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Efficacy of Control of Glyphosate-Tolerant Species of the Rubiaceae Family Through Double-Knockdown Applications

Eficácia do Controle de Espécies Tolerantes ao Glifosato da Família Rubiaceae Através de Aplicações em Golpe Duplo

ABSTRACT:

Spermacoce latifolia, S. verticillata, and Richardia brasiliensis (family Rubiaceae, tribe Spermacoceae) are glyphosate-tolerant weeds in the soybean producing areas of Brazil. The weed shifts to glyphosate-tolerant weeds across soybean-producing areas has shown the need for adoption of practices that conserve the efficacy of glyphosate. This study evaluated the effect of single- and double-knockdown herbicide applications on the control of S. latifolia, S. verticillata, and R. brasiliensis prior to soybean sowing. Trials were designed as a randomized block and treatments were arranged as a factorial. Factor A was three systemic herbicide treatments 10 days before sowing (DBS), while Factor B was three contact herbicide treatments applied 0 DBS (“sow and apply”). The single- and double-knockdown applications were followed by post-emergence applications of glyphosate or 2,4-D + glyphosate when the crop reached three leaves. The efficacy of control of each weed species was visually evaluated 14 days after sowing (DAS), as well as 0 and 28 days after post-emergence application (DAA). The double-knockdown applications generally provided higher levels of control for the target weeds of the Rubiaceae family than the single-knockdown applications. Glyphosate + 2,4-D, glyphosate + 2,4-D + diclosulam or glyphosate + [halauxifen-methyl + diclosulam] followed by glufosinate or paraquat achieved at least 90% of control of S. latifolia and R. brasiliensis, but did not control S. verticillata (<80%). Glufosinate at 457 g a.i. ha-1 was equivalent to paraquat at 400 g a.i. ha-1 as a contact herbicide in the double-knockdown applications, especially on the first assessment dates.

Keywords:
2,4-dichlorophenoxyacetic acid; ammonium glufosinate; Spermacoce latifolia; Spermacoce verticillata; Richardia brasiliensis

RESUMO:

Spermacoce latifolia, S. verticillata e Richardia brasiliensis (família Rubiaceae, tribo Spermacoceae) são plantas daninhas tolerantes ao glyphosate nas áreas de soja do Brasil. Mudanças na flora daninha para espécies tolerantes ao glyphosate nas áreas de soja evidenciam a necessidade de adoção de práticas que conservem a eficácia desse herbicida. Este estudo avaliou o efeito de aplicações de herbicidas em golpe simples e duplo no controle de S. latifolia, S. verticillata e R. brasiliensis antes da semeadura da soja. O delineamento foi o de blocos casualizados, com tratamentos em esquema fatorial. O fator A constou de três tratamentos de herbicidas sistêmicos aos 10 dias antes do plantio (DBS), enquanto o fator B constou de três tratamentos de herbicidas de contato aplicado aos 0 DBS (“plante e aplique”). As aplicações em golpe simples e duplo foram seguidas por aplicações em pós-emergência de glyphosate ou 2,4-D + glyphosate quando a cultura da soja atingiu três folhas expandidas. A eficácia do controle de cada espécie-alvo foi avaliada visualmente aos 14 dias após a semeadura (DAS), bem como aos 0 e 28 dias após a aplicação em pós-emergência (DAA) da cultura. As aplicações de golpe duplo geralmente proporcionaram maiores níveis de eficácia de controle para as plantas daninhas alvo da família Rubiaceae do que as aplicações em golpe simples. Glyphosate + 2,4-D, glyphosate + 2,4-D + diclosulam ou glyphosate + [halauxifen-metílico + diclosulam] seguido de glufosinato ou paraquat atingiram, pelo menos, 90% de controle de S. latifolia e R. brasiliensis, mas não controlaram S. verticillata (<80%). O glufosinato a 457 g i.a. ha-1 foi equivalente ao paraquat a 400 g i.a. ha-1 como herbicida de contato nas aplicações em golpe duplo, especialmente nas primeiras avaliações.

