such as food resources and nesting sites, which consequently increase the richness and abundance of pollinator insects and natural enemies (Nicholls and Altieri 2012 ; Karamaouna et al. 2019 ; Aguilera et al. 2020 ). Food resources are offered to floral visitors through nectar, pollen, oils, and floral fabrics of plants. Pollen is used by pollinator species as a source of lipids, proteins, carbohydrates, and minerals (Agostini et al. 2014), and nectar is an energy source for worker bees and the queen (Roulston and Cane 2000 ). Species of Solanacea, such as tomato S. lycopersicum , are an important source of pollen, especially for species that perform “pollination by buzzing” (Nunes-Silva et al. 2013 ; Santos et al. 2014 ; Silva-Neto et al. 2017 ; Vinícius-Silva et al. 2017 ). A diverse group of flower species with different phenologies increases the stability of resources for pollinators and, therefore, increases pollination services (Blüthgen and Klein 2011 ; Mandelik et al. 2012 ). The effect of the diversification of cilantro and sorghum attractive flower strips in tomato plants contributed to the total abundance of natural enemies, confirming that the management of landscape diversity has the potential to maintain or increase biological control services (Gardiner et al. 2009 ). This event indicates that an arrangement with non-agricultural species on a different special scale is a solution that improves the biological control of agricultural pests (Gagic et al. 2018 ). In fact, cilantro is considered an aromatic plant, which in addition to the floral resource available in the system can attract natural enemies through volatile constituent substances (Salamanca et al. 2018 ). Similar results of the increase in the abundance of natural enemies in attractive flower strips of cilantro in tomato crops have been found in previous studies with eggplant crops (Patt and Lashomb 1997 ), buckwheat (Piñero and Manandhar 2015 ), rose (Salamanca et al. 2015 ), cabbage (Morris and Li 2000 ; Silva; et al. 2016 ), carrot (Jankowska and Wojciechowicz-Zytko 2016 ), bean (Salamanca et al. 2018 ), and olive (Karamaouna et al. 2019 ). The natural odors emitted by aromatic plants influence the foraging and behavior of pollinators and natural enemies (Kessler and Baldwin 2006 ; Kessler and Halitschke 2007 ; Chen 2008 ; Heil 2008 ; Raguso 2008 ). These aromatic plants can attract, through volatile compounds, general natural enemies capable of controlling populations of insect pests (Togni et al. 2016 ). Cilantro is an aromatic plant capable of attracting a greater number of natural enemies when flowering (Medeiros et al. 2009 ; Togni et al. 2009 ). These volatile compounds emitted by cilantro increase the attractiveness of generalist predators, such as the ladybug Cycloneda sanguinea (Linnaeus) (Coccinellidae), as well as serving as oviposition sites for these insects. In this study, Coccinellidae were the most frequent predators among the beetles. In addition, the insertion of cilantro strips increases the efficiency of land use and provides extra income to the farmer (Resende et al. 2010 ; Medeiros et al. 2011 ; Togni et al. 2016 ). Keeping natural enemies abundant within a cultivation system can reduce the frequency with which some pests reach the level of action (Garratt et al. 2017 ). In our study, Syrphidae and Tachinidae were the most abundant families of natural enemies. Flies of the Syrphidae family are important predators for pest management; their larvae feed on aphids and thrips that infest many agricultural species (Rojo and Marcos-García 1997 ) and specifically tomato crops (Abro et al. 2019 ). Aphids and thrips are considered severe pests to tomato plants due to the transmission of the virus (Miranda et al. 1998 ). The Tachinidae family has groups of parasitic flies that are important for the management of pest populations, particularly coleopterous and lepidopterous populations (Stireman et al. 2006 ), as well as caterpillar Helicoverpa zea (Boddie) (Farrar et al. 1992 ). The attractive flower of sorghum together with cilantro was responsible for increasing the total abundance of natural enemies in tomato cultivation. Sorghum was used as a trap crop (Gordon et al. 2017 ); this terminology is used to define species that are used to attract, deflect, and intercept pest insects to decrease the damage to the main crop (Shelton and Badenes-Perez 2006 ). Sorghum is an efficient trap crop for reducing the management of phytophagous stink bugs in cotton crops (Tillman 2006 ), tomato (Majumdar et al. 2012 ; Gordon et al. 2017 ), organic gardens (Nielsen et al. 2016 ), and bell pepper (Blaauw et al. 2017 ). In cotton, the use of sorghum trap crops helped to control of Helicoverpa armigera (Hübner) (Prakasha et al. 2016 ) and to increase the population density of ladybugs (Tillman and Cottrell 2012 ). The method of “trapping crops”, used with attractive flower strips, can increase biodiversity due to the supply of nectar and pollen for beneficial insects, which favors the services provided by natural enemies, contributing to the reduction in the use of pesticides (Pollock 2012 ; Nielsen et al. 2016 ). Trap crops help to conserve fertile soil, reduce damage to commercial crops, and increase profit from the harvest by 10–30% (Prakasha et al. 2016 ). The richness of pollinators favored attractive flower strips of tomato and sorghum because sorghum can be foraged by bees from the Apidae and Halictidae families and used as a food source, especially when there are no food resources available (Schmidt and Bothma 2005 ). The richness of plant species with flowers adjacent to a crop promotes the diversity of pollinators (Scheper et al. 2013 ; Kremen and M’Gonigle 2015 ; Sutter et al. 2017 ; Kremen et al. 2018 ), which favors an increase in pollination services by up to 52% (Albrecht et al. 2020 ). The hypothesis that the production of tomato fruit would be favored by the diversity of pollinators and natural enemies due to the attractive flower strips of cilantro and sorghum was refuted in the present study. The diversity of pollinator insects and natural enemies did not influence productivity in other studies, such as tomato and pepper (Winfree et al. 2008 ), apple (Campbell et al. 2017 ), strawberry (Hodgkiss et al. 2019 ), and melon (Azpiazu et al. 2020 ). The absence of the effect of the diversity of pollinator insects and natural enemies on production may be associated with another factor, such as the size of the attractive flower strips (Hodgkiss et al. 2019 ). In our study, the size of the attractive flower strips may have contributed to the absence of an increase in tomato production in the studied cultivation area due to the size of the flower strip area, which was only 21 m², and we believe that in greater areas, a higher production would be found. Other studies showed that a high abundance of pollinator insects and a high rate of floral visitors were observed along borders with attractive flower strips in areas from 38 m² to 41 m² (Mayer et al. 2012 ) however, no production evaluation was performed. The diversity of pollinator insects and natural enemies in tomato cultivation did not increase with the proximity of the corn crop. Although agricultural species cultivated in the reproductive phase provided floral resources and increased pollinators in comparison with the remainder of the native vegetation; this was not observed for tomato in relation to corn. This fact could be due to the massive flowering of the attractive species monopolizing the visits of bees, as was observed for Hedysarum coronarium L. (Fabaceae), a native species from Portugal. In that study, proximity to crops caused a decrease in the abundance of pollinators in the native vegetation adjacent to the species (Montero-Castaño et al. 2016 ). The concentration of floral resources in the sunflower crop increased the abundance of pollinators within the cultivation area in relation to the Cerrado remnant (Almeida et al. 2020 ). Monoculture has mass flowering that attracts pollinators, temporarily decreasing the presence in adjacent forests (Montero-Castaño et al. 2016 ). Foraging behavior can be influenced, mainly by species of insects with short flight distances between floral visits (Gross 2001 ), so pollinators benefit from available high-quality floral resources (Dietzsch et al. 2011 ). Although flower visiting insects can perform pollination, due to the search for nectar or pollen in flowers as food resources for themselves or offspring, they do not always perform pollination (Alves-dos-Santos et al. 2016 ). In contrast, pollinating insects always transfer pollen from the anthers to the stigma of the flower of the same plant species. Floral visitor species that do not carry out buzz pollination can perform pollination, but due to the low vibration capacity of the flowers, this does not prevent the extraction and transfer of pollen to the stigma of the flowers, which is why they are less efficient in this process (De Luca and Vallejo-Marin 2013). Tomato flowers ( S. Lycopersicum ), as well as other species of the genus Solanum , have poricidal anthers, pollinated by social bees of the genus Melipona , Bombus , and solitary bees of the genus Xylocopa (De Luca and Vallejo-Marin 2013). In Brazil, Bombus morio (Swederus) was registered as a pollinator in Goiás, so it is expected that Bombus (Thoracobombus) brevivillus (Franklin, 1913), which was one of the species collected during tomato flowering in Mato Grosso, is an effective pollinator, due to be buzz-pollinate in Solanum stramonifolium Jacq (Bezerra and Machado 2003 ; Nunes-Silva; Hrncir; Imperatriz-Fonseca 2010 ). In addition to Bombus , species of the genus Augochloropsis and Megachile show vibratory behavior of flowers, which are considered important pollinators of the tomato crop (Teppner 2005 ; Vinícius-Silva et al. 2017 ). In our study, species of Augochloropsis and Megachile were recorded during flowering of the crop, so it is expected that they have the function of pollinators for Mato Grosso tomatoes. Species of Apis mellifera and Trigona spinipes (Linnaeus 1758) do not show vibratory behavior but collect pollen grains from flowers that result from buzz pollination by other bee species (Santos et al. 2014 ; Vinícius-Silva et al. 2017 ). These grains can be deposited on the stigma of other flowers due to the foraging behavior of the species (Toni et al. 2021), which is why it is considered a tomato pollinator (Santos et al. 2014 ; Giannini et al. 2015b ; Vinícius-Silva et al. 2017 ). Thus, A. mellifera that was present in tomato flowering can contribute to pollination, as well as the species Trigona dallatorreana (Friese 1900), collected in our study. Bee species with the potential to pollinate tomato plants are Oxaea flavescens (Deprá et al. 2014 ; Santos et al. 2014 ; Silva-Neto et al. 2017 ; Vinícius-Silva et al. 2017 ) and specimens of the genus Euglossa sp. (Deprá et al. 2014 ), so it is believed that Euglossa (Euglossa) carolina (Nemésio 2009) and Oxaea flavescens (Klug 1807), collected from tomatoes in Mato Grosso, are potential pollinators of the tomato crop in Mato Grosso. Among the insects that are classified as floral visitors of tomato plants, we can highlight the genus Frieseomellita and Tetragona (Silva-Neto et al. 2017 ; Vinícius-Silva et al. 2017 ). In our study, the species Tetragona clavipes (Fabricius 1804) and Frieseomelitta varia (Lepeletier 1836) were recorded visiting tomato flowers among other bees of these genus. Other floral visitor species recorded in our study were Ceratina (Calloceratina) chloris (Fabricius 1804) and Florilegus (Euflorilegus) aff. affinis (Urban 1970). CONCLUSION Our study provided a list of pollinator insect families and natural enemies sampled in the experimental tomato planting area. It was also identified that cilantro and sorghum are attractive plant species for pollinator insects and natural enemies when used in combination with tomato. The combination of cilantro and sorghum flower strips in tomatoes had a positive effect on beneficial insects. However, the diversity of pollinator insects and natural enemies did not increase with the proximity of the corn crop because the floral resources offered by the attractive flower strips of cilantro and sorghum may have influenced the permanence of pollinator insects and natural enemies within the tomato crop. The conclusion of the study was that the attractive flower strips of cilantro and sorghum influenced the increase in the diversity of pollinator insects and natural enemies in the tomato crop, contributing to the permanence of these insects in the crop field and preserving the ecosystem services provided by them. Declarations Author contribution All authors made substantial contributions to the conception and the design of this study. SCL contributed to the development of the fieldwork and to the writing of the manuscript. MFS, ESOJ, and CG contributed to the review of the manuscript. Finally, AS contributed to the statistical analysis of the manuscript. Acknowledgements The authors are thankful to the funding agency Coordenação de Aperfeiçoamento de Pessoal de Nível Superior-CAPES for the financial support and for the research grant. They are grateful to rural producer for the field crop to study. 