Zooplankton community responses to the mixture of imazethapyr with imazapic and bispyribac-sodium herbicides under rice paddy water conditions

Respostas da comunidade de zooplâncton à mistura dos herbicidas imazetapir com imazapique e bispiribaque-sódico em áreas de arroz irrigado

Abstracts

The aim of this study was to assess the effect of concentrations of imazethapyr, imazapic, and bispyribac-sodium herbicides on zooplankton community (Cladocer, Copepod and Rotifer) in rice paddy fields. The decrease of half-life dissipation (DT₅₀) of the herbicides under study in water was: imazethapyr, imazapic, and bispyribac-sodium with an average of 3.75, 3.73 and 1.91 days, respectively. The mixture of imazethapyr with imazapic caused change in the analyzed zooplankton, with an increase in the densities of Cladocer and adult Copepod groups, while bispyribac-sodium caused a reduction of density in Copepod group, both adults and nauplii, in the initial samples. Among the groups, Rotifer was slightly sensitive to the herbicides.

imidazoalinones; pyrimidinyloxybenzoic acid; crustacean; cladocera; copepoda; rotifera

O objetivo deste estudo foi avaliar o efeito das concentrações dos herbicidas imazetapir, imazapique e bispiribaque-sódico na comunidade zooplanctônica (Cladocera, Copepoda e Rotifera) na lavoura de arroz. A diminuição da dissipação de meia-vida (DT₅₀) desses herbicidas em estudo na água foi: imazetapir, imazapique e bispiribaque-sódico, com uma média de 3,75, 3,73 e 1,91 dias, respectivamente. A mistura de imazetapir com imazapic provocou alteração no zooplâncton analisado, com incremento nas densidades dos grupos Cladocera e Copepoda adultos, enquanto que bispiribaque-sódico causou redução de densidade no grupo Copepoda, tanto adulto quanto náuplio, nas amostragens iniciais. Dentre os grupos, Rotifera foi pouco sensível aos herbicidas.

imidazolinonas; ácido pirimidiniloxibenzóico; crustáceos; cladocera; copepoda; rotifera

INTRODUCTION

The worldwide use of herbicides in agriculture for controlling weeds has contributed to the rise of concerns on the contamination of surface and groundwater bodies, and must be considered a potential risk for aquatic life as well as for the quality of drinking water. Even herbicides, such as imazethapyr, imazapic and bispyribac-sodium, and others routinely employed in rice production for the last decades and specifically designed to eliminate weeds, are reported in literature as hazardous at low concentrations, both to aquatic vertebrates and invertebrates (MOORE et al., 1998). Previous researches conducted by PERSCHBACHER et al. (1997), VILLARROEL et al. (2003) (propanil), PERSCHBACHER et al. (2002) (clomazone and quinclorac), and SÁNCHEZ et al. (2006) (profoxydim) showed that herbicides can affect zooplanktonic community. Paddy fields provide habitat for several non-target organisms, such as planktonic species, which play a key role in freshwater ecosystems as they occupy a central position in the food chain, transferring energy from primary producers to organisms at higher trophic levels (CHANG et al., 2005). These organisms constitute an important food source for the numerous predatory insect larvae living in the paddies, all of which help to control rice pest species breeding in this agro-ecosystem (BAMBARADENIYA & AMERASINGHE, 2003).