Palavras-chave:
2,4-diclorofenoxiacético; glufosinato de amônio; Spermacoce latifolia; Spermacoce verticillata; Richardia brasiliensis

INTRODUCTION

The Rubiaceae is the fourth-largest family of the angiosperms by number of species, containing about 611 genera and approximately 13,100 species distributed throughout most of the world (Govaerts et al., 2007Govaerts R, Frodin DG, Ruhsam M, Bridson DM, Davis AP. World checklist & bibliography of Rubiaceae. Kew: The Trustees of the Royal Botanic Gardens; 2007.). In Brazil, 112 genera and 1,347 species of this family were found in surveys of natural vegetation, of which about 14 genera and 694 species are endemic to the country (Barbosa et al., 2015Barbosa MR, Zappi D, Taylor C, Cabral E, Jardim JG, Pereira MS, et al. Lista de espécies da flora do Brasil. Rio de Janeiro: Jardim Botânico do Rio de Janeiro; 2015. p.1545-91.). Herbaceous species of Rubiaceae are also widely distributed in the agricultural areas of Brazil, especially those from the Spermacoce tribe (Ikeda et al., 2008Ikeda FS, Mitja D, Vilela L, Silva JCS. Seedbanks in cerrado sensu stricto under burning and cultivation system. Pesq Agropec Bras. 2008;43:667-73.; Marques et al., 2011Marques LJP, Silva MRM, Lopes GS, Corrêa MJP, Araujo MS, Costa EA, et al. Phytosociology of weeds in cowpea and cassava crops under the slash-and-burn with plow. Planta Daninha. 2011;29:981-9.). These species are generally tolerant of a broad array of environmental conditions such as acid soil, drought, and even soils highly contaminated by arsenic and iron ore (Campos et al., 2014Campos NV, Loureiro ME, Azevedo AA. Differences in phosphorus translocation contributes to differential arsenic tolerance between plants of Borreria verticillata (Rubiaceae) from mine and non-mine sites. Environ Sci Pollut Res. 2014;21(8):5586-96.). As a result, species of Spermacoce have been reported as important weeds in both annual and perennial crops due their adaptation to the climate and soil conditions of agroecosystems.

Soybean, Glycine max (L.) Merrill, has considerable economic, cultural and social importance in Brazil, where it was grown in over 34 million hectares in the 2016-2017 growing season (USDA, 2017U.S. Department of Agriculture - USDA. World Agricultural Supply and Demand Estimates (WASDE-570), Washington, DC: 2017. [accessed: 20 Jan. 2018]. Available from: Available from: https://www.usda.gov/oce/commodity/wasde/latest.pdf
https://www.usda.gov/oce/commodity/wasde...
). In Brazil, weed communities have shifted to species with tolerance to glyphosate due to the widespread adoption of glyphosate-tolerant soybeans (Galon et al., 2013Galon L, Ferreira EA, Aspiazú I, Concenço G, Silva AF, Silva AA, et al. Glyphosate translocation in herbicide tolerant plants. Planta Daninha. 2013;31(1):193-201.; Takano et al., 2013Takano HK, Oliveira Jr RS, Constantin J, Biffe DF, Franchini LHM, Braz GBP, et al. Efeito da adição do 2,4-D ao glyphosate para o controle de espécies de plantas daninhas de difícil controle. Rev Bras Herbic. 2013;12:1-13.). Among the glyphosate-tolerant weeds that occur in the soybean areas, Spermacoce latifolia (Aubl.) and S. verticillata (L.) are some of the most common species of the Spermacoce tribe. Another common hard-to-kill weed species of this tribe is Richardia brasiliensis (Gomes), which is widely distributed in soybean areas across southern, southeastern, and midwestern Brazil. As glyphosate does not effectively control these tolerant weeds, other herbicide modes of action must be mixed with glyphosate (Vidal et al., 2010Vidal RA, Rainero HP, Kalsing A, Trezzi MM. Prospección de las combinaciones de herbicidas para prevenir malezas tolerantes y resistentes al glifosato. Planta Daninha. 2010;28(1):159-65.).