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Environ. 159, 112–122. https://doi.org/10.1016/j.agee.2012.06.020 Zhao J, Guo X, Tan X, Desneux N, Zhang F, Wang S (2016) Using Calendula officinalis as a floral resource to enhance aphid and thrips suppression by the flower bug Orius sauteri (Hemiptera: Anthocoridae). Pest Manag. Sci. 71. https://doi.org/10.1002/ps.4474 Cite Share Download PDF Status: Posted Version 1 posted You are reading this latest preprint version Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. As a division of Research Square Company, we’re committed to making research communication faster, fairer, and more useful. We do this by developing innovative software and high quality services for the global research community. Our growing team is made up of researchers and industry professionals working together to solve the most critical problems facing scientific publishing. Also discoverable on Platform About Our Team In Review Editorial Policies Advisory Board Help Center Resources Author Services Accessibility API Access RSS feed Manage Cookie Preferences © Research Square 2026 | ISSN 2693-5015 (online) Privacy Policy Terms of Service Do Not Sell My Personal Information {"props":{"pageProps":{"initialData":{"identity":"rs-2751744","acceptedTermsAndConditions":true,"allowDirectSubmit":true,"archivedVersions":[],"articleType":"Research Article","associatedPublications":[],"authors":[{"id":197153877,"identity":"97109c1d-95f6-4f36-a8a8-e5dd296b0101","order_by":0,"name":"Sarah Cavalari 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1","display":"","copyAsset":false,"role":"figure","size":789906,"visible":true,"origin":"","legend":"\u003cp\u003eLayout of the experimental field of tomato crops in the southwest of the State of Mato Grosso, Brazil.\u003c/p\u003e","description":"","filename":"1.png","url":"https://assets-eu.researchsquare.com/files/rs-2751744/v1/5f1ece47d0fbd83bbf7c7d98.png"},{"id":36652435,"identity":"c8fbd011-7efc-4495-a889-4590b1b5f233","added_by":"auto","created_at":"2023-05-05 15:26:11","extension":"png","order_by":2,"title":"Figure 2","display":"","copyAsset":false,"role":"figure","size":32766,"visible":true,"origin":"","legend":"\u003cp\u003eIndex of similarities between the families of beneficial insects (pollinators and natural enemies) with the attractive flower strips (cilantro and sorghum) and the control.\u003c/p\u003e","description":"","filename":"2.png","url":"https://assets-eu.researchsquare.com/files/rs-2751744/v1/2bd835ce60b36693cbc94037.png"},{"id":36652436,"identity":"ce19e8af-ec21-486a-97b9-db22d0fb7ab9","added_by":"auto","created_at":"2023-05-05 15:26:11","extension":"png","order_by":3,"title":"Figure 3","display":"","copyAsset":false,"role":"figure","size":31086,"visible":true,"origin":"","legend":"\u003cp\u003eDiversity of pollinators in the surrounding environments with attractive flower strips of sorghum and without attractive flower strips (control) in tomato plants, a) Pollinator richness and b) Pollinator abundance.\u003c/p\u003e","description":"","filename":"3.png","url":"https://assets-eu.researchsquare.com/files/rs-2751744/v1/7368be5477169d0d68361210.png"},{"id":36653152,"identity":"7d68f3e7-6b8a-400c-be0e-846cc847b70c","added_by":"auto","created_at":"2023-05-05 15:34:11","extension":"png","order_by":4,"title":"Figure 4","display":"","copyAsset":false,"role":"figure","size":110409,"visible":true,"origin":"","legend":"\u003cp\u003eTotal diversity of natural enemies and pollinators in the surrounding environments with attractive flower strips (mix of cilantro and sorghum) and without attractive flower strips (control) in tomato. a) Abundance of natural enemies, b) Richness of natural enemies, c) Abundance of pollinators and d) Richness of pollinators.\u003c/p\u003e","description":"","filename":"4.png","url":"https://assets-eu.researchsquare.com/files/rs-2751744/v1/da7645db8d66585e87d98a80.png"},{"id":36652437,"identity":"1b729338-c92c-4998-a8ce-734f67d2d455","added_by":"auto","created_at":"2023-05-05 15:26:11","extension":"png","order_by":5,"title":"Figure 5","display":"","copyAsset":false,"role":"figure","size":119144,"visible":true,"origin":"","legend":"\u003cp\u003eRelationship between the diversity of natural enemies and pollinators and the corn field distance. a) Richness of natural enemies (equation b: 0.97971 + 0.08918*x), b) Abundance of natural enemies (equation a: 0.63186 + 0.09351*x), c) Richness of pollinator (equation d: -1.41571 + 0.31012*x) and d) Abundance of pollinator (equation c: 1.46003 + 0.1491*x).\u003c/p\u003e","description":"","filename":"5.png","url":"https://assets-eu.researchsquare.com/files/rs-2751744/v1/e81ad37d748973bdab6a5ae6.png"},{"id":38401760,"identity":"c25c99e6-5535-40c8-be44-2c07514ee447","added_by":"auto","created_at":"2023-06-12 14:21:46","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":1518852,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-2751744/v1/01d2fa18-49f4-4f10-b15a-90e5caf2748c.pdf"}],"financialInterests":"","formattedTitle":"Use of flower strips to attract pollinator insects and natural enemies in tomato crops","fulltext":[{"header":"INTRODUCTION","content":"\u003cp\u003eThe intensified land use, pesticide use, climate change, and fragmentation of habitats have driven the decline in populations of beneficial insects like pollinators and natural enemies (Grubisic et al. \u003cspan citationid=\"CR51\" class=\"CitationRef\"\u003e2018\u003c/span\u003e). These changes reduce the areas of native vegetation and ecological corridors that interfere with the availability of food and nesting sites for insects (Kremen et al. \u003cspan citationid=\"CR68\" class=\"CitationRef\"\u003e2007\u003c/span\u003e; Oliveira and Maruyama \u003cspan citationid=\"CR87\" class=\"CitationRef\"\u003e2014\u003c/span\u003e). Furthermore, the use of pesticides can cause lethal or sublethal effects to exposed insects, which affects behavior, performance, and neurophysiology (Desneux et al. \u003cspan citationid=\"CR29\" class=\"CitationRef\"\u003e2007\u003c/span\u003e; Freitas and Pinheiro \u003cspan citationid=\"CR35\" class=\"CitationRef\"\u003e2010\u003c/span\u003e; Gierer et al. \u003cspan citationid=\"CR45\" class=\"CitationRef\"\u003e2019\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eInsects are the most diverse and abundant organisms on Earth and are providers of important ecosystem services essential for humanity, such as pollination and biological control of plagues (Garibaldi et al. \u003cspan citationid=\"CR40\" class=\"CitationRef\"\u003e2016\u003c/span\u003e; Schowalter et al. \u003cspan citationid=\"CR113\" class=\"CitationRef\"\u003e2018\u003c/span\u003e; Stork \u003cspan citationid=\"CR121\" class=\"CitationRef\"\u003e2018\u003c/span\u003e; Togni et al. \u003cspan citationid=\"CR130\" class=\"CitationRef\"\u003e2019\u003c/span\u003e). Biotic pollination, exercised by animals, is of utmost importance for the reproduction of plants, resulting in the formation of fruits and seeds (Biesmeijer et al. \u003cspan citationid=\"CR14\" class=\"CitationRef\"\u003e2006\u003c/span\u003e; Klein et al. \u003cspan citationid=\"CR62\" class=\"CitationRef\"\u003e2007\u003c/span\u003e; Ollerton et al. \u003cspan citationid=\"CR88\" class=\"CitationRef\"\u003e2011\u003c/span\u003e; Roubik \u003cspan citationid=\"CR105\" class=\"CitationRef\"\u003e2018\u003c/span\u003e). In tropical regions, approximately 94% of plants are pollinated by animals. From the studies about pollination, 72% are from temperate regions, and Brazil represents from 2\u0026ndash;5% of the studies, indicating a lack of information, according to Bartholom\u0026eacute;e and Lavorel (\u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e2019\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eIn agriculture, bees are the most abundant group of pollinators, visiting more than 90% of the 107 main agricultural crops in the world (Klein et al. \u003cspan citationid=\"CR62\" class=\"CitationRef\"\u003e2007\u003c/span\u003e). In Brazil, of 141 agricultural crops, 85 depend on pollinators. The economic contribution made by the pollination ecosystem service represented 30% of the total annual agricultural income of the dependent crops (Giannini et al. \u003cspan citationid=\"CR44\" class=\"CitationRef\"\u003e2015a\u003c/span\u003e). The absence of pollinators causes a decrease of 3\u0026ndash;8% in agricultural production, affecting the diversity and quantity of agriculture (Mau\u0026eacute;s \u003cspan citationid=\"CR72\" class=\"CitationRef\"\u003e2014\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eBesides, the biological control of agricultural pests is a service carried out by natural enemies that are fundamental for the regulation and suppression of pests from the agroecosystem. Biological control collaborates to reduce the use of pesticides due to the maintenance of the pests at a below action level, contributing to the increment of agricultural production (Ghosh \u003cspan citationid=\"CR42\" class=\"CitationRef\"\u003e2011\u003c/span\u003e; Naranjo et al. \u003cspan citationid=\"CR81\" class=\"CitationRef\"\u003e2015\u003c/span\u003e). Therefore, pollination ecosystem services, as well as biological controls, contribute to food production (Steward et al. \u003cspan citationid=\"CR119\" class=\"CitationRef\"\u003e2014\u003c/span\u003e) and are directly related to the richness of pollinators and natural enemies in the field (Dainese et al. \u003cspan citationid=\"CR25\" class=\"CitationRef\"\u003e2019\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eThe maintenance of the areas surrounding agricultural crops is of utmost importance for the permanence of beneficial pollinators (Garibaldi et al. \u003cspan citationid=\"CR39\" class=\"CitationRef\"\u003e2014\u003c/span\u003e; Oliveira and Maruyama \u003cspan citationid=\"CR87\" class=\"CitationRef\"\u003e2014\u003c/span\u003e; Kremen and M\u0026rsquo;Gonigle \u003cspan citationid=\"CR67\" class=\"CitationRef\"\u003e2015\u003c/span\u003e; Aizen et al. \u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e2019\u003c/span\u003e). In fact, the addition of flowering plant species favors an increase in the multifunctionality of the environment, attracting pollinator species and natural enemies (Wratten et al. \u003cspan citationid=\"CR140\" class=\"CitationRef\"\u003e2012\u003c/span\u003e; Gontijo et al. \u003cspan citationid=\"CR47\" class=\"CitationRef\"\u003e2013\u003c/span\u003e; Garibaldi et al. \u003cspan citationid=\"CR39\" class=\"CitationRef\"\u003e2014\u003c/span\u003e; Blaauw and Isaacs \u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e2015\u003c/span\u003e; Sidhu and Joshi \u003cspan citationid=\"CR115\" class=\"CitationRef\"\u003e2016\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eFlowering