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Tolerance of dark septate endophytic fungi (DSE) to agrochemicals in vitro
Tolerancia de hongos endofíticos septados oscuros a agroquímicos in vitro
Federico N. Spagnoletti, Viviana M. Chiocchio
Corresponding author
chiocchi@agro.uba.ar

Corresponding author.
Cátedra de Microbiología Agrícola, Facultad de Agronomía-UBA, Instituto de Investigaciones en Biociencias Agrícolas y Ambientales-CONICET, Av. San Martín 4453, (DSE 1427) CABA, Argentina
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            "es" => "<p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">A y B&#41; Electroforesis en gel de agarosa 1&#37; de los productos de amplificaci&#243;n con los cebadores TP5&#44; espec&#237;ficos para la cepa Az39&#46; C y D&#41; Electroforesis en gel de agarosa 1&#37; de los productos de amplificaci&#243;n con los cebadores 16S rRNA espec&#237;ficos de g&#233;nero &#40;Lin et al&#46;&#44; 2011&#41; utilizados como control positivo para las cepas <span class="elsevierStyleItalic">Azospirillum</span> spp&#46; <span class="elsevierStyleItalic">Referencias</span>&#58; &#40;MM&#41; marcador de peso molecular 100<span class="elsevierStyleHsp" style=""></span>bp Trans Plus ADN Ladder&#59; &#40;1&#41; <span class="elsevierStyleItalic">A&#46; brasilense</span> Az39&#59; &#40;2&#41; <span class="elsevierStyleItalic">A&#46; brasilense</span> Sp245&#59; &#40;3&#41; <span class="elsevierStyleItalic">A&#46; brasilense</span> FP2&#59; &#40;4&#41; <span class="elsevierStyleItalic">A&#46; brasilense</span> Abv5&#59; &#40;5&#41; <span class="elsevierStyleItalic">A&#46; brasilense</span> Abv6&#59; &#40;6&#41; <span class="elsevierStyleItalic">A&#46; brasilense</span> Az 19&#59; &#40;7&#41; <span class="elsevierStyleItalic">A&#46; brasilense</span> Az 36&#59; &#40;8&#41; <span class="elsevierStyleItalic">A&#46; brasilense</span> Az 45&#59; &#40;9&#41; <span class="elsevierStyleItalic">A&#46; brasilense</span> Az 48&#59; &#40;10&#41; <span class="elsevierStyleItalic">A&#46; brasilense</span> Az 63&#59; &#40;11&#41; <span class="elsevierStyleItalic">A&#46; brasilense</span> Az 65&#59; &#40;12&#41; <span class="elsevierStyleItalic">Pseudomonas protegens</span> CHA0&#59; &#40;13&#41; <span class="elsevierStyleItalic">Bradyrhizobium japonicum</span> E109&#59; &#40;14&#41; <span class="elsevierStyleItalic">A&#46; formosense</span> CC-Nfb-7&#59; &#40;15&#41; <span class="elsevierStyleItalic">A&#46; fermentarium</span> CC-LY743&#59; &#40;16&#41; <span class="elsevierStyleItalic">A&#46; halopraeferens</span> Au4&#59; &#40;17&#41; <span class="elsevierStyleItalic">A&#46; oryzae</span> COC8&#59; &#40;18&#41; <span class="elsevierStyleItalic">A&#46; palatum</span> WW10&#59; &#40;19&#41; <span class="elsevierStyleItalic">A&#46; melinis</span> TMYC 0552&#59; &#40;20&#41; <span class="elsevierStyleItalic">A&#46; lipoferum</span> Sp59b&#59; &#40;21&#41; <span class="elsevierStyleItalic">A&#46; canadense</span> DS2&#59; &#40;22&#41; <span class="elsevierStyleItalic">A&#46; rugosum</span> IMMIB AFH-6&#59; &#40;23&#41; <span class="elsevierStyleItalic">A&#46; agr&#237;cola</span> CC-HIH038&#59; &#40;24&#41; <span class="elsevierStyleItalic">A&#46; soli</span> CC-Ly788&#59; &#40;25&#41; <span class="elsevierStyleItalic">A&#46; zeae</span> N7&#59; &#40;C-&#41; control negativo &#40;agua&#41;&#46;</p>"
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    "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Introduction</span><p id="par0005" class="elsevierStylePara elsevierViewall">Agricultural practices include the application of different pesticides to maintain crop performance by controlling insects&#44; diseases and weeds&#46; In nature&#44; pesticide residues are subjected to physical&#44; chemical and biochemical degradation processes&#44; although they persist in the environment due to their high stability and water solubility<a class="elsevierStyleCrossRef" href="#bib0310"><span class="elsevierStyleSup">22</span></a>&#46; The inadequate use of pesticides can affect microorganisms and their activity&#44; causing alterations in the biological processes that impact on soil fertility and&#44; consequently&#44; on crop productivity<a class="elsevierStyleCrossRef" href="#bib0240"><span class="elsevierStyleSup">8</span></a>&#46; 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Fungal endophytes are organisms that colonize plant tissues during a specific period of their life cycle but cause no symptoms of tissue damage to their hosts<a class="elsevierStyleCrossRef" href="#bib0345"><span class="elsevierStyleSup">29</span></a>&#46; Among this highly diverse group of endophytic fungi&#44; dark septate endophytes &#40;DSE&#41; have received much attention in the recent years<a class="elsevierStyleCrossRefs" href="#bib0335"><span class="elsevierStyleSup">27&#44;31</span></a>&#46; The genera <span class="elsevierStyleItalic">Alternaria</span> sp&#46; and <span class="elsevierStyleItalic">Curvularia</span> sp&#46; are widely known as pathogenic fungi in several cereals of commercial value<a class="elsevierStyleCrossRefs" href="#bib0205"><span class="elsevierStyleSup">1&#44;40</span></a>&#59; however&#44; species of the genera <span class="elsevierStyleItalic">Alternaria</span> and <span class="elsevierStyleItalic">Curvularia</span> &#40;teleomorph&#58; <span class="elsevierStyleItalic">Cochliobolus</span>&#41; have been found to colonize grasses&#44; playing a role as DSE fungi and promoting plant growth<a class="elsevierStyleCrossRefs" href="#bib0270"><span class="elsevierStyleSup">14&#44;24</span></a>&#46; These DSE fungi are not thought to be pathogenic&#44; as they are observed on healthy plants<a class="elsevierStyleCrossRef" href="#bib0215"><span class="elsevierStyleSup">3</span></a>&#46;</p><p id="par0015" class="elsevierStylePara elsevierViewall">Colonization patterns by DSE seem to be different according to the plant host and the cultivation system<a class="elsevierStyleCrossRef" href="#bib0305"><span class="elsevierStyleSup">21</span></a>&#46; These fungi often inhabit oligotrophic soils