The commercial formulation of the herbicide Only^(r) is compounded by imazethapyr {2-[4,5-dihydro-4-methyl-4-(1-methylethyl)-5-oxo-1H-imidazol-2-yl]-5-ethyl-3-pyridinecarboxylic acid} and imazapic {2-[4,5-dihydro-4-methyl-4-(1-methylethyl)-5-oxo-1H-imidazol-2-yl]-5-methyl-3-pyridinecarboxylic acid}, which are members of the imidazoalinones family. These two chemical products present high water solubility, viz. 2200mg L^-1 and 36000mg L^-1 at 25ºC and pH 7, respectively (SENSEMAN, 2007). The commercial formulation of the herbicide Nominee^(r) is composed of bispyribac-sodium (sodium 2,6-bis(4,6-dimethoxypyrimidin-2-yloxy) benzoate), which is a member of the pyrimidinyloxybenzoic acid family, and is highly water soluble (64000mg L^-1) (TARAZONA & SANCHEZ, 2006). These two herbicides inhibit acetolactate synthase (ALS), which is responsible for the biosynthesis of the branched-chain amino acids leucine, isoleucine and valine and are recommended for controlling annual grasses and cyperaceae in irrigated rice in South Brazil (SOSBAI, 2007). Imazethapyr and imazapic form one of the herbicides registered for Clearfield^(r) Production System through the use of imidazoalinones rice tolerant variety, since this herbicide controls red rice in rice paddy.

However, due to the use of these herbicides in commercial rice being relatively recent, there are few research reports regarding effects of these herbicides when applied in rice paddy upon non target organisms, such as zooplankton community. Thus, this research aimed to investigate the recommended herbicide concentration of imazethapyr and imazapic, and bispyribac-sodium over zooplankton community (Cladocers, Copepods and Rotifers) in rice paddy water.

MATERIAL AND METHODS

The experiment was carried out at Universidade Federal de Santa Maria - UFSM (Rio Grande do Sul State, Brazil) whose geographical coordinates are 29°43'8.59" latitude south, 53°43'22.30" longitude west and 95m altitude, along 63 days (December 2007 to February 2008), using outdoor experimental irrigated rice plots set up in systematized lowland farming. The experimental design was a complete randomized block with three replications. Each experimental plot was 54m² (12 x 4.5m) in size. The treatments employed were the formulate mixture imazethapyr (75g L^-1) and imazapic (25g L^-1) (1L ha^-1), bispyribac-sodium (50g L^-1) (0.125L ha^-1), and control treatment (without herbicide). Herbicides were applied 30 days after the rice seeding, using a CO₂-pressurized backpack sprayer with four nozzles Teejet XR 11002 in a boom calibrated to deliver 150L ha^-1 of spray solution, and working at 275kPa. The irrigated rice crop received no other pesticides. The water lamina in the plots was kept about 0.10m throughout the crop cycle after the application of the treatment.

Water samplings for herbicides residues quantification were realized on 1^st, 3^rd, 5^th, 10^th, 14^th, 22^nd, 28^th, 37^th, and 60^th day after herbicides application. Samples were analyzed for imazethapyr and imazapic in accordance with the method described by GONÇALVES (2007) and bispyribac-sodium by KURZ et al. (2009), using High Performance Liquid Chromatography with Diode Array Detection (HPLC-DAD) with a Varian system (Palo Alto, CA, USA) composed of ProStar 210 pump and ProStar 335 DAD detector. The column configuration consisted of a Phenomenex (USA) C₁₈ reserved-phase column (250x4.6mm; 5µm) and a Phenomenex C₁₈ guard column (10x4.6mm; 5µm). The mobile phase consisted of purified water:methanol (35:65, v/v) acidified to pH 3.0 with phosphoric acid. A flow rate of 0.8mL min^-1 was used, with injection volume of 20µL and detection wavelength set at 254nm.

The persistence of herbicides in water was defined as the period between the application of herbicides and the last quantified concentration sampling. The pH, temperature, and morning dissolved oxygen were measured according to APHA (2005). Zooplankton samples were collected filtering 5-L water in three distinct points at each plot three days before application (-3 DBA) and on the 1^st, 3^rd, 14^th, 22^nd, 37^th, and 60^th day after application of herbicides (DAA), from 4:30 to 6:30 a.m., because this sampling will also provide a better estimate of macrozooplankton as well as an equally valid estimate of mesozooplankton in the same sample. For these samplings, a submerge pump attached to an electric motor was used, filtering them instantly through 25μm mesh net; then, the samples were field fixed in formaldehyde, totaling a final concentration of 4.0% and stored in amber glass flasks kept in darkness and at a low temperature until identification. Subsamples were taken with Hensen-Stemplel pipette and transferred to bogorov plates for enumeration and identification of principal zooplanktonic groups (LUDWIG, 1993), under a stereoscopy microscope.