plants can provide resources for pollinators beyond the flowering interval of adjacent crops (Rosas-Ramos et al. \u003cspan citationid=\"CR104\" class=\"CitationRef\"\u003e2019\u003c/span\u003e) or shorten the flight distance of these species, especially in large areas of cultivation (Garibaldi et al. \u003cspan citationid=\"CR39\" class=\"CitationRef\"\u003e2014\u003c/span\u003e). Thus, the surrounding crops can improve the reproduction rate (Carvell et al. \u003cspan citationid=\"CR20\" class=\"CitationRef\"\u003e2015\u003c/span\u003e), increasing the abundance and richness of species of beneficial insect pollinators (J\u0026ouml;nsson et al. \u003cspan citationid=\"CR57\" class=\"CitationRef\"\u003e2015\u003c/span\u003e; Scheper et al. \u003cspan citationid=\"CR110\" class=\"CitationRef\"\u003e2015\u003c/span\u003e). In addition, the provision of floral resources close to agricultural landscapes benefits natural enemies, which increases or maintains pest suppression (Isbell et al. \u003cspan citationid=\"CR55\" class=\"CitationRef\"\u003e2011\u003c/span\u003e; Kremen and Miles \u003cspan citationid=\"CR18\" class=\"CitationRef\"\u003e2012\u003c/span\u003e; Araj and Wratten \u003cspan citationid=\"CR7\" class=\"CitationRef\"\u003e2015\u003c/span\u003e; Tschumi et al. \u003cspan citationid=\"CR132\" class=\"CitationRef\"\u003e2016\u003c/span\u003e; Garratt et al. \u003cspan citationid=\"CR41\" class=\"CitationRef\"\u003e2017\u003c/span\u003e; Rand et al. \u003cspan citationid=\"CR99\" class=\"CitationRef\"\u003e2019\u003c/span\u003e; Rosas-Ramos et al. \u003cspan citationid=\"CR104\" class=\"CitationRef\"\u003e2019\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eAttractive flowers are classified by their function within habitat management and are known as floral plants, trap crops, habitat plants, and attractive flower strips (Frank \u003cspan citationid=\"CR34\" class=\"CitationRef\"\u003e2010\u003c/span\u003e; Parolin et al. \u003cspan citationid=\"CR89\" class=\"CitationRef\"\u003e2014\u003c/span\u003e). Recent studies have shown the efficiency of flowering species in the management of natural enemies within crops, such as the use of sweet alyssum \u003cem\u003eLobularia maritima\u003c/em\u003e (L.) Desv., \u003cem\u003eCoriandrum sativum\u003c/em\u003e L. (Pineda and Marcos-Garc\u0026iacute;a \u003cspan citationid=\"CR92\" class=\"CitationRef\"\u003e2008\u003c/span\u003e), \u003cem\u003eFagopyrum esculentum\u003c/em\u003e Moench. (Balzan and W\u0026auml;ckers \u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e2013\u003c/span\u003e; Rijn et al. \u003cspan citationid=\"CR101\" class=\"CitationRef\"\u003e2013\u003c/span\u003e), and \u003cem\u003eCalendula officinalis\u003c/em\u003e L. (Zhao et al. \u003cspan citationid=\"CR141\" class=\"CitationRef\"\u003e2016\u003c/span\u003e). In addition, other studies have demonstrated the efficiency of flowering plants in increasing the diversity and abundance of pollinators (Sutter et al. \u003cspan citationid=\"CR122\" class=\"CitationRef\"\u003e2017\u003c/span\u003e; Eeraerts et al. \u003cspan citationid=\"CR32\" class=\"CitationRef\"\u003e2019\u003c/span\u003e; Timberlake and Vaughan \u003cspan citationid=\"CR127\" class=\"CitationRef\"\u003e2019\u003c/span\u003e; Urbanowicz et al. \u003cspan citationid=\"CR133\" class=\"CitationRef\"\u003e2020\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eThe tomato (\u003cem\u003eSolanum lycopersicum\u003c/em\u003e L.) is considered an autogamous plant; however, the morphologic characteristic of the genus presents anthers with a poricidal opening, which requires the agitation of its flowers by the wind or pollinators for fertilization (Kevan et al. \u003cspan citationid=\"CR61\" class=\"CitationRef\"\u003e1991\u003c/span\u003e; Morandin et al. \u003cspan citationid=\"CR79\" class=\"CitationRef\"\u003e2001\u003c/span\u003e; C\u0026oacute;rdoba and Cocucci \u003cspan citationid=\"CR23\" class=\"CitationRef\"\u003e2011\u003c/span\u003e). The pollination dependency rate in this crop is considered to be modest from 10\u0026ndash;40%. This rate is set according to the effect of pollinators on the increase in crop production (Klein et al. \u003cspan citationid=\"CR62\" class=\"CitationRef\"\u003e2007\u003c/span\u003e; Giannini et al. \u003cspan citationid=\"CR44\" class=\"CitationRef\"\u003e2015a\u003c/span\u003e). However, recent results show that the pollination carried out by bees (pollination by buzzing) increases the productivity and quality of the tomato fruit (Gaglianone et al. \u003cspan citationid=\"CR37\" class=\"CitationRef\"\u003e2018\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eIn 2019, world tomato production was 37.38\u0026nbsp;million (M kg) (Tomato News Sas \u003cspan citationid=\"CR131\" class=\"CitationRef\"\u003e2020\u003c/span\u003e). In Brazil, Solanaceae is considered to be of great economic importance, with an annual production of 4.3 M kg, representing 57.4% of all the vegetables cultivated in the country (Instituto Brasileiro De Geografia E Estat\u0026iacute;stica \u0026ndash; IBGE 2019).\u003c/p\u003e \u003cp\u003eThe present study aimed to assess the effect of attractive flower strips on the regulation of environmental services by insects (pollination and biological control) in the tomato crop \u003cem\u003eS. lycopersicum\u003c/em\u003e. Thus, the following hypotheses were tested: (H1) the diversity of pollinator insects and natural enemies increases with the attractive flower strips of cilantro and sorghum in corn fields; and (H2) the production of tomato fruits increases according to the attractive flower strips of cilantro and sorghum.\u003c/p\u003e"},{"header":"MATERIALS AND METHODS","content":"\u003cdiv id=\"Sec3\" class=\"Section2\"\u003e \u003ch2\u003eStudy Area\u003c/h2\u003e \u003cp\u003eThe research was conducted on a rural property (15\u0026deg; 37\u0026rsquo; 38\u0026rsquo;\u0026rsquo; S 58\u0026deg; 10\u0026rsquo; 55\u0026rsquo;\u0026rsquo; W; 284 masl) in the municipality of S\u0026atilde;o Jos\u0026eacute; dos Quatro Marcos (Mato Grosso, Brazil). The rural property is in proximity to a remnant of secondary vegetation of 10.4 acres and cultivates species of tomato crop fields of different planting ages, banana (\u003cem\u003eMusa paradisiaca\u003c/em\u003e L.), cucumber (\u003cem\u003eCucumis sativus\u003c/em\u003e L.), and corn (\u003cem\u003eZea mays\u003c/em\u003e L.) in different flowering periods.\u003c/p\u003e \u003cp\u003eThe commercial tomato production used in our study corresponds to an autumn-winter planting, with an area of approximately 6.200 m\u0026sup2; and spacing of 1.25 m between rows and 1 meter between the plants (double rows of planting separated by 2.5 meters). The experimental parcel was 5 x 4 m, consisting of 16 tomato plants arranged in the experimental area of two treatment schemes: 1) tomato plants without attractive flower strips (control) and 2) tomato plants with attractive flower strips of cilantro and sorghum (Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e1\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eThe sample design was entirely randomized, consisting of 2 treatments: control (tomato plants without the attractive flower strips, T1-T5) and tomato plants with attractive flower strips (cilantro and sorghum, C1-C10) with 15 parcels, 5 repetitions for witness strips and 10 repetitions for the attractive flower strips. The parcels consisted of double rows of tomatoes, with 8 tomato plants per row, totaling 16 tomato plants per parcel (Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e1\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eThe cilantro row flourished before sorghum, and the two attractive species did not flower simultaneously. The cilantro was distributed among the tomato plant rows in the experimental parcel, 60 days after transplanting the tomato seedlings. Thus, we sowed the cilantro in a seedling tray with substrate, and after 7 days, we transplanted it into permanent pots that were distributed in the experimental area. Cilantro flowering occurred between 60 and 68 days after tomato transplantation.\u003c/p\u003e \u003cp\u003eThe graniferous sorghum was planted 48 days after transplanting the tomato seedlings to the study plot, to the border of the area, in a single strip with a line of 67 linear meters. Sorghum flowered between 72 and 80 days after the tomato transplant.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec4\" class=\"Section2\"\u003e \u003ch2\u003eSampling of pollinators and natural enemies\u003c/h2\u003e \u003cp\u003eThe sampling of the pollinator insects and natural enemies was carried out during the 8 days of the flowering period of the attractive flower strips. Two methods were used for sampling: active trapping (sweep netting) and passive trapping (pan traps, i.e., bee bowls). In the active trapping, the insects were sampled for 20 minutes in each parcel from 7:00 to 12:00 in the morning and captured with an entomological net. The total sampling effort was 40 hours at the end of the 8 days of sampling. The trap used was the bee bowl (BB), according to the methodology adapted from Wheelock and O\u0026rsquo;Neal (\u003cspan citationid=\"CR136\" class=\"CitationRef\"\u003e2016\u003c/span\u003e), which allocated 1 bee bowl per parcel.\u003c/p\u003e \u003cp\u003eTo collect natural enemies and pollinators together, the traps were installed every 2 days within the 8-day period for active sampling. The sampling of the insects occurred at two moments, the first from 60 to 68 days of tomato transplantation when the cilantro was flowering, and the second moment from 72 to 80 days of tomato transplantation when the sorghum was flowering. The collected insects were identified at the family level with the assistance of taxonomic identification keys and at the morph types. The insects were assigned to one of the following functional groups as \u0026ldquo;pollinators or natural enemies\u0026rdquo; based on specific literature (Rosas-Ramos et al. \u003cspan citationid=\"CR104\" class=\"CitationRef\"\u003e2019\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eTo evaluate the tomato production within the parcel, 8 tomato plants were evaluated per parcel. The green and ripe tomato fruits were harvested 90 days after transplantation of the tomato seedlings and weighed with an electronic balance.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec5\" class=\"Section2\"\u003e \u003ch2\u003eStatistical Analysis\u003c/h2\u003e \u003cp\u003eThe generalized linear model (GLM) was used to model the number of beneficial insects (richness and abundance of pollinators and natural enemies) as a function of the attractive flower strip using the Poisson, Quasipoisson, or binomial negative distribution errors. The overdispersion, Q-Q plots, and Akaike's criterion (AIC) of each model were evaluated, and the better error function distribution was chosen.\u003c/p\u003e \u003cp\u003eThe explanatory variable (x) was composed of two levels, 1. tomato plants without an attractive flower strip (control) and 2. tomato plants with an attractive flower strip, and the response variables (y) were pollinator richness, pollinator abundance, richness of natural enemies, and abundance of natural enemies.\u003c/p\u003e \u003cp\u003eThe analyses were separated by the flowering time of each species of attractive flower strips, according to the flowering period, first for cilantro and second for sorghum. Therefore, the analysis of the variable responses was carried out in three different periods, corresponding to the effect of cilantro flowering from 60 to 68 days after tomato transplanting; the sorghum flowering strips from 72 to 80 days of tomato transplanting; and the sum of the richness in the two flowering periods (mix of cilantro flower and sorghum), for which the total richness denomination was used. Likewise, the total abundance was analyzed using the sum of the sampled insects in the two flowering periods (mix of flower cilantro and sorghum). This analysis was made from the sum of the morph types of insects in the attractive flower strips of cilantro and sorghum.