The weeds’ tolerance to herbicides generally may be explained by differential herbicide uptake, translocation, metabolization, compartmentalization, and affinity with the specific site of action (Galon et al., 2009Galon L, Ferreira EA, Concenço G, Silva AA, Vargas L. Tolerância de culturas e plantas daninhas a herbicidas. In: Agostinetto D, Vargas L, editores. Resistência de plantas daninhas a herbicidas no Brasil. Passo Fundo: Berthier; 2009. p.37-74. ). Also, the level of insensibility can be influenced by many factors such as weed growth stage and weather conditions, among others, which interact with the weeds’ tolerance mechanisms. In S. latifolia, the use of 14C-glyphosate showed that about 89% of the herbicide remained in the treated leaf and only 2% reached the plant roots by 72 hours after treatment (Galon et al., 2013). Thus, it was concluded that S. latifolia showed lower glyphosate translocation into the plant, illustrating at least one of the mechanisms that provide greater tolerance to this herbicide. The same tolerance mechanism to glyphosate was found in Ipomoea grandifolia (Dammer), while Commelina benghalensis (L.) had differential metabolization (Monquero et al., 2004Monquero PA, Christoffoleti PJ, Osuna MD, Prado RA. Absorption, translocation and metabolism of glyphosate by plants tolerant and susceptible to this herbicide. Planta Daninha. 2004;22:445-51.).

The rapidly weed shifting to glyphosate-tolerant weed species throughout the soybean-producing areas of Brazil has shown the need for adoption of practices that would conserve the glyphosate efficacy. “Double-knockdown” applications have been a strategy for the control of glyphosate-resistant weeds as well as for the delay their herbicide resistance (Neve et al., 2003Neve P, Diggle AJ, Smith FP, Powles SB. Simulating evolution of glyphosate resistance in Lolium rigidum II: past, present and future glyphosate use in Australian cropping. Weed Res. 2003;43:418-27.; Weersink et al., 2005Weersink A, Llewellyn RS, Pannell DJ. Economics of pre-emptive management to avoid weed resistance to glyphosate in Australia. Crop Prot. 2005;24:659-65.). This technique involves a burndown application of systemic herbicide (e.g., glyphosate) followed by a subsequent herbicide treatment of a non selective contact herbicide (e.g., paraquat). Glyphosate followed by paraquat + diquat with 2-10 days interval between sprays provided 98 100% control of glyphosate-resistant Lolium rigidum (Gaud.) (Borger and Hashem, 2007Borger CA, Hashem A. Evaluating the double knockdown technique: sequence, application interval, and annual ryegrass growth stage. Aust J Agric Res. 2007;58:265-71.). In addition to consistently improving pre-planting weed control over a single application, the double-knockdown technique can decrease the evolution of glyphosate resistance (Neve et al., 2003).

The objective of this study was to evaluate the effect of single- and double-knockdown herbicide applications prior to soybean sowing on the control of S. latifolia, S. verticillata, and R. brasiliensis.

MATERIALS AND METHODS

Five trials were conducted under field conditions during the 2016-2017 summer rainy season at different locations distributed across the southern, southeastern, and midwestern regions of Brazil (Table 1). The experimental areas were selected based on the commercial importance of soybean production and showed natural infestations of at least one of the weed species of the Rubiaceae family. Glyphosate-tolerant varieties indicated to each location were sown from October 27, 2016, to December 19, 2016, in rows spaced from 45 to 50 cm apart and seeded from 32 to 36 seeds m-2. Agronomic practices and general inputs were those recommended to each region, and soil fertilization was planned based on soil analysis performed prior to the soybean sowing. The experimental areas always relied on natural rainfall coming from the summer rainy season, and the total rainfall amount was collected by local automated remote weather stations.

Table 1
Area coordinates, soil characteristics, rainfall amount, soybean sowing and variety, application timing, and target weeds

The experimental design was a completely randomized block arranged as a factorial, with four replications. Factor A was three systemic herbicide treatments applied 10 days before sowing (DBS), while Factor B was three contact herbicide treatments applied 0 DBS (“sow and spray”) (Table 2). Therefore, the full combination of Factor A and Factor B provided three single- (treatments 1, 4, and 7) and six double-knockdown herbicide applications (treatments 2, 3, 5, 6, 8, and 9). In addition, three single-knockdown applications (treatments 10, 11, and 12) as well as an untreated check-plot (treatment 13) were also included as standard treatments for comparison. The experimental units consisted of field plots measuring 3 m wide and 5 m long (15 m2). Applications of the treatments were always performed in 100 L ha-1 using CO2 backpack sprayers at 276 kPa equipped with a 3 m wide boom and AIXR 110015 flat-fan nozzles. The application conditions were: average air temperature ranging from 23 oC to 28 oC; average relative humidity of air ranging from 58 to 78%, average wind speed lower than 0.5 km h-1 and clear sky with few clouds.