The first-order rate constant "k" was determined from the slope of the linear plot of the natural logarithm of the remaining herbicide concentration [ln(C/C _o)] at various sampling intervals in relation to time. The dissipation time (DT ₅₀), i.e. the time taken for the concentration of pesticide to be reduced to 50% of its initial value, was calculated using the equation DT ₅₀=ln(2)/k, where k is the absolute value of the slope and first-order rate constant for the herbicide.

Before analysis, the zooplankton data were square root (x+0.5) transformed, where x is the density value. This was done to approximate the data to a normal distribution. The results of the zooplankton groups density were submitted to the two-factor (treatment and days) analysis of variance (ANOVA) for the evaluation of the interaction among them. The means were compared by Fisher's LSD test (P<0.05) to determine the differences among treatments. The analysis was performed using the SPSS 12.0.

RESULTS AND DISCUSSION

The accuracy, in terms of recovery, for bispyribac-sodium, imazethapyr and imazapic varied from 76.1 to 110.9, 89.3 to 106.7 and 80.9 to 106.6%, respectively. The precision of the method, in terms of relative standard deviation (RSD), presented values <10.1, <7.1 and <5.2%, respectively, for bispyribac-sodium, imazethapyr and imazapic. These results show that the sample preparation and analysis were efficient. Maximum imazethapyr, imazapic and bispyribac-sodium field concentration, measured one day after application was 27µg L^-1 (SD 11.3; n=3), 3.1µg L^-1 (SD 0.98; n=3), and 22.4µg L^-1 (SD 1.37; n=3), that dissipate <0.1µg L^-1 after 28 days, <0.04µg L^-1 after 14 days, and <0.01µg L^-1 after 22 days, respectively. For the persistence of herbicides in water, the initial dissipation times (DT ₅₀) calculated for imazethapyr and imazapic were <4 days, and for bispyribac-sodium were <2 days, which showed a first-order rate constant (k) (Figure 1).

Figure 1
Imazethapyr, imazapic and bispyribac-sodium herbicides concentration in rice paddy water during sampling days. The first-order rate constant (k) of herbicides were 0.19, 0.19 and 0.38μg L-1 day-1 for imazethapyr, imazapic and bispyribac-sodium, respectively

In the present study, rice paddy water herbicide imazethapyr concentrations were detected until 28DAA, and imazapic concentrations were detected until 14DAA. In Brazil, imazethapyr was detected in irrigation water up to 20 days after application with concentration under 5µg L^-1, when applied before permanent flood (SANTOS et al., 2008), and up to 30 days after application, with concentration under 3µg L^-1 (MARCOLIN et al., 2003) when applied after permanent flood. Maximum bispyribac-sodium concentration in 1DAA was 22.4µg L^-1, and it was detected by 21DAA, reinforcing the results obtained by SÁNCHEZ et al. (1999), with initial concentration of bispyribac-sodium in paddy water of 30µg L^-1.

Water quality values, dissolved oxygen concentration, temperature, pH and total hardness showed a significant difference among sampling days. In general, morning dissolved oxygen levels (0.42-6.53mg L^-1) were higher in the sample taken -3DBA, whereas after application samples remained low until 60DAA. Water temperature ranged from 17.1 to 26.5°C. The pH values (5.4-7.6) decreased in all treatments toward -3 DBA sampling. Thus, it was observed a lower value of morning dissolved oxygen concentration and pH after imazethapyr and imazapic and bispyribac-sodium application in relation to the control treatment. Dissolved oxygen and water pH levels decreased in collected control treatment before herbicide application, possibly due to precipitation occurring between -3DBA and 1DAA of 81mm along four days. Herbicides imazethapyr, imazapic, and bispyribac-sodium, in initial experimental days, provided decreased dissolved oxygen and water pH levels. The same chemical water changes after herbicide application have been demonstrated (GURNEY & ROBINSON, 1989).