\u003c/p\u003e \u003cp\u003eTo verify the hypothesis that the diversity of pollinator insects and natural enemies increases with the proximity of the corn field, which was in a productive phase during the study period, an F test was used. In the statistical model, the variable (x) was composed of the distance between the parcels of the tomato plant area and the corn field, and the variable response (y) was the richness in the pollinators. The same model was used for the other variable responses, such as the abundance of pollinators, the richness of natural enemies, and the abundance of natural enemies. This analysis was done because the corn field is located between the tomato field of the experiment and the fragment of native vegetation (Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e1\u003c/span\u003e). Therefore, it was possible to verify whether corn attracted the insect pollinators and natural enemies to the tomato plants or was a barrier between the tomato plants and the fragment of native vegetation.\u003c/p\u003e \u003cp\u003eJaccard similarity indices were used to compare associations between absence/presence data of insect and treatment (1. flower strips of cilantro, 2. flower strips of sorghum, and 3. without attractive flower strips - control). The indices ranged from 0 (no similarity) to 1 (identity) and were used in the free program PAST-Paleontological Statistics.\u003c/p\u003e \u003cp\u003eFurthermore, to verify the relationship between the production of tomato fruits and the surrounding tomato plants and the diversity of the pollinator insects, multiple regression was used, with tomato production (kg) as the variable response (y). The explanatory variables were surrounding the tomato (x1) (1. without attractive flower strips and 2. with attractive flower strips of cilantro and sorghum), total richness of the pollinator morphotypes (x2), and total abundance of the pollinators (x3), in addition to the interaction between x1:x2 and x1:x3. The same model was used to verify whether there was a contribution from the natural enemies to the production of the tomato fruits. The analysis procedure was backward, and the model was simplified by removing the nonsignificant variables with an F test required to be below 5%.\u003c/p\u003e \u003cp\u003eStatistical models were applied to critically appraise the final model with model-checking plots. All analyses were fitted in R (R Core Team 2019). The normality test was applied to verify the adjustment of the response variable to the distribution of errors.\u003c/p\u003e \u003c/div\u003e"},{"header":"RESULTS","content":"\u003cp\u003eThe abundance of the sampled morph types was 216 insects distributed in 6 orders and 31 families. Among the pollinators, orders Diptera, Coleoptera, and Hymenoptera were identified. Order Hymenoptera was the most abundant (49.15%), represented mainly by bees from the Apidae family.\u003c/p\u003e \u003cp\u003eDiptera was the most abundant order of the natural enemies sampled (18. 9%), represented mainly by flies Syrphidae and Tachinidae, followed by order Hymenoptera (7. 9%), Coleoptera (3. 2%), Odonata (1. 8%), and Neuroptera (0.5%). From the 31 families identified, 15 were classified as pollinators, 9 as natural enemies, and 7 as pollinators and natural enemies (Table\u0026nbsp;\u003cspan refid=\"Tab1\" class=\"InternalRef\"\u003e1\u003c/span\u003e).\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab1\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 1\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003eInsects identified after active trapping (sweep netting and pan traps) in an experimental tomato crop field in southwestern Mato Grosso State. In the attractive flower strips: 1) Control (without stripe), 2) With cilantro flower stripe, and 3) With sorghum flower stripe.\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"6\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c4\" colnum=\"4\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c5\" colnum=\"5\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c6\" colnum=\"6\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\"\u003e \u003cp\u003eFamily\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c2\"\u003e \u003cp\u003eAttractive flower strips\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c3\"\u003e \u003cp\u003eFunctional groups\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c4\"\u003e \u003cp\u003eN\u0026ordm;\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c5\"\u003e \u003cp\u003e%\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c6\"\u003e \u003cp\u003eReference\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eDiptera\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eSyrphidae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e1,2,3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003ePollinator/Predator\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e16\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e5.9\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e(Morales and K\u0026ouml;hler \u003cspan citationid=\"CR78\" class=\"CitationRef\"\u003e2006\u003c/span\u003e)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eStratiomyidae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e1,2,3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003ePollinator\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e4\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e1.5\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e(Roig-Ju\u0026ntilde;ent et al. \u003cspan citationid=\"CR102\" class=\"CitationRef\"\u003e2015\u003c/span\u003e)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eHermetia illucens\u003c/em\u003e (L.)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e1,2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003ePollinator\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e(Pujol-Luz, JR and Pujol-Luz CVA 2014)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eHermetia albitarsis\u003c/em\u003e (Fabricius)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003ePollinator\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e(Cusser et al. \u003cspan citationid=\"CR24\" class=\"CitationRef\"\u003e2015\u003c/span\u003e)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eSargus fasciatus\u003c/em\u003e (Valenciennes)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003ePollinator\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e(Pujol-Luz, JR and Pujol-Luz CVA 2014)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eTachinidae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e1,2,3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eParasitoid\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e16\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e5.9\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e(De Groot et al. \u003cspan citationid=\"CR26\" class=\"CitationRef\"\u003e2007\u003c/span\u003e)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eBombyliidae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003ePollinator/ Parasitoide/ Predator\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e6\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e2.2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e(Deyrup MA \u003cspan citationid=\"CR30\" class=\"CitationRef\"\u003e1988\u003c/span\u003e; Koptur et al. \u003cspan citationid=\"CR64\" class=\"CitationRef\"\u003e2013\u003c/span\u003e; Oliveira and Maruyama \u003cspan citationid=\"CR87\" class=\"CitationRef\"\u003e2014\u003c/span\u003e; Van Herk et al. \u003cspan citationid=\"CR134\" class=\"CitationRef\"\u003e2015\u003c/span\u003e; Barbosa et al. \u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e2016\u003c/span\u003e)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eTachinidae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e1,2,3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eParasitoid\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e16\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e5.9\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e(De Groot et al. \u003cspan citationid=\"CR26\" class=\"CitationRef\"\u003e2007\u003c/span\u003e)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eBombyliidae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003ePollinator/ Parasitoide/ Predator\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e6\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e2.2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\" morerows=\"3\" rowspan=\"4\"\u003e \u003cp\u003e(Deyrup MA \u003cspan citationid=\"CR30\" class=\"CitationRef\"\u003e1988\u003c/span\u003e; Koptur et al. \u003cspan citationid=\"CR64\" class=\"CitationRef\"\u003e2013\u003c/span\u003e; Oliveira and Maruyama \u003cspan citationid=\"CR87\" class=\"CitationRef\"\u003e2014\u003c/span\u003e; Van Herk et al. \u003cspan citationid=\"CR134\" class=\"CitationRef\"\u003e2015\u003c/span\u003e; Barbosa et al. \u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e2016\u003c/span\u003e)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003ePoecilognathus\u003c/em\u003e spp. (Jaenicke)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003ePollinator\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eVilla\u003c/em\u003e spp. (Lioy)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eParasitoid\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eCeratopogonidae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003ePollinator/ Ectoparasite\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e0.4\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eAsilidae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003ePollinator/ Predator\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e0.4\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\" morerows=\"2\" rowspan=\"3\"\u003e \u003cp\u003e(Berti Filho and Macedo \u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e2011\u003c/span\u003e;; Kohler et al. \u003cspan citationid=\"CR63\" class=\"CitationRef\"\u003e2013\u003c/span\u003e; Koptur et al. \u003cspan citationid=\"CR64\" class=\"CitationRef\"\u003e2013\u003c/span\u003e; Wolowski et al. \u003cspan citationid=\"CR139\" class=\"CitationRef\"\u003e2019\u003c/span\u003e)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eMallophora calida\u003c/em\u003e (Fabricius)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003ePredator\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eTabanidae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003ePollinator/Parasitoid\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e0.4\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eChrysops variegatus\u003c/em\u003e (De Geer)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003ePollinator\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e(Tamayo-Cen \u003cspan citationid=\"CR123\" class=\"CitationRef\"\u003e2020\u003c/span\u003e)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eColeoptera\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eScarabaeidae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e1,2,3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003ePollinator\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e9\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e3.3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003e(Paulino-Neto \u003cspan citationid=\"CR91\" class=\"CitationRef\"\u003e2014\u003c/span\u003e)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eCrysomelidae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e1,2,3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003ePollinator\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e13\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e4.8\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eCoccinellidae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e2,3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003ePollinator/Predator\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e4\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e1.5\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e(Berti