Introduction

The red palm mite, Raoiella indica Hirst (Acari: Tenuipalpidae), is the most important and invasive pest introduced in the Americas (^{Amaro and Gomes, 2012}; ^{Dowling et al., 2012}; ^{Kane et al., 2012}). This pest has spread rapidly in the Caribbean countries (^{Rodrigues et al., 2007}; ^{Roda et al., 2008}), Florida, USA (^{Cocco and Hoy, 2009}), Mexico (^{NAPPO, 2009}), Brazil (^{Navia et al., 2011}), Colombia (^{Carrillo et al., 2011}), and Venezuela (^{Vásquez and De Moraes, 2013}). The presence of R. indica in the Neotropical region affects mainly to economically-important crops such as coconut (Cocos nucifera L.), bananas (Musa spp.) and tropical flowers of the Heliconiaceae family (^{Amaro and Gomes, 2012}; ^{Carrillo et al., 2012}; ^{Dowling et al., 2012}; ^{Kane et al., 2012}).

After detecting this pest in Mexico, the Federal Government implemented the campaign against the red palm mite, through the Servicio Nacional de Sanidad, Inocuidad y Calidad Agroalimentaria (National Health, Innocuousness, and Agrifood Quality Service: SENASICA). Its purpose was to reduce infestation levels and to mitigate the propagation risk to domestic agricultural areas. The operational strategy includes sampling, diagnosis, and control of infestation points by means of sanitary pruning and application of acaricides (^{SENASICA, 2013}). However, the pest has spread in the country (^{SENASICA, 2015}).

The chemical control of mites is crucial for the comprehensive handling programs for pest in the world and it is unlikely that it will be eliminated soon (^{Van Leeuwen et al., 2015}). Besides, chemical treatments are useful to control population outbreaks (^{Fountain et al., 2010}) or to mitigate their propagation (^{De Assis et al., 2013}). One challenge of chemical control is using innocuous acaricides or that cause little damage to the beneficial fauna and mammals, and with short environmental persistence (^{Dekeyser, 2005}; ^{Van Leeuwen et al., 2015}).

Mites include pest species with high potential to develop resistance to acaricides (^{Whalon et al., 2008}). Acaricides are applied with more frequency than other pesticides, due to the mites’ high fertility and short life cycle, which result in the rapid development of resistance (^{Van Leeuwen et al., 2010}). In order to delay that development, actions such as alternation, sequencing, rotation, and the use of compound mixtures with different action mechanisms are suggested (^{Marcic, 2012}). For this reason, the main challenge to effective chemical control lies in recognizing the basic toxicity of local acaricides. Rotating acaricides with different mechanisms of action is necessary, in order to diversify the mortality mechanism (^{Whalon et al., 2008}). The use of a single active ingredient for pest control will continue promoting rapid resistance (^{Whalon et al., 2008}).

In Mexico, researches about the potential of R. indica’s natural predators are inconclusive, and acaricides are still used in the campaign against red palm mite (^{SENASICA, 2015}). The Comisión Federal para la Protección contra Riesgos Sanitarios (Federal Commission for the Protection Against Sanitary Risks) temporarily recommended and authorized these acaricides: abamectin, spiridiclofen, and sulfur (COFEPRIS) (^{SENASICA, 2013}). This recommendation is based on the information generated in Brazil (^{De Assis et al., 2013}), and Puerto Rico and USA (^{Rodrigues and Peña, 2012}). Our hypothesis was that R. indica local populations have different responses to these acaricides. In addition, some of the recommended chemicals are not authorized or available in Mexico. With this background, the objective of this study was to determine the lethal concentration (50 % and 90 %) against R. indica of the commercial acaricides available in Mexico. This information is necessary solve emergency situations that involve the chemical control of this pest and to lay the foundations for a strategy to make a rational use of acaricides.

Materials and Methods

Acaricides evaluated

The selected acaricides are chemicals products for agricultural use and control of different species of fruit, vegetables and ornamental phytophagous mites. All acaricides have in force registration in ^{COFEPRIS, 2015} and they are sold in the study area (Table 1). The acaricides were used following the suggestions included in the products’ labels and bibliography (^{Dekeyser, 2005}; ^{Marcic, 2012}; ^{Sparks and Nauen, 2015}; ^{Van Leeuwen et al., 2015}). Acaricides that only affect the immature stages were discarded, because the bioassays were conducted in adult mites.