that are associated with the roots of hundreds of plant species in all climate regions and major biome types<a class="elsevierStyleCrossRef" href="#bib0365"><span class="elsevierStyleSup">33</span></a> as well as promoters of plant growth under greenhouse conditions<a class="elsevierStyleCrossRef" href="#bib0335"><span class="elsevierStyleSup">27</span></a>&#46; Dark septate endophytes are able to hydrolyze major C&#44; N and P polymers into usable subunits and therefore could provide N and P to the host plant<a class="elsevierStyleCrossRef" href="#bib0225"><span class="elsevierStyleSup">5</span></a>&#46; Newsham<a class="elsevierStyleCrossRef" href="#bib0305"><span class="elsevierStyleSup">21</span></a> performed a meta-analysis of independent studies to assess the inoculation of DSE in different crops&#44; concluding that the contents of N and P in inoculated plant biomass were higher compared to non-inoculated plants&#46; Conversely&#44; another meta-analysis suggested negative to neutral effects of DSE inoculations<a class="elsevierStyleCrossRef" href="#bib0290"><span class="elsevierStyleSup">18</span></a>&#46;</p><p id="par0020" class="elsevierStylePara elsevierViewall">Wheat is one of the winter cereals of major importance in Latin America&#46; Agricultural production is one of the fundamental economic activities of Argentina&#44; which is among the main world producers of crops such as soybeans&#44; wheat&#44; sunflower and corn&#46; In Argentina&#44; the production area destined for the wheat crop was estimated in 5&#46;95 million hectares&#44; producing 18 million tons of the cereal<a class="elsevierStyleCrossRef" href="#bib0295"><span class="elsevierStyleSup">19</span></a>&#46; Most studies have evaluated mycorrhizal and DSE root colonization in different hosts and Argentine regions<a class="elsevierStyleCrossRefs" href="#bib0285"><span class="elsevierStyleSup">17&#44;28</span></a>&#46; Nevertheless&#44; little information is available about the biology of DSE isolated from cereals<a class="elsevierStyleCrossRefs" href="#bib0335"><span class="elsevierStyleSup">27&#44;31</span></a>&#46; The widespread use of pesticides has raised concerns about their potential impact on microbial communities and in this sense there are no studies evaluating the effects of agrochemicals on DSE&#46; Therefore&#44; the aim of this study is to isolate DSE from wheat roots and to assess the tolerance of isolated strains to different chemicals commonly used in agricultural practices&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0030">Materials and methods</span><p id="par0025" class="elsevierStylePara elsevierViewall">Thirty wheat plants were randomly collected from two sites located in Arenales and Ferr&#233; in July 2011 &#40;Buenos Aires Province&#44; Argentina&#41;&#46; The plants were at phenological stage Z5&#46; Samples were transported to the laboratory and placed in a cold chamber at 4<span class="elsevierStyleHsp" style=""></span>&#176;C until their use&#46; The roots were washed under tap water and sterilized superficially by immersing them in 70&#37; ethanol for 2<span class="elsevierStyleHsp" style=""></span>min followed by 1&#37; sodium hypochlorite &#40;NaOCl&#41; for 3<span class="elsevierStyleHsp" style=""></span>min and thoroughly rinsed five times with sterile distilled water&#46; Subsequently&#44; twenty five root pieces &#40;5<span class="elsevierStyleHsp" style=""></span>mm&#41; of each plant were placed into drops of Gel-Gro &#40;ICN Biochemicals&#44; USA&#41; with streptomycin and tetracycline hydrochloride 1&#37; &#40;Sigma&#8211;Aldrich&#44; USA&#41; in sterile Petri Plates 30 Plates<a class="elsevierStyleCrossRef" href="#bib0350"><span class="elsevierStyleSup">30</span></a>&#46; The root pieces were incubated in the dark at 25<span class="elsevierStyleHsp" style=""></span>&#176;C and were periodically observed under a stereoscopic microscope &#40;Nikon H550S&#44; Japan&#41;&#46; The segments of roots in which fungal growth was observed were placed on plates containing Malt Extract Agar &#40;MEA&#41; and cultured on such medium at 25<span class="elsevierStyleHsp" style=""></span>&#176;C&#44; thereby obtaining several isolates&#46; The endophytic nature of the thirty isolates was corroborated following the test of resynthesis &#40;Koch&#39;s postulates&#41; under greenhouse conditions<a class="elsevierStyleCrossRef" href="#bib0355"><span class="elsevierStyleSup">31</span></a>&#46; Five isolates were identified following classical<a class="elsevierStyleCrossRefs" href="#bib0250"><span class="elsevierStyleSup">10&#44;36</span></a> and molecular methodologies<a class="elsevierStyleCrossRef" href="#bib0355"><span class="elsevierStyleSup">31</span></a>&#46; The strains were deposited at the Fungi Bank of the Facultad de Agronom&#237;a&#44; Universidad de Buenos Aires<a class="elsevierStyleCrossRef" href="#bib0335"><span class="elsevierStyleSup">27</span></a>&#46; Two isolates were selected for this assay due to their extracellular enzymatic production<a class="elsevierStyleCrossRef" href="#bib0375"><span class="elsevierStyleSup">35</span></a>&#44; their phosphorus solubilization<a class="elsevierStyleCrossRef" href="#bib0355"><span class="elsevierStyleSup">31</span></a> and their tolerance to different sodium salts<a class="elsevierStyleCrossRef" href="#bib0360"><span class="elsevierStyleSup">32</span></a>&#46;</p><p id="par0030" class="elsevierStylePara elsevierViewall">A culture of each strain grown on MEA for 7 days at 25<span class="elsevierStyleHsp" style=""></span>&#176;C was used as inoculum to evaluate their tolerance to pesticides&#46; Subsequently&#44; two successive picks were conducted on basal salt medium &#40;BSM&#41;<a class="elsevierStyleCrossRef" href="#bib0275"><span class="elsevierStyleSup">15</span></a> with the purpose of causing them a nutritional stress &#40;starvation&#41;&#46; The BSM containing the herbicide &#40;glyphosate&#41;&#44; the fungicide &#40;carbendazim&#41; or the insecticide &#40;cypermethrin&#41; was used in an agronomic common dose &#40;AD&#41;&#44; 2 AD and 10 