Table 2
Treatments and respective doses and application timings prior to soybean sowing

To obtain and evaluate a complete weed control program as typically performed by soybean growers in Brazil, the treatments were followed by post-emergence applications when the crop reached three leaf stage. Treatments 1 through 10 were followed by a pre-mix of 2,4-D choline salt 195 g a.e. L-1 + glyphosate dimethylamine (DMA) salt 205 g a.e. L-1 at 780 + 820 g a.e. ha-1, respectively (1,600 g a.e. ha-1). This herbicide treatment will be an alternative for post emergence weed control in 2,4 D-tolerant soybean which are under development in Brazil and other countries. Treatments 11 and 12 were followed by glyphosate DMA salt 480 g a.e. L-1 at 1,440 g a.e. ha-1, simulating a conventional utilization of this herbicide in glyphosate-tolerant soybeans. Post-emergence applications were performed as described for the burndown applications.

The efficacy of control of each target weed of the Rubiaceae family was assessed using a linear scale varying from 0 (no weed control) to 100% (complete weed control), according to Camper (1986Camper ND. Research methods in weed science. 3rd ed. Champaign: Southern Weed Science Society; 1986.). In all trials, the assessments were visually performed 14 days after soybean sowing (DAS) as well as 0 and 28 days after application (DAA) of the post-emergence herbicides treatments. In these studies, the soybean was just established as a crop model on the experimental areas and consequently no visual assessments were performed to evaluate the treatments’ effect on the crop.

Initially, the treatments designed as a factorial (treatments1 through 9) was analysed with the following mixed model (eq. 1):

% E f f i c a c y i j k l = μ + a i + b j + a × b i j + c k + a × c i k + b × c j k + a × b × c i j k + d l ( k ) (eq. 1)

where systemic herbicides (a), contact herbicides (b), locations (c) and their interactions were considered as fixed effects in the model, and block (d) was considered as random effect. Additionally, in order to compare the treatments into the factorial design with the standard treatments, data from all herbicide treatments (treatments 1 through 12) were analysed with the following mixed model (eq. 2):

% E f f i c a c y i j k l = μ + a i + b j + a × b i j + c l ( k ) (eq. 2)

where herbicide (a) (each herbicide program), locations (b) and their interactions were considered as fixed effects in the model, and block (c) was considered as random effect. The linear mixed models were estimated with the restricted maximum likelihood method (REML), and means were compared with Tukey’s test (α=0.05).

RESULTS AND DISCUSSION

The efficacy of Spermacoce latifolia control has varied as a function of the interaction between systemic (applied 10 DBS) and contact (applied 0 DBS) herbicide treatments in the evaluation at 14 DAS (Table 3). The herbicide treatments 3 through 8 achieved the highest levels of S. latifolia control in this evaluation date, with average values of efficacy of control ranging from 87% to 99% (Table 4). These results persisted in the assessment performed when the crop reached three leaves (0 DAA), and higher levels of control were observed in Primavera do Leste/MT than Itanhangá-MT. S. latifolia control varied as a function of the systemic herbicide treatments at 28 DAA (Table 3), and treatments followed by 2,4-D and glyphosate were effective in its control (>95%) (Table 4). The effect of double-knockdown applications did not differ from the effect of single-knockdown applications at this evaluation date, regardless of the systemic herbicides, contact herbicides, and locations.

Table 3
P-values of the analysis of variance through the F-test for efficacy of control of Spermacoce latifolia (Aubl.), S. verticillata (L.) and Richardia brasiliensis (Gomes) in three assessment dates, in the 2016-2017 summer rainy season
Table 4
Efficacy of control of Spermacoce latifolia (Aubl.) in three evaluation dates as a function of single- and double-knockdown herbicide applications observed in Primavera do Leste/MT (PDL) and Itanhangá/MT (ITA), in the 2016-17 summer rainy season