Filho and Macedo \u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e2011\u003c/span\u003e; Wolowski et al. \u003cspan citationid=\"CR139\" class=\"CitationRef\"\u003e2019\u003c/span\u003e)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eCarabidae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e1,3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003ePredator\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e1.1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e(Berti Filho and Macedo \u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e2011\u003c/span\u003e)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eTenebrionidae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003ePollinator\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e0.4\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003e(Witt et al. \u003cspan citationid=\"CR138\" class=\"CitationRef\"\u003e2004\u003c/span\u003e; Paulino-Neto \u003cspan citationid=\"CR91\" class=\"CitationRef\"\u003e2014\u003c/span\u003e)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eCurculinonidae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003ePollinator\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e0.4\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eCerambycidae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003ePollinator\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e0.4\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e(Wolowski et al. \u003cspan citationid=\"CR139\" class=\"CitationRef\"\u003e2019\u003c/span\u003e)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eElateridae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003ePollinator\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e0.4\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e(Paulino-Neto \u003cspan citationid=\"CR91\" class=\"CitationRef\"\u003e2014\u003c/span\u003e)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eHemiptera\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eScutelleridae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e1,2,3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003ePollinator\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e8\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e2.9\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e(Berti Filho and Macedo \u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e2011\u003c/span\u003e; Wolowski et al. \u003cspan citationid=\"CR139\" class=\"CitationRef\"\u003e2019\u003c/span\u003e)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eReduviidae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003ePredator\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e0.4\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e(Berti Filho and Macedo \u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e2011\u003c/span\u003e)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eCoreidae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e1,3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003ePollinator\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e0.7\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e(Wolowski et al. \u003cspan citationid=\"CR139\" class=\"CitationRef\"\u003e2019\u003c/span\u003e)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eHymenoptera\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eApidae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e1,2,3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003ePollinator\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e95\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e35.1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e(Oliveira and Maruyama \u003cspan citationid=\"CR87\" class=\"CitationRef\"\u003e2014\u003c/span\u003e)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eApis mellifera\u003c/em\u003e (Linnaeus, 1758)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003ePolinizador\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e(Santos et al. \u003cspan citationid=\"CR109\" class=\"CitationRef\"\u003e2014\u003c/span\u003e; Giannini et al. 2015; Vin\u0026iacute;cius-Silva et al. \u003cspan citationid=\"CR135\" class=\"CitationRef\"\u003e2017\u003c/span\u003e; Toni et al. 2021)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eEuglossa (Euglossa) carolina\u003c/em\u003e (Nem\u0026eacute;sio, 2009)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003ePotencial Polinizador\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e(Depr\u0026aacute; et al. \u003cspan citationid=\"CR28\" class=\"CitationRef\"\u003e2014\u003c/span\u003e)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eBombus (Thoracobombus) brevivillus\u003c/em\u003e (Franklin, 1913)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003ePolinizador\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e(De Luca and Vallejo-Marin 2013)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eTetragona clavipes\u003c/em\u003e (Fabricius, 1804)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eVisitante floral\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e(Silva-Neto et al. \u003cspan citationid=\"CR116\" class=\"CitationRef\"\u003e2017\u003c/span\u003e)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eFrieseomelitta varia\u003c/em\u003e (Lepeletier, 1836)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eVisitante floral\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e. (Silva-Neto et al. \u003cspan citationid=\"CR116\" class=\"CitationRef\"\u003e2017\u003c/span\u003e; Vin\u0026iacute;cius-Silva et al. \u003cspan citationid=\"CR135\" class=\"CitationRef\"\u003e2017\u003c/span\u003e)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eTrigona dallatorreana\u003c/em\u003e (Friese, 1900)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003ePolinizador\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e(Santos et al. \u003cspan citationid=\"CR109\" class=\"CitationRef\"\u003e2014\u003c/span\u003e; Vin\u0026iacute;cius-Silva et al. \u003cspan citationid=\"CR135\" class=\"CitationRef\"\u003e2017\u003c/span\u003e)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eOxytrigona aff. flaveola\u003c/em\u003e (Friese, 1900)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e?\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e-\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eCeratina (Calloceratina) chloris\u003c/em\u003e (Fabricius, 1804)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e?\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e-\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eFlorilegus (Euflorilegus) aff. affinis\u003c/em\u003e (Urban, 1970)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e?\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e-\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eVespidae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e1,2,3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003ePollinator/Predator\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e12\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e4.4\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e( Berti Filho and Macedo \u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e2011\u003c/span\u003e; Oliveira and Maruyama \u003cspan citationid=\"CR87\" class=\"CitationRef\"\u003e2014\u003c/span\u003e)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eHalictidae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e2,3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003ePollinator\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e0.7\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e( Berti Filho and Macedo \u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e2011\u003c/span\u003e; Oliveira and Maruyama \u003cspan citationid=\"CR87\" class=\"CitationRef\"\u003e2014\u003c/span\u003e)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eAugochloropsis\u003c/em\u003e sp. 22\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003ePolinizador\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e(Teppner \u003cspan citationid=\"CR124\" class=\"CitationRef\"\u003e2005\u003c/span\u003e; Vin\u0026iacute;cius-Silva et al. \u003cspan citationid=\"CR135\" class=\"CitationRef\"\u003e2017\u003c/span\u003e)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eMegachilidae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e1,2,3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003ePollinator\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e4\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e1.5\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e( Berti Filho and Macedo \u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e2011\u003c/span\u003e; Oliveira and Maruyama \u003cspan citationid=\"CR87\" class=\"CitationRef\"\u003e2014\u003c/span\u003e)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eMegachile (Sayapis)\u003c/em\u003e sp. 1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003ePolinizador\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e(Teppner \u003cspan citationid=\"CR124\" class=\"CitationRef\"\u003e2005\u003c/span\u003e; Vin\u0026iacute;cius-Silva et al. \u003cspan citationid=\"CR135\" class=\"CitationRef\"\u003e2017\u003c/span\u003e)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eMegachile (Leptorachis)\u003c/em\u003e sp. 1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003ePolinizador\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e(Teppner \u003cspan citationid=\"CR124\" class=\"CitationRef\"\u003e2005\u003c/span\u003e; Vin\u0026iacute;cius-Silva et al. \u003cspan citationid=\"CR135\" class=\"CitationRef\"\u003e2017\u003c/span\u003e)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eAndrenidae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003ePollinator\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e0.7\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e( Berti Filho and Macedo \u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e2011\u003c/span\u003e; Oliveira and Maruyama \u003cspan citationid=\"CR87\" class=\"CitationRef\"\u003e2014\u003c/span\u003e)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eOxaea flavescens\u003c/em\u003e (Klug, 1807)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003ePotencial Polinizador\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e(Depr\u0026aacute; et al. \u003cspan citationid=\"CR28\" class=\"CitationRef\"\u003e2014\u003c/span\u003e; Santos et al. \u003cspan citationid=\"CR109\" class=\"CitationRef\"\u003e2014\u003c/span\u003e; Silva-Neto et al. \u003cspan citationid=\"CR116\" class=\"CitationRef\"\u003e2017\u003c/span\u003e; Vin\u0026iacute;cius-Silva et al. \u003cspan citationid=\"CR135\" class=\"CitationRef\"\u003e2017\u003c/span\u003e)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eMellitidae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003ePollinator\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e0.4\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e(Castro and Singer \u003cspan citationid=\"CR21\" class=\"CitationRef\"\u003e2019\u003c/span\u003e)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eFormicidae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003ePollinator\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e0.7\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e(G\u0026oacute;mez and Zamora \u003cspan citationid=\"CR46\" class=\"CitationRef\"\u003e1992\u003c/span\u003e)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eEvaniidae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e2,3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eParasitoid\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e0.7\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003e(Berti Filho and