AD&#46; Doses per Petri dish were 0&#46;20<span class="elsevierStyleHsp" style=""></span>ppm&#44; 0&#46;40<span class="elsevierStyleHsp" style=""></span>ppm and 2<span class="elsevierStyleHsp" style=""></span>ppm for the herbicide&#59; 18&#46;12<span class="elsevierStyleHsp" style=""></span>ppm&#44; 36&#46;25<span class="elsevierStyleHsp" style=""></span>ppm and 181&#46;25<span class="elsevierStyleHsp" style=""></span>ppm for the fungicide&#59; and 2&#46;02<span class="elsevierStyleHsp" style=""></span>ppm&#44; 4&#46;04<span class="elsevierStyleHsp" style=""></span>ppm and 20&#46;2<span class="elsevierStyleHsp" style=""></span>ppm for the insecticide respectively&#46; The control treatment was BSM medium plus sucrose &#40;2&#37;&#41;&#46; The inoculum was standardized using 5<span class="elsevierStyleHsp" style=""></span>mm-diameter disks obtained from the zone with active growth of a colony with 7 days of growth for all strains and all tested media&#46; Each agrochemical dose and its respective control were tested in quintuplicate&#46; Fungal growth was assessed periodically from the third day by measuring the colony diameter at 12 days&#46; Fungal growth rates were analyzed using the following formula<a class="elsevierStyleCrossRef" href="#bib0330"><span class="elsevierStyleSup">26</span></a>&#58; Growth rate<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>&#40;Fd<span class="elsevierStyleHsp" style=""></span>&#8722;<span class="elsevierStyleHsp" style=""></span>Id&#41;&#47;&#40;Ft<span class="elsevierStyleHsp" style=""></span>&#8722;<span class="elsevierStyleHsp" style=""></span>&#41;&#44; where&#58; Fd is the final diameter &#40;cm&#41;&#44; Id is the initial diameter &#40;cm&#41;&#44; Ft is the final time &#40;days&#41; and It is the initial time &#40;days&#41;&#46;</p><p id="par0035" class="elsevierStylePara elsevierViewall">Moreover&#44; the inhibition percentage was calculated for each fungi and each agrochemical at 6 and 12 days using the following formula&#58; Inhibition &#40;&#37;&#41;<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>&#40;Cd<span class="elsevierStyleHsp" style=""></span>&#8722;<span class="elsevierStyleHsp" style=""></span>Td&#41;&#47;Cd<span class="elsevierStyleHsp" style=""></span>&#215;<span class="elsevierStyleHsp" style=""></span>100&#44; where&#58; Cd is the mean colony diameter in the control treatment &#40;cm&#41; and Td is the mean colony diameter in the agrochemical treatment &#40;cm&#41;&#46;</p></span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Statistical analysis</span><p id="par0040" class="elsevierStylePara elsevierViewall">A two-way analysis of variance &#40;ANOVA&#41; with DSE strains &#40;<span class="elsevierStyleItalic">A&#46; alternata</span> and <span class="elsevierStyleItalic">Cochliobolus</span> sp&#46;&#41; and agrochemical type &#40;4 levels&#58; 0&#59; AD&#59; 2 AD&#59; 10 AD&#41; as factors was performed from the data obtained on growth parameters and effective concentration &#40;EC 50&#41; using the statistical software Infostat Professional version 2&#46;0&#46; Normality and homogeneity of variance were tested&#46; Comparisons were made using the Tukey&#39;s test with <span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;05&#46;</p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Results</span><p id="par0045" class="elsevierStylePara elsevierViewall">The physicochemical properties of the soil &#40;Typic Argiudoll&#41; were&#58; organic carbon 1&#46;7&#37;&#44; available phosphorous 15&#46;0<span class="elsevierStyleHsp" style=""></span>mg&#47;kg &#40;Kurtz and Bray No&#46; 1 method&#41;&#44; pH 6&#46;2&#44; electrical conductivity 0&#46;5<span class="elsevierStyleHsp" style=""></span>d&#47;Sm clay 27&#46;5&#37;&#44; silt 50&#46;5&#37; and sand 22&#37;&#46; <a class="elsevierStyleCrossRef" href="#fig0005">Figure 1</a> shows the morphology of the DSE colony of <span class="elsevierStyleItalic">A&#46; alternata</span> and <span class="elsevierStyleItalic">Cochliobolus</span> sp&#46;</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><p id="par0050" class="elsevierStylePara elsevierViewall">The strain <span class="elsevierStyleItalic">Cochliobolus</span> sp&#46; reached a diameter of 75<span class="elsevierStyleHsp" style=""></span>mm of the colony after 12 days of growth while <span class="elsevierStyleItalic">A&#46; alternata</span> completed the culture dish &#40;90<span class="elsevierStyleHsp" style=""></span>mm&#41; after 9 days &#40;data not shown&#41;&#46; There was significant change in the kinetics of growth of the strains by adding the different kinds of agrochemicals to the medium&#46; The results from the two-way analysis of variance showed that there were significant interactions between the DSE strains and the agrochemicals in growth rate &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;0001&#41;&#46; Therefore&#44; this interaction was further analyzed&#46; <a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a> shows that the growth of <span class="elsevierStyleItalic">A&#46; alternata</span> was significantly faster than that of <span class="elsevierStyleItalic">Cochliobolus</span> sp&#46; in the control treatment and was less affected than <span class="elsevierStyleItalic">Cochliobolus</span> sp&#46; when the agrochemicals were added&#46;</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><p id="par0055" class="elsevierStylePara elsevierViewall">The presence of glyphosate reduced the growth rate of both DSE strains&#46; <span class="elsevierStyleItalic">A&#46; alternata</span> showed significant differences in AD and 2 AD regarding <span class="elsevierStyleItalic">Cochliobolus</span> sp&#46;&#59; however&#44; when the dose was increased to 10 AD&#44; no differences were found between both strains&#46;</p><p id="par0060" class="elsevierStylePara elsevierViewall">The fungicide carbendazim was the most tolerated agrochemical by the DSE strains&#46; The growth rate of <span class="elsevierStyleItalic">A&#46; alternata</span> was reduced by the addition of carbendazim as its dose increased in the solid