The Cladocer group was observed to undergo a change in the organism density because of herbicides when compared to control treatment (Figure 2). Among the sampling days for imazethapyr and imazapic treatment toward 1DAA, there was a significant increase in Cladocers' density in relation to the -3DBA, remaining until 37DAA. In this same group, a tendency for increasing organism density was observed.

Figure 2
Mean abundance of crustacean and rotifer zooplankton groups in rice paddy during sampling days, expresses as differences from average control abundance

No significant difference between bispyribac-sodium and control treatment was observed to affect Cladocers' density. The high Cladocers density in imazethapyr and imazapic treatments found in this study, during sampling, corroborates with RELYEA (2009), whose studies suggest that low concentration of atrazine and 2,4-D herbicides have no effect in Cladocers' survival, or may cause an increase in their population due to high reproduction rate. Cladocer species exposed to the herbicide symetryn were clearly affected, while the majority of Rotifers was less affected and Copepods were apparently not depressed (KASAI & HANAZATO, 1995).

The density of Rotifers increased rapidly when the imazethapyr and imazapic herbicide was applied, but decreased later (3DAA), after which there was an increase where the density remained high until 22DAA. Comparing sampling days, bispyribac-sodium presented an increase of organism density from the 14^th until the 37^thDAA. As well as Cladocers, Rotifers presented no significant difference comparing the use of this herbicide and control treatment among sampling days. Rotifers presented high density in imazethapyr and imazapic treatment on the 1^stDAA. Similar results were observed by PERSCHBACHER et al. (1997), when imazaquin herbicide, which belongs to the same chemical group (imidazoalinone), was tested. The present study showed Rotifers to be less susceptible to the studied herbicides at tested concentration, as it was found out by HAVENS & HANAZATO (1993); SANDERSON et al. (2004).

Copepod Adults' density showed an increase after imazethapyr and imazapic application, remaining high until 22^ndDAA. However, by comparing organism density obtained in this group to the control treatment in 1^st, 14^th, 22^nd and 60^thDAA, it was observed that findings were above the expected for control treatment. Among sampling days, Copepod adults exposed to bispyribac-sodium demonstrated an increase toward 3^rdDAA, remaining at a high density until 60^thDAA. By comparing Copepod adults' density to the control treatment, statistics show a significant organism density alteration on the 1^st and 22^ndDAA.

For imazethapyr and imazapic treatment, no significant difference was found between this compound and control treatment among sampling days. Copepod nauplii, exposed to bispyribac-sodium, showed a decreasing density occurred on the 3^rd and 14^thDAA, in relation to the control treatment.

According to NEVES et al. (2003), the high densities of the immature forms are generally a result of the continuous reproduction of these organisms in tropical regions. The feeding habits of Copepods vary with the life phase at which they are, since adult Copepods can be carnivores (predators), detritivores and filter-feeders, whereas nauplii are filter-feeders, and frequently herbivores. It is important to point out that within the zooplankton community there is competition for food (bacteria, unicellular algae, among others) and even intra and inter-specific predation. So, toxicant exposure could increase or decrease predation rates in aquatic ecosystems. Even at sub-lethal concentrations, if predators are sensitive, pesticides may affect the survivorship of zooplankton in the presence of predators by controlling prey behavior (HANAZATO, 2001).

Among zooplankton groups, the population lowering rate cannot be attributed directly to applied herbicides, since other biological factors can interact with pesticides, creating consequences for the population of these groups (JAK et al., 1996). According to GAGNETEN (2002), herbicides can provoke zooplankton density reduction, especially among herbivorous crustaceans (Cladocers and Copepods), determine feeding decrease and algae community structure exchanges, presenting toxic effects.