Macedo \u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e2011\u003c/span\u003e)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eIchneumonidae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eParasitoid\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e1.1\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eOdonata\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eCoenagrionidae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003ePredator\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e0.7\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e(Siregar et al. \u003cspan citationid=\"CR118\" class=\"CitationRef\"\u003e2016\u003c/span\u003e)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eLibellulidae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e1,2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003ePredator\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e0.7\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e(Gorayeb and Pinger \u003cspan citationid=\"CR48\" class=\"CitationRef\"\u003e1978\u003c/span\u003e)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eNeuroptera\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eChrysopidae\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003ePredator\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e0.4\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e \u003cp\u003e(Berti Filho and Macedo \u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e2011\u003c/span\u003e)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eTotal\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e216\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e100%\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c6\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003ctfoot\u003e \u003ctr\u003e\u003ctd colspan=\"6\"\u003eSource: Ladeia, 2021\u003c/td\u003e\u003c/tr\u003e \u003c/tfoot\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003cp\u003eIn the tomato plants without attractive flower strips (control), 43 insects (15.93%) were sampled; in the tomato plants with attractive flower strips of cilantro, 105 insects (38.89%) were sampled; and 122 insects (45.18%) were sampled in the treatment with attractive flower strips of sorghum. The similarities between the families of the beneficial insects (pollinators and natural enemies) in the cilantro flower strips and in the control were more homogeneous than the insect similarity in the sorghum flower strips (Fig.\u0026nbsp;\u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e2\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eDuring the flowering of cilantro, the pollinator insect and natural enemies in the tomato plants without the attractive flower strips did not differ from the tomato plants with the strips, both for richness of morph types (X\u003csup\u003e2\u003c/sup\u003e\u0026thinsp;=\u0026thinsp;4.33, N\u0026thinsp;=\u0026thinsp;8, p\u0026thinsp;=\u0026thinsp;0.09) and abundance of natural enemies (X\u003csup\u003e2\u003c/sup\u003e\u0026thinsp;=\u0026thinsp;4.33, N\u0026thinsp;=\u0026thinsp;8, p\u0026thinsp;=\u0026thinsp;0.09). The absence of the effect of the cilantro strip was observed for the pollinator insects, where no difference was found for the richness of morph types (X\u003csup\u003e2\u003c/sup\u003e\u0026thinsp;=\u0026thinsp;1.25, N\u0026thinsp;=\u0026thinsp;11, p\u0026thinsp;=\u0026thinsp;0.34), and for an abundance of pollinating insects, there was also no difference (X\u003csup\u003e2\u003c/sup\u003e\u0026thinsp;=\u0026thinsp;3.86, N\u0026thinsp;=\u0026thinsp;11, p\u0026thinsp;=\u0026thinsp;0.19) with an increase in coriander flower strips in relation to the control.\u003c/p\u003e \u003cp\u003eIn sorghum flowering, natural enemies did not differ between tomato plants without strips of attractive flowers and tomato plants with strips, both for richness (X\u003csup\u003e2\u003c/sup\u003e\u0026thinsp;=\u0026thinsp;2.36, N\u0026thinsp;=\u0026thinsp;11, p\u0026thinsp;=\u0026thinsp;0.14) and abundance (X\u003csup\u003e2\u003c/sup\u003e\u0026thinsp;=\u0026thinsp;2.36, N\u0026thinsp;=\u0026thinsp;11, p\u0026thinsp;=\u0026thinsp;0.12). For pollinators, the morph-type richness was two times higher in the tomato plants with attractive flower strips of sorghum than in the tomato plants without the strips (with sorghum strips\u0026thinsp;=\u0026thinsp;5.56, control\u0026thinsp;=\u0026thinsp;2.5, X\u0026sup2;=6.28, N\u0026thinsp;=\u0026thinsp;11, p\u0026thinsp;=\u0026thinsp;0.04) (Fig.\u0026nbsp;\u003cspan refid=\"Fig4\" class=\"InternalRef\"\u003e3\u003c/span\u003ea).\u003c/p\u003e \u003cp\u003eThe abundance of the pollinating insects was three times higher in tomato plants with attractive strips of sorghum than in tomato plants without strips (with sorghum strips\u0026thinsp;=\u0026thinsp;10.67, control\u0026thinsp;=\u0026thinsp;3.5, X\u0026sup2;=4.94, N\u0026thinsp;=\u0026thinsp;11, p\u0026thinsp;=\u0026thinsp;0.02) (Fig.\u0026nbsp;\u003cspan refid=\"Fig4\" class=\"InternalRef\"\u003e3\u003c/span\u003eb).\u003c/p\u003e \u003cp\u003eThe effect of the two attractive flower strips intercropped (with mixed strips of cilantro and sorghum) increased the total abundance of natural enemies by more than three times in the tomato plants with strips of cilantro and sorghum compared to the tomato plants without the strips (mix of cilantro and sorghum\u0026thinsp;=\u0026thinsp;6.56, control\u0026thinsp;=\u0026thinsp;2.6, Χ2\u0026thinsp;=\u0026thinsp;7.16, N\u0026thinsp;=\u0026thinsp;12, p\u0026thinsp;=\u0026thinsp;0.007) (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e4\u003c/span\u003ea). The same effect was observed for the total richness of natural enemies (mix of cilantro and sorghum\u0026thinsp;=\u0026thinsp;6.44, control\u0026thinsp;=\u0026thinsp;2.4, Χ\u0026sup2;=7.91, N\u0026thinsp;=\u0026thinsp;12, p\u0026thinsp;=\u0026thinsp;0.005) (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e4\u003c/span\u003eb). The total abundance of pollinators was three times higher in the mix of cilantro and sorghum than in the control (mix of cilantro and sorghum\u0026thinsp;=\u0026thinsp;17.1, control\u0026thinsp;=\u0026thinsp;5.8, Χ\u0026sup2;=35.81, N\u0026thinsp;=\u0026thinsp;12, p\u0026thinsp;=\u0026thinsp;0.02) (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e4\u003c/span\u003ec). The mix of cilantro flower and sorghum increased the total richness of morph types by two times (mix of cilantro and sorghum\u0026thinsp;=\u0026thinsp;10.4, control\u0026thinsp;=\u0026thinsp;4.8, Χ\u0026sup2;=13.29, N\u0026thinsp;=\u0026thinsp;12, p\u0026thinsp;=\u0026thinsp;0.03) (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e4\u003c/span\u003ed).\u003c/p\u003e \u003cp\u003eThe diversity of natural enemy insects increased with the distance from the corn field, which was observed for the morph type richness (p\u0026thinsp;=\u0026thinsp;0.02, N\u0026thinsp;=\u0026thinsp;12, r\u0026sup2;=0.37) (Fig.\u0026nbsp;\u003cspan refid=\"Fig5\" class=\"InternalRef\"\u003e5\u003c/span\u003ea) and abundance (p\u0026thinsp;=\u0026thinsp;0.03, N\u0026thinsp;=\u0026thinsp;12, r\u0026sup2;=0.33) (Fig.\u0026nbsp;\u003cspan refid=\"Fig5\" class=\"InternalRef\"\u003e5\u003c/span\u003eb). The distance from the corn field ,when combined with the attractive flower strips, had no effect on natural enemies or the interactions (corn field distance * attractive flower strips/species richness p\u0026thinsp;=\u0026thinsp;0.4 and abundance p\u0026thinsp;=\u0026thinsp;0.5). For the pollinators, the morph-type richness increased with distance from the corn field (p\u0026thinsp;=\u0026thinsp;0.004, N\u0026thinsp;=\u0026thinsp;12, r\u0026sup2;=0.50) (Fig.\u0026nbsp;\u003cspan refid=\"Fig5\" class=\"InternalRef\"\u003e5\u003c/span\u003ec), as did the abundance (p\u0026thinsp;=\u0026thinsp;0.003, N\u0026thinsp;=\u0026thinsp;12, r\u0026sup2;=0.53) (Fig.\u0026nbsp;\u003cspan refid=\"Fig5\" class=\"InternalRef\"\u003e5\u003c/span\u003ed). The interactions of the corn field distance and the attractive strips were not significant (corn field distance * attractive flower strips/species richness p\u0026thinsp;=\u0026thinsp;0.48 and abundance p\u0026thinsp;=\u0026thinsp;0.38).\u003c/p\u003e \u003cp\u003eTomato production was not influenced by the use of attractive flower strips (mix of cilantro flowers and sorghum; p\u0026thinsp;=\u0026thinsp;0.26) in consortium with tomato plants or by the diversity of natural enemies (total morph-type richness with strips\u0026thinsp;=\u0026thinsp;7\u0026thinsp;\u0026plusmn;\u0026thinsp;3.68, control\u0026thinsp;=\u0026thinsp;2\u0026thinsp;\u0026plusmn;\u0026thinsp;1.14, p\u0026thinsp;=\u0026thinsp;0.46, N\u0026thinsp;=\u0026thinsp;8 and total abundance with strips\u0026thinsp;=\u0026thinsp;7\u0026thinsp;\u0026plusmn;\u0026thinsp;3.75, control\u0026thinsp;=\u0026thinsp;3 \u0026plusmn;\u0026thinsp;1.14, p\u0026thinsp;=\u0026thinsp;0.13, N\u0026thinsp;=\u0026thinsp;8). The diversity of pollinators did not influence tomato production (total morph-type richness with strips\u0026thinsp;=\u0026thinsp;10\u0026thinsp;\u0026plusmn;\u0026thinsp;4.39, control\u0026thinsp;=\u0026thinsp;3\u0026thinsp;\u0026plusmn;\u0026thinsp;3.63, p\u0026thinsp;=\u0026thinsp;0.64, N\u0026thinsp;=\u0026thinsp;8 and total abundance with strips\u0026thinsp;=\u0026thinsp;15\u0026thinsp;\u0026plusmn;\u0026thinsp;9.77, control\u0026thinsp;=\u0026thinsp;5\u0026thinsp;\u0026plusmn;\u0026thinsp;5.26, p\u0026thinsp;=\u0026thinsp;0.52, N\u0026thinsp;=\u0026thinsp;8), and the surroundings did not show an effect (p\u0026thinsp;=\u0026thinsp;0.34) when combined with the pollinators. The diversity of pollinators did not influence tomato production (total morph-type richness with strips\u0026thinsp;=\u0026thinsp;10\u0026thinsp;\u0026plusmn;\u0026thinsp;4.39, control\u0026thinsp;=\u0026thinsp;3\u0026thinsp;\u0026plusmn;\u0026thinsp;3.63, p\u0026thinsp;=\u0026thinsp;0.64, N\u0026thinsp;=\u0026thinsp;8 and total abundance with strips\u0026thinsp;=\u0026thinsp;15\u0026thinsp;\u0026plusmn;\u0026thinsp;9.77, control\u0026thinsp;=\u0026thinsp;5\u0026thinsp;\u0026plusmn;\u0026thinsp;5.26,p\u0026thinsp;=\u0026thinsp;0.52, N\u0026thinsp;=\u0026thinsp;8), and the surroundings did not show an effect (p\u0026thinsp;=\u0026thinsp;0.34) when combined with the pollinators.