media&#46; No differences were found in 2 AD between both fungi &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#46; On the other hand&#44; the insecticide &#40;cypermethrin&#41; was the most toxic agrochemical on growth rate&#46; <span class="elsevierStyleItalic">A&#46; alternata</span> reduced its growth rate as the dose of cypermethrin increased in the media&#44; while a dose equal to or greater than 2 AD inhibited the growth of <span class="elsevierStyleItalic">Cochliobolus</span> sp&#46; &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#46;</p><p id="par0065" class="elsevierStylePara elsevierViewall">The percentages of growth inhibition are shown in <a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a>A&#8211;C&#46; The herbicide &#40;<a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a>A&#41; increased this parameter &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;05&#41; in all the agrochemicals and doses tested for both fungi and on both days evaluated &#40;day 6 and day 12&#41;&#46; The fungicide increased the growth inhibition percentage of <span class="elsevierStyleItalic">Cochliobolus</span> sp&#46;&#59; however&#44; an induction of the growth of <span class="elsevierStyleItalic">A&#46;</span><span class="elsevierStyleItalic">alternata</span> was observed when the fungicide was added at AD and 2 AD evaluated at 6 days&#46; In these doses&#44; at the end of the growth &#40;day 12&#41; no significant differences were detected with respect to the control treatment&#46; For both evaluation days&#44; the addition of carbendazim at 10 AD generated a significant increase &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;05&#41; in the inhibition percentage &#40;<a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a>B&#41;&#46;</p><elsevierMultimedia ident="tbl0010"></elsevierMultimedia><p id="par0070" class="elsevierStylePara elsevierViewall"><a class="elsevierStyleCrossRef" href="#tbl0010">Table 2</a>C shows the percentages of growth inhibition generated by the insecticide&#46; The DSE <span class="elsevierStyleItalic">Cochliobolus</span> sp&#46; exhibited significant inhibition when the AD was placed in the culture medium &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;05&#41;&#59; however&#44; no changes were detected between 2 AD and 10 AD&#46; On the contrary&#44; <span class="elsevierStyleItalic">A&#46; alternata</span> recorded increases in inhibition in all the doses studied &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;05&#41;&#46;</p><p id="par0075" class="elsevierStylePara elsevierViewall">The concentrations of the agrochemicals that caused a 50&#37; reduction in fungal growth compared to the control &#40;effective concentration&#58; EC 50&#41; varied depending on the agrochemical type &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>&#41;&#46; In all the agrochemicals analyzed&#44; the fungus <span class="elsevierStyleItalic">A&#46; alternata</span> was the most tolerant&#44; presenting higher EC 50&#46; The insecticide was the agrochemical that caused the greatest effect on DSE growth&#44; followed by the herbicide&#46; The fungicide proved to be the least toxic agrochemical for these fungi &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>&#41;&#46; <span class="elsevierStyleItalic">Cochliobolus</span> sp&#46; did not differ significantly from <span class="elsevierStyleItalic">A&#46; alternata</span> in the EC 50 against carbendazim&#46;</p><elsevierMultimedia ident="fig0010"></elsevierMultimedia></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Discussion</span><p id="par0080" class="elsevierStylePara elsevierViewall">This study evaluates the tolerance of two DSE fungi to different agrochemicals&#46; The tested DSE fungi were isolates of <span class="elsevierStyleItalic">A&#46;</span><span class="elsevierStyleItalic">alternata</span> and <span class="elsevierStyleItalic">Cochliobolus</span> sp&#46; It is known that these fungi are grass pathogens&#59; however&#44; several studies have shown that they can also be found in the roots as DSE as non-pathogenic fungi<a class="elsevierStyleCrossRefs" href="#bib0215"><span class="elsevierStyleSup">3&#44;37</span></a>&#46; Therefore&#44; the fungal species classified as non-pathogenic cause disease symptoms in certain host plants but are neutral or beneficial in other hosts&#46;</p><p id="par0085" class="elsevierStylePara elsevierViewall">Moreover&#44; although pesticides are designed to be as specific as possible&#44; they have effects on non-target fungal organisms&#46; In accordance with our results&#44; glyphosate &#40;using equivalent herbicide concentrations&#41; had an <span class="elsevierStyleItalic">in vitro</span> toxic effect on culturable mycobiota &#40;<span class="elsevierStyleItalic">Aspergillus</span> section Flavi&#41; strains from agricultural soils<a class="elsevierStyleCrossRef" href="#bib0230"><span class="elsevierStyleSup">6</span></a>&#46; Likewise&#44; other authors<a class="elsevierStyleCrossRef" href="#bib0260"><span class="elsevierStyleSup">12</span></a> found a reduction of microbial biomass at a higher glyphosate concentration and a temporary inhibitory effect at recommended field doses&#46; Furthermore&#44; effects of glyphosate on soil microbial communities and its mineralization in soils after various applications of this herbicide have been found<a class="elsevierStyleCrossRef" href="#bib0280"><span class="elsevierStyleSup">16</span></a>&#46; A recent study<a class="elsevierStyleCrossRef" href="#bib0255"><span class="elsevierStyleSup">11</span></a> also demonstrated behavioral differences between glyphosate and its major metabolite&#44; AMPA&#44; related to the physical properties of saturated hydraulic conductivity &#40;Ks&#41; and soil moisture&#46; Other authors found that glyphosate affects arbuscular mycorrhizal fungi due to a reduction in spore viability&#44; root colonization and arbuscule percentage<a class="elsevierStyleCrossRef" href="#bib0245"><span class="elsevierStyleSup">9</span></a>&#46; However&#44; DSEs are more tolerant to different types of