CONCLUSION

During the research period (sixty-three days), the zooplankton community showed distinct responses to the tested herbicides. Most changes occurred in each sample were followed by recovery up to the end of the study. Imazethapyr and imazapic treatment provoked increasing densities of Cladocer and Copepod adult groups. Bispyribac-sodium treatment caused reduction in the density of Copepod adults and nauplii in the initial samples. Rotifers were slightly affected by imazethapyr and imazapic, manifesting fast recovery in relation to the control treatment density.

ACKNOWLEDGEMENTS

The authors thanks to Universidade Federal de Santa Maria (UFSM), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for financial support.

REFERENCES

• APHA. Standard methods for the examination of water and wastewater. 21.ed. Washington DC: American Public Health Association, 2005. 1368p.
• BAMBARADENIYA, C.N.B.; AMERASINGHE, F.P. Biodiversity associated with the rice field agroecosystem in asian countries: a brief review. Colombo: International Water Management Institute, 2003. 24p.
• CHANG, K.H. et al. Impact of pesticide application on zooplankton communities with different densities of invertebrate predators: an experimental analysis using small-scale mesocosms. Aquatic Toxicology, v.72, n.4, p.373-382, 2005. Available from: <http://www.sciencedirect.com/science/article/pii/S0166445X05000688>. Accessed: Jan. 25, 2012. doi: 10.1016/j.aquatox.2005.02.005.
  » https://doi.org/10.1016/j.aquatox.2005.02.005» http://www.sciencedirect.com/science/article/pii/S0166445X05000688
• GAGNETEN, A.M. Efectos del herbicida paraquat sobre el zooplancton. Iheringia, v.92, p.47-56, 2002. Available from: <http://www.scielo.br/scielo.php?script=sci_arttext&pid=S0073-4 7212002000300005>. Accessed: Sept. 11, 2011. doi: 10.1590/S0073-47212002000300005.
  » https://doi.org/10.1590/S0073-47212002000300005» http://www.scielo.br/scielo.php?script=sci_arttext&pid=S0073-4 7212002000300005
• GONÇALVES, F.F. Estudo de métodos empregando HPLC-DAD e LC-MS/MS para determinação de resíduos de herbicidas em água e solo do cultivo de arroz irrigado. 2007. 148f. Tese (Doutorado em Química) - Curso de Pós-graduação em Química, Universidade Federal de Santa Maria, RS.
• GURNEY, S.E.; ROBINSON, G.G.C. The influence of two triazine herbicides on the productivity, biomass and community composition of freshwater marsh periphyton. Aquatic Botany, v.36, p.1-22, 1989. Available from: <http://www.sciencedirect.com/science/article/pii/0304377089900879>. Accessed: Sept. 11, 2011. doi: 10.1016/0304-3770(89)90087-9.
  » https://doi.org/10.1016/0304-3770(89)90087-9» http://www.sciencedirect.com/science/article/pii/0304377089900879
• HANAZATO, T. Pesticide effects on freshwater zooplankton: an ecological perspective. Environmental Pollution, v.112, n.1, p.1-10, 2001. Available from: <http://www.sciencedirect.com/science/article/pii/S026974910000110X>. Accessed: Sept. 11, 2012. doi: 10.1016/S0269-7491(00)00110-X.
  » https://doi.org/10.1016/S0269-7491(00)00110-X» http://www.sciencedirect.com/science/article/pii/S026974910000110X
• HAVENS, K.E.; HANAZATO, T. Zooplankton community responses to chemical stressors: a comparison of results from acidification and pesticide contamination research. Environmental Pollution, v.82, p.277-288, 1993. Available from: <http://www.sciencedirect.com/science/article/pii/026974919390130G>. Accessed: Sept. 11, 2011. doi:10.1016/0269-7491(93)90130-G.