\u003c/p\u003e"},{"header":"DISCUSSION","content":"\u003cp\u003eThe working hypothesis was that the consortium of tomato plants with cilantro and sorghum contributes to the increase in the abundance and richness of pollinator insects and natural enemies. In our tomato study, the hypothesis was accepted for the richness of pollinators due to sorghum and the abundance of natural enemies when using cilantro together with the crop planting. The heterogeneity of agricultural landscapes provides complementary resources over time and space, such as food resources and nesting sites, which consequently increase the richness and abundance of pollinator insects and natural enemies (Nicholls and Altieri \u003cspan citationid=\"CR82\" class=\"CitationRef\"\u003e2012\u003c/span\u003e; Karamaouna et al. \u003cspan citationid=\"CR58\" class=\"CitationRef\"\u003e2019\u003c/span\u003e; Aguilera et al. \u003cspan citationid=\"CR2\" class=\"CitationRef\"\u003e2020\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eFood resources are offered to floral visitors through nectar, pollen, oils, and floral fabrics of plants. Pollen is used by pollinator species as a source of lipids, proteins, carbohydrates, and minerals (Agostini et al. 2014), and nectar is an energy source for worker bees and the queen (Roulston and Cane \u003cspan citationid=\"CR106\" class=\"CitationRef\"\u003e2000\u003c/span\u003e). Species of Solanacea, such as tomato \u003cem\u003eS. lycopersicum\u003c/em\u003e, are an important source of pollen, especially for species that perform \u0026ldquo;pollination by buzzing\u0026rdquo; (Nunes-Silva et al. \u003cspan citationid=\"CR85\" class=\"CitationRef\"\u003e2013\u003c/span\u003e; Santos et al. \u003cspan citationid=\"CR109\" class=\"CitationRef\"\u003e2014\u003c/span\u003e; Silva-Neto et al. \u003cspan citationid=\"CR116\" class=\"CitationRef\"\u003e2017\u003c/span\u003e; Vin\u0026iacute;cius-Silva et al. \u003cspan citationid=\"CR135\" class=\"CitationRef\"\u003e2017\u003c/span\u003e). A diverse group of flower species with different phenologies increases the stability of resources for pollinators and, therefore, increases pollination services (Bl\u0026uuml;thgen and Klein \u003cspan citationid=\"CR17\" class=\"CitationRef\"\u003e2011\u003c/span\u003e; Mandelik et al. \u003cspan citationid=\"CR71\" class=\"CitationRef\"\u003e2012\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eThe effect of the diversification of cilantro and sorghum attractive flower strips in tomato plants contributed to the total abundance of natural enemies, confirming that the management of landscape diversity has the potential to maintain or increase biological control services (Gardiner et al. \u003cspan citationid=\"CR38\" class=\"CitationRef\"\u003e2009\u003c/span\u003e). This event indicates that an arrangement with non-agricultural species on a different special scale is a solution that improves the biological control of agricultural pests (Gagic et al. \u003cspan citationid=\"CR36\" class=\"CitationRef\"\u003e2018\u003c/span\u003e). In fact, cilantro is considered an aromatic plant, which in addition to the floral resource available in the system can attract natural enemies through volatile constituent substances (Salamanca et al. \u003cspan citationid=\"CR108\" class=\"CitationRef\"\u003e2018\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eSimilar results of the increase in the abundance of natural enemies in attractive flower strips of cilantro in tomato crops have been found in previous studies with eggplant crops (Patt and Lashomb \u003cspan citationid=\"CR90\" class=\"CitationRef\"\u003e1997\u003c/span\u003e), buckwheat (Pi\u0026ntilde;ero and Manandhar \u003cspan citationid=\"CR93\" class=\"CitationRef\"\u003e2015\u003c/span\u003e), rose (Salamanca et al. \u003cspan citationid=\"CR107\" class=\"CitationRef\"\u003e2015\u003c/span\u003e), cabbage (Morris and Li \u003cspan citationid=\"CR80\" class=\"CitationRef\"\u003e2000\u003c/span\u003e; Silva; et al. \u003cspan citationid=\"CR117\" class=\"CitationRef\"\u003e2016\u003c/span\u003e), carrot (Jankowska and Wojciechowicz-Zytko \u003cspan citationid=\"CR56\" class=\"CitationRef\"\u003e2016\u003c/span\u003e), bean (Salamanca et al. \u003cspan citationid=\"CR108\" class=\"CitationRef\"\u003e2018\u003c/span\u003e), and olive (Karamaouna et al. \u003cspan citationid=\"CR58\" class=\"CitationRef\"\u003e2019\u003c/span\u003e). The natural odors emitted by aromatic plants influence the foraging and behavior of pollinators and natural enemies (Kessler and Baldwin \u003cspan citationid=\"CR60\" class=\"CitationRef\"\u003e2006\u003c/span\u003e; Kessler and Halitschke \u003cspan citationid=\"CR59\" class=\"CitationRef\"\u003e2007\u003c/span\u003e; Chen \u003cspan citationid=\"CR22\" class=\"CitationRef\"\u003e2008\u003c/span\u003e; Heil \u003cspan citationid=\"CR52\" class=\"CitationRef\"\u003e2008\u003c/span\u003e; Raguso \u003cspan citationid=\"CR98\" class=\"CitationRef\"\u003e2008\u003c/span\u003e). These aromatic plants can attract, through volatile compounds, general natural enemies capable of controlling populations of insect pests (Togni et al. \u003cspan citationid=\"CR129\" class=\"CitationRef\"\u003e2016\u003c/span\u003e). Cilantro is an aromatic plant capable of attracting a greater number of natural enemies when flowering (Medeiros et al. \u003cspan citationid=\"CR74\" class=\"CitationRef\"\u003e2009\u003c/span\u003e; Togni et al. \u003cspan citationid=\"CR128\" class=\"CitationRef\"\u003e2009\u003c/span\u003e). These volatile compounds emitted by cilantro increase the attractiveness of generalist predators, such as the ladybug \u003cem\u003eCycloneda sanguinea\u003c/em\u003e (Linnaeus) (Coccinellidae), as well as serving as oviposition sites for these insects. In this study, Coccinellidae were the most frequent predators among the beetles. In addition, the insertion of cilantro strips increases the efficiency of land use and provides extra income to the farmer (Resende et al. \u003cspan citationid=\"CR100\" class=\"CitationRef\"\u003e2010\u003c/span\u003e; Medeiros et al. \u003cspan citationid=\"CR75\" class=\"CitationRef\"\u003e2011\u003c/span\u003e; Togni et al. \u003cspan citationid=\"CR129\" class=\"CitationRef\"\u003e2016\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eKeeping natural enemies abundant within a cultivation system can reduce the frequency with which some pests reach the level of action (Garratt et al. \u003cspan citationid=\"CR41\" class=\"CitationRef\"\u003e2017\u003c/span\u003e). In our study, Syrphidae and Tachinidae were the most abundant families of natural enemies. Flies of the Syrphidae family are important predators for pest management; their larvae feed on aphids and thrips that infest many agricultural species (Rojo and Marcos-Garc\u0026iacute;a \u003cspan citationid=\"CR103\" class=\"CitationRef\"\u003e1997\u003c/span\u003e) and specifically tomato crops (Abro et al. \u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e2019\u003c/span\u003e). Aphids and thrips are considered severe pests to tomato plants due to the transmission of the virus (Miranda et al. \u003cspan citationid=\"CR76\" class=\"CitationRef\"\u003e1998\u003c/span\u003e). The Tachinidae family has groups of parasitic flies that are important for the management of pest populations, particularly coleopterous and lepidopterous populations (Stireman et al. \u003cspan citationid=\"CR120\" class=\"CitationRef\"\u003e2006\u003c/span\u003e), as well as caterpillar \u003cem\u003eHelicoverpa zea\u003c/em\u003e (Boddie) (Farrar et al. \u003cspan citationid=\"CR33\" class=\"CitationRef\"\u003e1992\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eThe attractive flower of sorghum together with cilantro was responsible for increasing the total abundance of natural enemies in tomato cultivation. Sorghum was used as a trap crop (Gordon et al. \u003cspan citationid=\"CR49\" class=\"CitationRef\"\u003e2017\u003c/span\u003e); this terminology is used to define species that are used to attract, deflect, and intercept pest insects to decrease the damage to the main crop (Shelton and Badenes-Perez \u003cspan citationid=\"CR114\" class=\"CitationRef\"\u003e2006\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eSorghum is an efficient trap crop for reducing the management of phytophagous stink bugs in cotton crops (Tillman \u003cspan citationid=\"CR125\" class=\"CitationRef\"\u003e2006\u003c/span\u003e), tomato (Majumdar et al. \u003cspan citationid=\"CR70\" class=\"CitationRef\"\u003e2012\u003c/span\u003e; Gordon et al. \u003cspan citationid=\"CR49\" class=\"CitationRef\"\u003e2017\u003c/span\u003e), organic gardens (Nielsen et al. \u003cspan citationid=\"CR83\" class=\"CitationRef\"\u003e2016\u003c/span\u003e), and bell pepper (Blaauw et al. \u003cspan citationid=\"CR16\" class=\"CitationRef\"\u003e2017\u003c/span\u003e). In cotton, the use of sorghum trap crops helped to control of \u003cem\u003eHelicoverpa armigera\u003c/em\u003e (H\u0026uuml;bner) (Prakasha et al. \u003cspan citationid=\"CR95\" class=\"CitationRef\"\u003e2016\u003c/span\u003e) and to increase the population density of ladybugs (Tillman and Cottrell \u003cspan citationid=\"CR126\" class=\"CitationRef\"\u003e2012\u003c/span\u003e). The method of \u0026ldquo;trapping crops\u0026rdquo;, used with attractive flower strips, can increase biodiversity due to the supply of nectar and pollen for beneficial insects, which favors the services provided by natural enemies, contributing to the reduction in the use of pesticides (Pollock \u003cspan citationid=\"CR94\" class=\"CitationRef\"\u003e2012\u003c/span\u003e; Nielsen et al. \u003cspan citationid=\"CR83\" class=\"CitationRef\"\u003e2016\u003c/span\u003e). Trap crops help to conserve fertile soil, reduce damage to commercial crops, and increase profit from the harvest by 10\u0026ndash;30% (Prakasha et al. \u003cspan citationid=\"CR95\" class=\"CitationRef\"\u003e2016\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eThe richness of pollinators favored attractive flower strips of tomato and sorghum because sorghum can be foraged by bees from the Apidae and Halictidae families and used as a food source, especially when there are no food resources available (Schmidt and Bothma \u003cspan citationid=\"CR112\" class=\"CitationRef\"\u003e2005\u003c/span\u003e). The richness of plant species with flowers adjacent to a crop promotes the diversity of pollinators (Scheper et al. \u003cspan citationid=\"CR111\" class=\"CitationRef\"\u003e2013\u003c/span\u003e; Kremen and M\u0026rsquo;Gonigle \u003cspan citationid=\"CR67\" class=\"CitationRef\"\u003e2015\u003c/span\u003e; Sutter et al. \u003cspan citationid=\"CR122\" class=\"CitationRef\"\u003e2017\u003c/span\u003e; Kremen et al. \u003cspan citationid=\"CR65\" class=\"CitationRef\"\u003e2018\u003c/span\u003e), which favors an increase in pollination services by up to 52% (Albrecht et al. \u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e2020\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eThe hypothesis that the production of tomato fruit would be favored by the diversity of pollinators and natural enemies due to the attractive flower strips of cilantro and sorghum was refuted in the present study. The diversity of pollinator insects and natural enemies did not influence productivity in other studies, such as tomato and pepper (Winfree et al. \u003cspan citationid=\"CR137\" class=\"CitationRef\"\u003e2008\u003c/span\u003e), apple (Campbell et al. \u003cspan citationid=\"CR19\" class=\"CitationRef\"\u003e2017\u003c/span\u003e), strawberry (Hodgkiss et al. \u003cspan citationid=\"CR53\" class=\"CitationRef\"\u003e2019\u003c/span\u003e), and melon (Azpiazu et al. \u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e2020\u003c/span\u003e). The absence of the effect of the diversity of pollinator insects and natural enemies on production may be associated with another factor, such as the size of the attractive flower strips (Hodgkiss et al. \u003cspan citationid=\"CR53\" class=\"CitationRef\"\u003e2019\u003c/span\u003e). In our study, the size of the attractive flower strips may have contributed to the absence of an increase in tomato production in the studied cultivation area due to the size of the flower strip area, which was only 21 m\u0026sup2;, and we believe that in greater areas, a higher production would be found. Other studies showed that a high abundance of pollinator insects and a high rate of floral visitors were observed along borders with attractive flower strips in areas from 38 m\u0026sup2; to 41 m\u0026sup2; (Mayer et al. \u003cspan citationid=\"CR73\" class=\"CitationRef\"\u003e2012\u003c/span\u003e) however, no production evaluation was performed.