In the case of S. verticillata, the efficacy of control was also dependent on the interaction between both systemic and contact herbicide treatments in the evaluation performed at 14 DAS (Table 3). Generally, higher controls were obtained with the use of double than single-knockdown applications, and glufosinate was equivalent to paraquat as a second herbicide application (Table 5). At 0 DAA, double-knockdown applications were also the most effective practice to control S. verticillata, but differences in weed control levels were even more evident between the locations. The effect of most herbicide treatments was lower in Correntina-BA when compared to the effect of the same herbicide treatments in Itanhangá-MT and Sinop-MT. At 28 DAA, glyphosate + chlorimuron and glyphosate + 2,4-D + saflufenacil followed by glyphosate were the only treatments which achieved 80% of control, except in Corrrentina-BA.

Table 5
Efficacy of control of Spermacoce verticillata (L.) in three evaluation dates as a function of single- and double-knockdown herbicide applications observed in Correntina-BA (COR), Itanhangá-MT (ITA) and Sinop/MT (SIN), in the 2016-17 summer rainy season

The interaction of systemic herbicide treatments and contact herbicide treatments was significant for the efficacy of Richardia brasiliensis control in the visual assessment performed in Jaguapitã-PR at 14 DAS (Table 3). Although double-knockdown applications provided better levels of weed control than single applications, there were not always significant differences among their average values (Table 6). The superiority of double-knockdown applications persisted in the evaluation at 0 DAA and was significant when the first application was glyphosate + [halauxifen-methyl + diclosulam]. R. brasiliensis control did not vary as a function of the factors tested at 28 DAA (Table 3), and all herbicide treatments provided satisfactory control of this weed species (>94%) (Table 6). The effect of double-knockdown applications did not differ from the effect of single-knockdown applications at this assessment date, regardless of the systemic herbicides and contact herbicides.

Table 6
Efficacy of control of Richardia brasiliensis (Gomes) in three evaluation dates as a function of single- and double-knockdown herbicide applications observed in Jaguapitã-PR, in the 2016-16 summer rainy season

No previous field studies were found in the scientific literature evaluating the efficacy of control of weed species of the Rubiaceae family through the utilization of double-knockdown applications. In single-knockdown studies - one application timing- with S. latifolia, S. verticillata, and R. brasiliensis, several herbicide associations have been effective in killing these weed species. While glyphosate at 1,440 g a.e. ha-1 resulted in less than 85% control of S. latifolia and R. brasiliensis, mixing it with carfentrazone or flumioxazin provided control above 95% (Ferreira et al., 2006Ferreira ACB, Barros AC, Lamas FM. Manejo de plantas daninhas na cultura do algodoeiro. Campina Grande: Embrapa; 2006. 8p.). In other cases, glyphosate at 1,080 g a.e. ha-1 achieved 84% control of B. densiflora and mixing it with 2,4-D (670 g a.e. ha-1) provided complete control (Martins and Christoffoleti, 2014Martins BAB, Christoffoleti PJ. Herbicide efficacy on Borreria densiflora control in pre- and post-emergence conditions. Planta Daninha. 2014;32:817-25.). Lactofen at 120 g a.i. ha-1, paraquat at 400 g a.i. ha-1, chlorimuron at 12 g a.i. ha-1, and imazethapyr at 74 g a.i. ha-1 also delivered control of more than 90% of B. densiflora in the same study.

At least three explanations for the reduced effect of herbicide treatments between the present study and data from the literature may be examined, as well as differences among the locations of the present study. First, it is possible that the field identification of one or both species of Spermacoce genus is not correct, because they may possess morphological plasticity throughout soybean production areas. In fact, S. latifolia and S. verticillata are considered by many authors to be a distinct genus, Borreria, which shows that their identification itself is still not well-defined (Ferreira Jr. et al., 2012Ferreira Jr JC, Lemos RPL, Conserva LM. Chemical constituents from Spermacoce verticillata (Rubiaceae). Biochem Syst Ecol. 2012;44:208-11.). Second, weed growth stages may have directly affected the herbicide control efficacy, since in the present study the target weeds were at advanced or even perennial growth stages (Table 1). Third, the environmental conditions at application may have also negatively influenced the levels of weed control in the locations with lower rainfall amounts, such as in Correntina-BA (Table 1).