stress than other soil fungi<a class="elsevierStyleCrossRef" href="#bib0315"><span class="elsevierStyleSup">23</span></a>&#46; This could be due to the fact that the chemical compounds act effectively on the mycelium&#44; while spores and chlamydospores are more resistant to these compounds due to their low activity given their water content and the presence of a large amount of unsaturated fatty acids<a class="elsevierStyleCrossRef" href="#bib0220"><span class="elsevierStyleSup">4</span></a>&#46;</p><p id="par0090" class="elsevierStylePara elsevierViewall">There is much less research on the effect of carbendazim on fungi&#46; However&#44; this fungicide has detrimental effects to fungal and bacterial biocontrol agents such as <span class="elsevierStyleItalic">Trichoderma harzianum</span>&#44; <span class="elsevierStyleItalic">Trichoderma virens</span>&#44; <span class="elsevierStyleItalic">Bacillus subtilis</span> and <span class="elsevierStyleItalic">Pseudomonas fluorescens</span><a class="elsevierStyleCrossRef" href="#bib0300"><span class="elsevierStyleSup">20</span></a>&#46; In this research&#44; we found that DSE strains have the potential to tolerate high concentrations &#40;181&#46;25<span class="elsevierStyleHsp" style=""></span>ppm&#44; 10 AD&#41; of fungicide&#59; these results are in accordance with those of others authors<a class="elsevierStyleCrossRef" href="#bib0210"><span class="elsevierStyleSup">2</span></a>&#46; One study showed that the type of fungicide applied to the soil must be seriously considered as the authors detected negative effects on <span class="elsevierStyleItalic">Rhizophagus fasciculatus</span> &#40;arbuscular mycorrhizal fungi&#41; with benomyl &#40;systemic benzimidazole&#41;&#59; however&#44; they found no effects when captan &#40;non-systemic fungicide&#41;<a class="elsevierStyleCrossRef" href="#bib0235"><span class="elsevierStyleSup">7</span></a> was applied&#46; Nevertheless&#44; our results showed high tolerance of DSE fungi against carbendazim&#44; which is a derivative of benomyl&#46; <span class="elsevierStyleItalic">Bipolaris tetramera</span> and <span class="elsevierStyleItalic">A&#46; alternata</span> have potential to tolerate and degrade 100<span class="elsevierStyleHsp" style=""></span>ppm of carbendazim <span class="elsevierStyleItalic">in vitro</span><a class="elsevierStyleCrossRef" href="#bib0390"><span class="elsevierStyleSup">38</span></a>&#46; In accordance with that article&#44; we found negative inhibition values in agronomic doses&#44; 2 AD and no differences compared with control&#46; These results would indicate an <span class="elsevierStyleItalic">Alternaria</span> sp&#46; promotion growth when grown with the addition of carbendazim&#46;</p><p id="par0095" class="elsevierStylePara elsevierViewall">In the case of cypermethrin&#44; there are studies that demonstrate that this insecticide caused a negative effect on soil enzymatic activities and microbial diversity<a class="elsevierStyleCrossRef" href="#bib0370"><span class="elsevierStyleSup">34</span></a>&#46; Our DSE strains showed low cypermethrin tolerance&#44; high inhibition percentage and low EC50&#46; Nevertheless&#44; a study revealed that when the pesticide is applied on pepper plants there is an increase in bacterial abundance and a change in the composition of the community of the Firmicutes phylum to Bacteroidetes and &#947;-Proteobacteria phyla<a class="elsevierStyleCrossRef" href="#bib0395"><span class="elsevierStyleSup">39</span></a>&#46; Other authors showed the potential of <span class="elsevierStyleItalic">Aspergillus niger</span>&#44; <span class="elsevierStyleItalic">Aspergillus terreus</span>&#44; <span class="elsevierStyleItalic">Monilochaetes</span> and <span class="elsevierStyleItalic">Fusarium</span> strains in the biodegradation of 50&#8211;150<span class="elsevierStyleHsp" style=""></span>ppm of this pyrethroid<a class="elsevierStyleCrossRef" href="#bib0325"><span class="elsevierStyleSup">25</span></a>&#46;</p><p id="par0100" class="elsevierStylePara elsevierViewall">This research has shown that agrochemicals commonly used in agriculture have detrimental effects on the growth of DSE fungi&#44; even when these agrochemicals are used at recommended doses&#59; however&#44; these negative effects vary according to the agrochemical considered&#46; Moreover&#44; this paper makes evident that DSE response to this type of toxin depends on the studied species of DSE fungus&#46; This research is a contribution to a better understanding of the behavior of DSE against xenobiotics&#44; evaluating the tolerance and&#47;or their use as a source of nutrients&#46;</p></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Conclusion</span><p id="par0105" class="elsevierStylePara elsevierViewall">The DSE <span class="elsevierStyleItalic">A&#46; alternata</span> tolerates all three agrochemicals at the tested doses while <span class="elsevierStyleItalic">Cochliobolus</span> sp&#46; is glyphosate and carbendazim-tolerant in all three doses but shows no tolerance to cypermethrin when the agronomic dose is twofold&#46; In general&#44; there is a decrease in the growth of the strains when increasing the dose of the agrochemicals studied&#46;</p></span><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0055">Conflict of interest</span><p id="par0110" class="elsevierStylePara elsevierViewall">The authors declare that they have no conflicts of interest&#46;</p></span></span>"
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        "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Dark septate endophytes &#40;DSE&#41; are a heterogeneous group of fungi&#44; mostly belonging to the Phylum Ascomycota&#44; that are involved in a mutualistic symbiosis with plant roots&#46; The aim of this study is to evaluate the behavior of two strains of DSE isolated from wheat roots of two cropping areas in the province of Buenos Aires&#44; Argentina&#44; against some agrochemicals&#46; Of all the isolates obtained&#44; two strains were identified as <span class="elsevierStyleItalic">Alternaria alternata</span> and <span class="elsevierStyleItalic">Cochliobolus</span> sp&#46; These DSE were found to be tolerant to glyphosate&#44; carbendazim and cypermethrin when evaluated at the recommended agronomic dose &#40;AD&#41;&#44; 2 AD and&#44; in some cases&#44; 10 AD&#46; This work contributes to the study of the biology of this group of fungi and their tolerance in the presence of xenobiotics widely used in agriculture&#46;</p></span>"