\u003c/p\u003e \u003cp\u003eThe diversity of pollinator insects and natural enemies in tomato cultivation did not increase with the proximity of the corn crop. Although agricultural species cultivated in the reproductive phase provided floral resources and increased pollinators in comparison with the remainder of the native vegetation; this was not observed for tomato in relation to corn. This fact could be due to the massive flowering of the attractive species monopolizing the visits of bees, as was observed for \u003cem\u003eHedysarum coronarium\u003c/em\u003e L. (Fabaceae), a native species from Portugal. In that study, proximity to crops caused a decrease in the abundance of pollinators in the native vegetation adjacent to the species (Montero-Casta\u0026ntilde;o et al. \u003cspan citationid=\"CR77\" class=\"CitationRef\"\u003e2016\u003c/span\u003e). The concentration of floral resources in the sunflower crop increased the abundance of pollinators within the cultivation area in relation to the Cerrado remnant (Almeida et al. \u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e2020\u003c/span\u003e). Monoculture has mass flowering that attracts pollinators, temporarily decreasing the presence in adjacent forests (Montero-Casta\u0026ntilde;o et al. \u003cspan citationid=\"CR77\" class=\"CitationRef\"\u003e2016\u003c/span\u003e). Foraging behavior can be influenced, mainly by species of insects with short flight distances between floral visits (Gross \u003cspan citationid=\"CR50\" class=\"CitationRef\"\u003e2001\u003c/span\u003e), so pollinators benefit from available high-quality floral resources (Dietzsch et al. \u003cspan citationid=\"CR31\" class=\"CitationRef\"\u003e2011\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eAlthough flower visiting insects can perform pollination, due to the search for nectar or pollen in flowers as food resources for themselves or offspring, they do not always perform pollination (Alves-dos-Santos et al. \u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e2016\u003c/span\u003e). In contrast, pollinating insects always transfer pollen from the anthers to the stigma of the flower of the same plant species. Floral visitor species that do not carry out buzz pollination can perform pollination, but due to the low vibration capacity of the flowers, this does not prevent the extraction and transfer of pollen to the stigma of the flowers, which is why they are less efficient in this process (De Luca and Vallejo-Marin 2013).\u003c/p\u003e \u003cp\u003eTomato flowers (\u003cem\u003eS. Lycopersicum\u003c/em\u003e), as well as other species of the genus \u003cem\u003eSolanum\u003c/em\u003e, have poricidal anthers, pollinated by social bees of the genus \u003cem\u003eMelipona\u003c/em\u003e, \u003cem\u003eBombus\u003c/em\u003e, and solitary bees of the genus \u003cem\u003eXylocopa\u003c/em\u003e (De Luca and Vallejo-Marin 2013). In Brazil, \u003cem\u003eBombus morio\u003c/em\u003e (Swederus) was registered as a pollinator in Goi\u0026aacute;s, so it is expected that \u003cem\u003eBombus (Thoracobombus) brevivillus\u003c/em\u003e (Franklin, 1913), which was one of the species collected during tomato flowering in Mato Grosso, is an effective pollinator, due to be buzz-pollinate in \u003cem\u003eSolanum stramonifolium\u003c/em\u003e Jacq (Bezerra and Machado \u003cspan citationid=\"CR13\" class=\"CitationRef\"\u003e2003\u003c/span\u003e; Nunes-Silva; Hrncir; Imperatriz-Fonseca \u003cspan citationid=\"CR84\" class=\"CitationRef\"\u003e2010\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eIn addition to \u003cem\u003eBombus\u003c/em\u003e, species of the genus \u003cem\u003eAugochloropsis\u003c/em\u003e and \u003cem\u003eMegachile\u003c/em\u003e show vibratory behavior of flowers, which are considered important pollinators of the tomato crop (Teppner \u003cspan citationid=\"CR124\" class=\"CitationRef\"\u003e2005\u003c/span\u003e; Vin\u0026iacute;cius-Silva et al. \u003cspan citationid=\"CR135\" class=\"CitationRef\"\u003e2017\u003c/span\u003e). In our study, species of \u003cem\u003eAugochloropsis\u003c/em\u003e and \u003cem\u003eMegachile\u003c/em\u003e were recorded during flowering of the crop, so it is expected that they have the function of pollinators for Mato Grosso tomatoes.\u003c/p\u003e \u003cp\u003eSpecies of \u003cem\u003eApis mellifera\u003c/em\u003e and \u003cem\u003eTrigona spinipes\u003c/em\u003e (Linnaeus 1758) do not show vibratory behavior but collect pollen grains from flowers that result from buzz pollination by other bee species (Santos et al. \u003cspan citationid=\"CR109\" class=\"CitationRef\"\u003e2014\u003c/span\u003e; Vin\u0026iacute;cius-Silva et al. \u003cspan citationid=\"CR135\" class=\"CitationRef\"\u003e2017\u003c/span\u003e). These grains can be deposited on the stigma of other flowers due to the foraging behavior of the species (Toni et al. 2021), which is why it is considered a tomato pollinator (Santos et al. \u003cspan citationid=\"CR109\" class=\"CitationRef\"\u003e2014\u003c/span\u003e; Giannini et al. \u003cspan citationid=\"CR43\" class=\"CitationRef\"\u003e2015b\u003c/span\u003e; Vin\u0026iacute;cius-Silva et al. \u003cspan citationid=\"CR135\" class=\"CitationRef\"\u003e2017\u003c/span\u003e). Thus, \u003cem\u003eA. mellifera\u003c/em\u003e that was present in tomato flowering can contribute to pollination, as well as the species \u003cem\u003eTrigona dallatorreana\u003c/em\u003e (Friese 1900), collected in our study.\u003c/p\u003e \u003cp\u003eBee species with the potential to pollinate tomato plants are \u003cem\u003eOxaea flavescens\u003c/em\u003e (Depr\u0026aacute; et al. \u003cspan citationid=\"CR28\" class=\"CitationRef\"\u003e2014\u003c/span\u003e; Santos et al. \u003cspan citationid=\"CR109\" class=\"CitationRef\"\u003e2014\u003c/span\u003e; Silva-Neto et al. \u003cspan citationid=\"CR116\" class=\"CitationRef\"\u003e2017\u003c/span\u003e; Vin\u0026iacute;cius-Silva et al. \u003cspan citationid=\"CR135\" class=\"CitationRef\"\u003e2017\u003c/span\u003e) and specimens of the genus \u003cem\u003eEuglossa\u003c/em\u003e sp. (Depr\u0026aacute; et al. \u003cspan citationid=\"CR28\" class=\"CitationRef\"\u003e2014\u003c/span\u003e), so it is believed that \u003cem\u003eEuglossa (Euglossa) carolina\u003c/em\u003e (Nem\u0026eacute;sio 2009) and \u003cem\u003eOxaea flavescens\u003c/em\u003e (Klug 1807), collected from tomatoes in Mato Grosso, are potential pollinators of the tomato crop in Mato Grosso.\u003c/p\u003e \u003cp\u003eAmong the insects that are classified as floral visitors of tomato plants, we can highlight the genus \u003cem\u003eFrieseomellita\u003c/em\u003e and \u003cem\u003eTetragona\u003c/em\u003e (Silva-Neto et al. \u003cspan citationid=\"CR116\" class=\"CitationRef\"\u003e2017\u003c/span\u003e; Vin\u0026iacute;cius-Silva et al. \u003cspan citationid=\"CR135\" class=\"CitationRef\"\u003e2017\u003c/span\u003e). In our study, the species \u003cem\u003eTetragona clavipes\u003c/em\u003e (Fabricius 1804) and \u003cem\u003eFrieseomelitta varia\u003c/em\u003e (Lepeletier 1836) were recorded visiting tomato flowers among other bees of these genus. Other floral visitor species recorded in our study were \u003cem\u003eCeratina (Calloceratina) chloris\u003c/em\u003e (Fabricius 1804) and \u003cem\u003eFlorilegus (Euflorilegus) aff. affinis\u003c/em\u003e (Urban 1970).\u003c/p\u003e"},{"header":"CONCLUSION","content":"\u003cp\u003eOur study provided a list of pollinator insect families and natural enemies sampled in the experimental tomato planting area. It was also identified that cilantro and sorghum are attractive plant species for pollinator insects and natural enemies when used in combination with tomato.\u003c/p\u003e \u003cp\u003eThe combination of cilantro and sorghum flower strips in tomatoes had a positive effect on beneficial insects. However, the diversity of pollinator insects and natural enemies did not increase with the proximity of the corn crop because the floral resources offered by the attractive flower strips of cilantro and sorghum may have influenced the permanence of pollinator insects and natural enemies within the tomato crop.\u003c/p\u003e \u003cp\u003eThe conclusion of the study was that the attractive flower strips of cilantro and sorghum influenced the increase in the diversity of pollinator insects and natural enemies in the tomato crop, contributing to the permanence of these insects in the crop field and preserving the ecosystem services provided by them.\u003c/p\u003e"},{"header":"Declarations","content":"\u003cp\u003e\u003cstrong\u003eAuthor contribution\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eAll authors made substantial contributions to the conception and the design of this study. SCL contributed to the development of the fieldwork and to the writing of the manuscript. MFS, ESOJ, and CG contributed to the review of the manuscript. Finally, AS contributed to the statistical analysis of the manuscript.\u0026nbsp;\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eAcknowledgements\u0026nbsp;\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe authors are thankful to the funding agency Coordena\u0026ccedil;\u0026atilde;o de Aperfei\u0026ccedil;oamento de Pessoal de N\u0026iacute;vel Superior-CAPES for the financial support and for the research grant. They are grateful to rural producer for the field crop to study.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eConflict of interest\u003c/strong\u003e The authors declare no competing interests\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\n\u003cli\u003eAbro KK, Memon N, Ansari A, Memon MI (2019) Host plant range of \u003cem\u003eAphidophagous \u003c/em\u003ehoverflies in relation to their prey aphids in Badin, Sindh, Pakistan. Pure Appl. 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Sci. 71. https://doi.org/10.1002/ps.4474\u003c/li\u003e\n\u003c/ol\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":true,"highlight":"","institution":"","isAcceptedByJournal":false,"isAuthorSuppliedPdf":false,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true},"keywords":"Environmental service, floral resource, sorghum, mix of sorghum flowers and cilantro","lastPublishedDoi":"10.21203/rs.3.rs-2751744/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-2751744/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003cp\u003eThe goal of this research was to analyze the effect of flower strips and the proximity of corn fields on the environmental services of regulation by insects (pollination and biological control) in tomato crops (\u003cem\u003eSolanum lycopersicum\u003c/em\u003e). The study was conducted using commercial tomatoes (6.200 m\u0026sup2;) in the Brazilian Cerrado. The experimental outline was completely randomized with 15 plots of 5 x 4 meters, constructed with 16 tomato plants, in two treatments: 1) tomato plants without attractive flower strips (control) and 2) tomato plants with attractive flower strips of cilantro and sorghum. The sampling of pollinator insects and natural enemies was performed using trap-type \u003cem\u003ebee bowls\u003c/em\u003e and active collection. Data were analyzed by generalized linear models (GLM) to compare insect diversity and abundance between treatments. As a result, the richness (p\u0026thinsp;=\u0026thinsp;0.040) and abundance (p\u0026thinsp;=\u0026thinsp;0.030) of pollinating insects were significantly higher in tomatoes with sorghum flowers than in the control. The effect of mixing strips of intercropped flowers (cilantro and sorghum) increased the abundance (p\u0026thinsp;=\u0026thinsp;0.007) and richness (p\u0026thinsp;=\u0026thinsp;0.005) of the total natural enemies and pollinators in richness (p\u0026thinsp;=\u0026thinsp;0.030) and abundance (p\u0026thinsp;=\u0026thinsp;0.020) in the tomato plants with the flower strips compared to the tomato plants without the strips. Our results clearly show that the use of attractive flower strips of the mix of cilantro and sorghum in interleaved periods with tomato plants contributes to the permanence of the services provided by insects to the crop field.\u003c/p\u003e","manuscriptTitle":"Use of flower strips to attract pollinator insects and natural enemies in tomato crops","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2023-05-05 15:26:06","doi":"10.21203/rs.3.rs-2751744/v1","editorialEvents":[{"type":"communityComments","content":0}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true}}],"origin":"","ownerIdentity":"38d5ab9b-17c9-4bf7-b6e5-05dc856abd2d","owner":[],"postedDate":"May 5th, 2023","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"posted","subjectAreas":[],"tags":[],"updatedAt":"2023-06-12T14:21:38+00:00","versionOfRecord":[],"versionCreatedAt":"2023-05-05 15:26:06","video":"","vorDoi":"","vorDoiUrl":"","workflowStages":[]},"version":"v1","identity":"rs-2751744","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-2751744","identity":"rs-2751744","version":["v1"]},"buildId":"FbvkV6FR0MCFSLy54lSbu","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}