  » https://doi.org/doi:10.1016/0269-7491(93)90130-G» http://www.sciencedirect.com/science/article/pii/026974919390130G
• JAK, R.G. et al. Evaluation of laboratory derived toxic effect concentration of a mixture of metals by testing fresh water plankton communities in enclosures. Water Research, v.30, p.1215-1227, 1996. Available from: <http://www.sciencedirect.com/science/article/pii/0043135495002723>. Accessed: Sept. 11, 2011. doi:10.1016/0043-1354(95)00272-3.
  » https://doi.org/doi:10.1016/0043-1354(95)00272-3» http://www.sciencedirect.com/science/article/pii/0043135495002723
• KASAI, F.; HANAZATO, T. Effects of the triazine herbicide, simetryn, on freshwater plankton communities in experimental ponds. Environmental Pollution, v.89, p.197-202, 1995 . Available from: <http://www.sciencedirect.com/science/article/pii/026974919400053G>. Accessed: Sept. 11, 2011. doi: 10.1016/0269-7491(94)00053-G.
  » https://doi.org/doi: 10.1016/0269-7491(94)00053-G» http://www.sciencedirect.com/science/article/pii/026974919400053G
• KURZ, M.H.S. et al. Rapid and accurate HPLC-DAD method for the determination of the herbicide bispyribac-sodium in surface water, and its validation. Química Nova, v.32, n.6, p.1457-1460, 2009. Available from: <http://www.scielo.br/pdf/qn/v32n6/18.pdf>. Accessed: Sept. 11, 2011. doi: 10.1590/S0100-40422009000600018.
  » https://doi.org/10.1590/S0100-40422009000600018» http://www.scielo.br/pdf/qn/v32n6/18.pdf
• LUDWIG, G.M. Effects of trichlorfon, fenthion, and diflubenzuron on the zooplankton community and on production of reciprocal-cross hybrid striped bass fry in culture ponds. Aquaculture, v.110, p.301-319, 1993. Available from: <http://www.sciencedirect.com/science/article/pii/004484869390378C>. Accessed: Sept. 11, 2011. doi: 10.1016/0044-8486(93)90378-C.
  » https://doi.org/10.1016/0044-8486(93)90378-C» http://www.sciencedirect.com/science/article/pii/004484869390378C
• MARCOLIN, E. et al. Persistência do herbicida imazethapyr na lâmina de água em três sistemas de cultivo de arroz irrigado. In: REUNIÃO DA CULTURA DO ARROZ IRRIGADO, 25., 2003, Balneário Camboriú, SC. Anais... Florianópolis: EPAGRI, 2003. V.1. 686p.
• MOORE, M.T. et al. Responses of non-target aquatic organisms to aqueous propanil exposure. Bulletin of Environmental Contamination and Toxicology, v.61, n.4, p.169-174, 1998. Available from: <http://www.springerlink.com/content/4mn8ttfawbt74dba/>. Acessed: Sept. 12, 2011. doi: 10.1007/s001289900744.
  » https://doi.org/10.1007/s001289900744» http://www.springerlink.com/content/4mn8ttfawbt74dba/
• NEVES, I.F. et al. Zooplankton community structure of two marginal lakes of the river Cuiabá (Mato Grosso, Brazil) with analysis of Rotifera and Cladocera diversity. Brazilian Journal Biology, v.63, p.329-343, 2003.
• PERSCHBACHER, P.W. et al. Evaluation of effects of common aerially-applied soybean herbicides and propanil on the plankton communities of aquaculture ponds. Aquaculture, v.157, n.1-2, p.117-122, 1997. Available from: <http://www.sciencedirect.com/science/article/pii/S0044848697001476>. Accessed: Sept. 12, 2011. doi: 10.1016/S0044-8486(97)00147-6.
  » https://doi.org/10.1016/S0044-8486(97)00147-6» http://www.sciencedirect.com/science/article/pii/S0044848697001476
• PERSCHBACHER, P.W. et al. Effects of common aerially applied rice herbicides on the plankton communities of aquaculture ponds. Aquaculture, v.214, n.1-4, p.241-246, 2002. Available from: <http://www.sciencedirect.com/science/article/pii/S0044848602003964>. Accessed: Sept. 12, 2011. doi: 10.1016/S0044-8486(02)00396-4.