      ]
      "es" => array:2 [
        "titulo" => "Resumen"
        "resumen" => "<span id="abst0010" class="elsevierStyleSection elsevierViewall"><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">Los end&#243;fitos septados oscuros &#40;DSE&#41; son un grupo heterog&#233;neo de hongos que participan de una simbiosis mutualista con ra&#237;ces de plantas&#44; perteneciendo principalmente al <span class="elsevierStyleItalic">Phylum</span><span class="elsevierStyleItalic">Ascomycota</span>&#46; El objetivo de este estudio fue aislar DSE de ra&#237;ces de trigo proveniente de dos &#225;reas de cultivo de la provincia de Buenos Aires y evaluar el comportamiento de dos cepas de DSE aisladas de ra&#237;ces de trigo frente a algunos agroqu&#237;micos en dos &#225;reas de cultivo de la provincia de Buenos Aires&#46; De todos los aislamientos obtenidos se seleccionaron dos cepas que se identificaron como <span class="elsevierStyleItalic">Alternaria alternata</span> y <span class="elsevierStyleItalic">Cochliobolus</span> sp&#46; Se encontr&#243; que estos DSE son tolerantes al glifosato&#44; el carbendazim y la cipermetrina&#44; evaluados a las dosis agron&#243;micas recomendadas &#40;AD&#41;&#44; a 2x AD y&#44; en algunos casos&#44; a 10x AD&#46; Este trabajo contribuye al conocimiento de la biolog&#237;a de este grupo de hongos y su tolerancia a xenobi&#243;ticos ampliamente utilizados en la agricultura&#46;</p></span>"
      ]
    ]
    "multimedia" => array:4 [
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        "etiqueta" => "Figure 1"
        "tipo" => "MULTIMEDIAFIGURA"
        "mostrarFloat" => true
        "mostrarDisplay" => false
        "figura" => array:1 [
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          "en" => "<p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">Morphology of DSE&#39;s colony grown in MEA plate&#46; &#40;A&#41; <span class="elsevierStyleItalic">Alternaria alternata</span>&#46; &#40;B&#41; <span class="elsevierStyleItalic">Cochliobolus</span> sp&#46;</p>"
        ]
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      1 => array:7 [
        "identificador" => "fig0010"
        "etiqueta" => "Figure 2"
        "tipo" => "MULTIMEDIAFIGURA"
        "mostrarFloat" => true
        "mostrarDisplay" => false
        "figura" => array:1 [
          0 => array:4 [
            "imagen" => "gr2.jpeg"
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        "descripcion" => array:1 [
          "en" => "<p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">Effective concentration &#40;EC 50&#41;&#44; the concentrations of the herbicide&#44; fungicide and insecticide that caused a 50&#37; reduction in fungal growth compared to the control&#46; Means<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>SD &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>5&#41;&#46; Different letters differ significantly &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;05&#41;&#46;</p>"
        ]
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        "etiqueta" => "Table 1"
        "tipo" => "MULTIMEDIATABLA"
        "mostrarFloat" => true
        "mostrarDisplay" => false
        "detalles" => array:1 [
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        "tabla" => array:2 [
          "leyenda" => "<p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">4 levels of agrochemicals&#58; 0&#59; AD &#40;agronomic dose&#41;&#59; 2 AD&#59; 10 AD&#46; Means<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>SD &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>5&#41;&#46; Different letters differ significantly &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;05&#41;&#46;</p>"
          "tablatextoimagen" => array:1 [
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                  \t\t\t\t\tvoid\n
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                  \t\t\t\t ; entry_with_role_rowhead " align="center" valign="\n
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                  \t\t\t\t" scope="col">Agrochemicals&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="center" valign="\n
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                  \t\t\t\t" scope="col">Treatments&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " colspan="2" align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">DSE strains</th></tr><tr title="table-row"><th class="td" title="\n
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                  \t\t\t\t  " align="" valign="\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="" valign="\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="center" valign="\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black"><span class="elsevierStyleItalic">Cochliobolus</span> sp&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th><th class="td" title="\n
                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="center" valign="\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black"><span class="elsevierStyleItalic">Alternaria alternata</span>&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " rowspan="4" align="center" valign="\n
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                  \t\t\t\t">Glyphosate</td><td class="td" title="\n
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                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Control&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
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                  \t\t\t\t">0&#46;53<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;06 b&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t  " align="center" valign="\n