The effect of glufosinate at 457 g a.i. ha-1 as a contact herbicide in the second spray was generally equivalent to paraquat at 400 g a.i. ha-1, especially in the two first assessment dates (Tables 4,5and6). This herbicide controls a great variety of weeds by irreversibly inhibiting glutamine synthetase, which is an enzyme that creates glutamine from glutamate and ammonium (Berlicki, 2008Berlicki L. Inhibitors of glutamine synthetase and their potential application in medicine. Mini-Rev Med Chem. 2008;8:869-78.). Glufosinate at 400 g a.i. ha-1 was also reported as an alternative on the Conyzaspp. control in burndown conditions, even with plants at the pre-flowering growth stage (Moreira et al., 2010Moreira MS, Melo MSC, Carvalho SJP, Nicolai M, Crhistoffoleti PJ Alternative herbicides to control glyphosate-resistant biotypes of Conyza bonariensis and C. canadensis. Planta Daninha. 2010;28(1):167-75.). Thus, this herbicide can be used as an effective alternative to paraquat, which will be commercially banned in three years in Brazil by the 177 Collegiate Board Resolution (ANVISA, 2017Agência Nacional De Vigilância Sanitária - ANVISA. Resolução de diretoria colegiada - RDC Nº 177, de 21 de setembro 2017. [acessado em: 22 jan. 2018]. Disponível em: Disponível em: http://portal.anvisa.gov.br/documents/10181/2871639/RDC_177_2017_.pdf/399e71db-5efb-4b34-a344-9d7e66510bce?version=1.0 .
http://portal.anvisa.gov.br/documents/10...
).

Double-knockdown applications did not always result in a higher level of weed control than in single applications against weed species of the Rubiaceae family, especially in the case of S. verticillata (Table 6). However, the sequential application of systemic and contact herbicide treatments is likely to delay and even prevent the evolution of herbicide resistance to either chemical (Neve et al., 2003Neve P, Diggle AJ, Smith FP, Powles SB. Simulating evolution of glyphosate resistance in Lolium rigidum II: past, present and future glyphosate use in Australian cropping. Weed Res. 2003;43:418-27.). For example, Hedyotis verticillata (syn.S. verticillata) was found to have high level of resistance to both glyphosate and paraquat in oil palm plantations from Malaysia (Chuah et al., 2005Chuah TS, Noor-Zalila MR, Cha TS, Ismail BS. Paraquat and glyphosate resistance in woody borreria (Hedyotis verticillata) growing at oil palm plantations in Terengganu, Malaysia. Malays Appl Biol. 2005;34(2):43-49.). Thus, the double-knockdown application is a valuable tool in integrated weed management strategies to decrease the risk of developing glyphosate resistance (Llewellyn et al., 2005Llewellyn RS, Lindner RK, Pannell DJ, Powles SB. When does double knockdown strategy pay? In: Douglas A, editor. Crop updates: weed updates. Perth: Department of Agriculture; 2005. p.54-6.). Additionally, this strategy could also reduce weed shifting to weed species with inherent tolerance to glyphosate such as S. latifolia, S. verticillata, and R. brasiliensis, among others.

In the present study, double-knockdown applications generally provided higher levels of control of S. latifolia, S. verticillata, and R. brasiliensis than the single-knockdown applications. Glyphosate + 2,4-D, glyphosate + 2,4-D + diclosulam, and glyphosate + [halauxifen-methyl + diclosulam] followed by glufosinate or paraquat achieved at least 90% of control of S. latifolia and R. brasiliensis, but did not achieve satisfactory level of control (> 80%) of S. verticillata. The effect of glufosinate at 457 g a.i. ha-1 as a contact herbicide in the double-knockdown applications was generally equivalent to paraquat at 400 g a.i. ha-1, especially in the first assessment dates.

REFERENCES

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Publication Dates

  • Publication in this collection
    17 Apr 2020
  • Date of issue
    2020

History

  • Received
    24 Jan 2018
  • Accepted
    27 Apr 2018
Sociedade Brasileira da Ciência das Plantas Daninhas Departamento de Fitotecnia - DFT, Universidade Federal de Viçosa - UFV, 36570-000 - Viçosa-MG - Brasil, Tel./Fax::(+55 31) 3899-2611 - Viçosa - MG - Brazil
E-mail: rpdaninha@gmail.com