  » https://doi.org/10.1016/S0044-8486(02)00396-4» http://www.sciencedirect.com/science/article/pii/S0044848602003964
• RELYEA, R.A. A cocktail of contaminants: how mixtures of pesticides at low concentrations affect aquatic communities. Oecologia, v.159, p.363-376, 2009. Available from: <http://www.springerlink.com/content/3420j3486k108805>. doi: 10.1007/s00442-008-1213-9.
  » https://doi.org/10.1007/s00442-008-1213-9» http://www.springerlink.com/content/3420j3486k108805
• SÁNCHEZ, P. et al. Ecological risk assessment for rice pesticides. Spanish proposal for the development of a generic exposure scenario. In: EUROPEAN CROP PROTECTION ASSOCIATION ON ENVIRONMENTAL RISK PARAMETERS FOR USE OF PLANT PROTECTIONPRODUCTS IN RICE, 1999, Cremona, Italy. Proceedings... Cremona: Workshop Documentation, 1999. p.33-43.
• SÁNCHEZ, P. et al. Aquatic risk assessment of the new rice herbicide profoxydim. Environmental Pollution, v.142, n.1, p.181-189, 2006. Available from: <http://www.sciencedirect.com/science/article/pii/S0269749105005026>. Accessed: Sept. 13, 2011. doi: 10.1016/j.envpol.2005.08.076.
  » https://doi.org/10.1016/j.envpol.2005.08.076» http://www.sciencedirect.com/science/article/pii/S0269749105005026
• SANDERSON, H. et al. Effects of perfluorooctane sulfonate and perfluorooctanoic acid on the zooplanktonic community. Ecotoxicology and Environmental Safety, v.58, n.1, p.68-76, 2004. Available from: <http://www.sciencencedirect.com/science/article/pii/S0147651303001775>. Accessed: Sept. 13, 2011. doi: 10.1016/j.ecoenv.2003.09.012.
  » https://doi.org/10.1016/j.ecoenv.2003.09.012» http://www.sciencencedirect.com/science/article/pii/S0147651303001775
• SANTOS, F.M. et al. Persistência dos herbicidas imazethapyr e clomazone em lâmina de água do arroz irrigado. Planta Daninha, v.26, n.4, p.875-881, 2008. Available from: <http://www.scielo.br/pdf/pd/v26n4/19.pdf>. Accessed: Sept. 13, 2011. doi: 10.1590/S0100-83582008000400019.
  » https://doi.org/10.1590/S0100-83582008000400019» http://www.scielo.br/pdf/pd/v26n4/19.pdf
• SENSEMAN, S.A. Herbicide handbook. 9.ed. Lawrence, KS: Weed Science Society of America, 2007. 458p.
• SOSBAI (SOCIEDADE SUL-BRASILEIRA DE ARROZ IRRIGADO). Arroz irrigado: recomendações técnicas da pesquisa para o Sul do Brasil. Santa Maria-RS: SOSBAI, 2007. 161p.
• TARAZONA, J.V.; SANCHEZ, P. Development of an innovative conceptual model and a tiered testing strategy for the ecological risk assessment of rice pesticides. Paddy and Water Environment, v.4, p.53-59, 2006. Available from: <http://www.springerlink.com/content/h2016231k3512502/>. Accessed: Sept. 13, 2011. doi: 10.1007/s10333-005-0030-6.
  » https://doi.org/10.1007/s10333-005-0030-6» http://www.springerlink.com/content/h2016231k3512502/
• VILLARROEL, M.J. et al. Acute, chronic and sub-lethal effects of the herbicide propanil on Daphnia magna. Chemosphere, v.53, n.8, p.857-864, 2003. Available from: <http://www.sciencedirect.com/science/article/pii/S0045653503005460>. Accessed: Sept. 13, 2011. doi: 10.1016?/S0045-6535(03)00546-0.
  » https://doi.org/10.1016?/S0045-6535(03)00546-0» http://www.sciencedirect.com/science/article/pii/S0045653503005460

Publication Dates

• Publication in this collection
  Aug 2014

History

• Received
  05 Oct 2011
• Accepted
  24 Feb 2014