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                  \t\t\t\t">0&#46;58<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;01 a&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
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                  \t\t\t\t ; entry_with_role_rowhead " align="center" valign="\n
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                  \t\t\t\t">AD&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
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                  \t\t\t\t">0&#46;25<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;01 e&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t  " align="center" valign="\n
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                  \t\t\t\t">0&#46;42<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;02 c&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">2 AD&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">0&#46;22<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;01 f&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">0&#46;37<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;03 d&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">10 AD&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">0&#46;05<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;01<span class="elsevierStyleHsp" style=""></span>g&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">0&#46;03<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;00<span class="elsevierStyleHsp" style=""></span>g&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " rowspan="4" align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Carbendazim</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Control&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">0&#46;53<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;06 b&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
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                  \t\t\t\t">0&#46;58<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;01 a&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">AD&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">0&#46;42<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;00 c&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">0&#46;51<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;00 b&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">2 AD&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">0&#46;46<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;05 c&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">0&#46;46<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;02 c&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">10 AD&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">0&#46;21<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;05 f&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">0&#46;33<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;02 d&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " rowspan="4" align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Cypermethrin</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Control&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">0&#46;53<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;06 b&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">0&#46;58<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;01 a&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">AD&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">0&#46;19<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;04 f&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">0&#46;54<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;02 b&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">2 AD&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">0&#46;00<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;00<span class="elsevierStyleHsp" style=""></span>g&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">0&#46;20<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;00 f&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">10 AD&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">0&#46;00<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;00<span class="elsevierStyleHsp" style=""></span>g&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">0&#46;03<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;00<span class="elsevierStyleHsp" style=""></span>g&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr></tbody></table>
                  """
              ]
              "imagenFichero" => array:1 [
                0 => "xTab2257471.png"
              ]
            ]
          ]
        ]
        "descripcion" => array:1 [
          "en" => "<p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">Growth rate of <span class="elsevierStyleItalic">Cochliobolu</span>s sp&#46; and <span class="elsevierStyleItalic">Alternaria</span><span class="elsevierStyleItalic">alternata</span> &#40;DSE strains&#41;&#46; Comparison between DSE strains <span class="elsevierStyleItalic">A&#46; alternata</span> and <span class="elsevierStyleItalic">Cochliobolus</span> sp&#46; and agrochemical type</p>"
        ]
      ]
      3 => array:8 [
        "identificador" => "tbl0010"
        "etiqueta" => "Table 2"
        "tipo" => "MULTIMEDIATABLA"
        "mostrarFloat" => true
        "mostrarDisplay" => false
        "detalles" => array:1 [
          0 => array:3 [
            "identificador" => "at2"
            "detalle" => "Table "
            "rol" => "short"
          ]
        ]
        "tabla" => array:2 [
          "leyenda" => "<p id="spar0040" class="elsevierStyleSimplePara elsevierViewall">Each value represents the mean value<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>SD &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>5&#41;&#46; Different letters differ significantly &#40;<span class="elsevierStyleItalic">p</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>0&#46;05&#41;&#46;</p>"
          "tablatextoimagen" => array:3 [
            0 => array:2 [
              "tabla" => array:1 [
                0 => """
                  <table border="0" frame="\n
                  \t\t\t\t\tvoid\n
                  \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td-with-role" title="\n
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                  \t\t\t\t ; entry_with_role_rowhead " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col">&#40;A&#41; Strains&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="center" valign="\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">AD&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="center" valign="\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">2 AD&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">10 AD&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " rowspan="2" align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t"><span class="elsevierStyleItalic">Cochliobolus</span> sp&#46;</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">6&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">0&#46;00<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;00 a&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">36&#46;70<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>2&#46;14 b&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">41&#46;53<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;91 c&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">78&#46;68<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>1&#46;25 d&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">12&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t">0&#46;00<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;00 a&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">44&#46;28<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>1&#46;90 b&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">50&#46;56<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>1&#46;23 c&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
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                  \t\t\t\t">84&#46;29<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>2&#46;25 d&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " rowspan="2" align="center" valign="\n
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                  \t\t\t\t"><span class="elsevierStyleItalic">A&#46;</span><span class="elsevierStyleItalic">alternata</span></td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">6&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">0&#46;00<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;00 a&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">35&#46;86<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>3&#46;25 b&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">46&#46;89<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>1&#46;98 c&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">78&#46;96<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>1&#46;30 d&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
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                  \t\t\t\t\ttop\n
                  \t\t\t\t">12&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">0&#46;00<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;00 a&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">24&#46;95<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>3&#46;68 b&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">36&#46;00<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>3&#46;14 c&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="center" valign="\n
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                  \t\t\t\t">81&#46;87<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>3&#46;95 d&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr></tbody></table>
                  """
              ]
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                0 => "xTab2257470.png"
              ]
            ]
            1 => array:2 [
              "tabla" => array:1 [
                0 => """
                  <table border="0" frame="\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="center" valign="\n
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                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="center" valign="\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">2 AD&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-head\n
                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">10 AD&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
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                  \t\t\t\t"><span class="elsevierStyleItalic">Cochliobolus</span> sp&#46;</td><td class="td" title="\n
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                  \t\t\t\t  " align="center" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">6&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
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                  \t\t\t\t">0&#46;00<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;00 a&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">6&#46;37<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>3&#46;42 b&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
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                  \t\t\t\t">10&#46;76<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>3&#46;59 b&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="center" valign="\n
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                  \t\t\t\t">0&#46;00<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>0&#46;00 b&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="center" valign="\n
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                  \t\t\t\t">&#8722;4&#46;31<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>1&#46;05 a&nbsp;\t\t\t\t\t\t\n
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ISSN: 03257541
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