Table 1 Chacaracteristics of the acaricides used against adult red palm mite Raioella indica 

†Insecticide Resistance Action Committee (IRAC) (^{Sparks and Nauen, 2015}). ¶ ^{Whalon et al. (2016}) § Restricted Use (^{COFEPRIS, 2015}).

Results and Discussion

Mortality data of Raoiella indica’s were properly adjusted to the Probit model (c², p> 0.05) (Table 2). Mite mortality in control was zero, except in abamectin (5 % mortality). The estimated concentrations that caused 50 and 90% mortality (LC₅₀ and LC₉₀, respectively), and the 95 % trust interval for LC₉₀ indicated that the most toxic acaricides were fenazaquin and milbemectin, followed by abamectin and dicofol. Acequinocyl, fenpyroximate, propargite, formetanate hydrochloride, sulfur, and bifenthrin were the less toxic (Table 2). According to LC₉₀ values and their trust limits, the fenazaquin and milbemectin had the same toxicity level. Both acaricides were 20 and 27 times more toxic than abamectin and dicofol, respectively (Table 2). These results are similar to those obtained by ^{De Assis et al. (2013}) in Roraima, Brazil, with 10 acaricides, under laboratory conditions, and consequently abamectin and milbemectin were identified as the most toxic for the adult R. indica.

Table 2 Toxicity of 10 commercial acaricides for adult red palm mite Raioella indica in Tabasco, Mexico. 

† Bioassay’s total females. ¶ Degree of freedom. §Chi-square value (p>0.05). φMean standard erros. ¤ Letal concentraction 50 (CL₅₀). †† Lethal concentration 90 (CL₉₀), in i. a. L^-1 mg with their 95 % trust interval. ¶¶ CL₉₀ toxicity rate level.

Due to results of the preliminary bioassays, spirodiclofen, spiromesifen, bifenazate, and amitraz were discarded from the final test because -even in a maximum concentration of 1000 ppm-, they did not produce 100 % mortality of R. indica adults. A probable reason is that spirodiclofen and spiromesifen are more toxic for eggs and immature stages than adults, and the reduction of female fecundity and fertility is slow (^{Marcic, 2012}). According to ^{De Assis et al. (2013}), spiromesifen was the least toxic against adult R. indica out of 10 acaricides evaluated. But ^{Dekeyser (2005}) indicated that spirodiclofen and spiromesifen affect all development stages in a wide range of phytophagous mites. In addition, bifenazate is classified as an inhibitor of mite development and is very active against the mobile stages and eggs of Tetranychus urticae and other species (^{Dekeyser (2005}). Amitraz is considered a low toxicity acaricide against T. urticae (^{Dennehy et al., 1993}). Acaricides that affect immature stages could improve their effect against R. indica under in situ conditions, where all development stages can be found.

The gradient of concentration-mortality regression lines of acaricides against R. indica adults varied from 0.31 to 0.76 (Table 2), similar to the 0.39-1.69 range observed by ^{De Assis et al. (2013}) in bioassays with acaricides and the same species. These values (1.62-2.38) are relatively low compared with those obtained with abamectin in nine T. urticae populations (^{Monteiro et al., 2015}), and with abamectin, bifenazate, dicofol, propargite, and spiromesifen against the same species (1.25-11.24) (^{Latheef and Hoffmann, 2014}). According to ^{Lagunes-Tejeda and Vázquez-Navarro (1994}), the gradient is an adequate estimator of the heterogeneity of the population under study: the lower the gradient, the higher the data heterogeneity. In this regard, ^{Robertson et al. (2007}) indicated that there is evidence that the enzymatic detoxification levels of organisms in heterogeneous populations have higher quantitative differences. The variance in age and nutritional conditions of R. indica adult field specimens probably affected this study’s gradient.

A problem for the chemical control of phytophagous mites is their high potential to develop resistance to acaricides (^{Whalon et al., 2008}). Thus, ^{Sawicki and Denholm (1987}) defined the pesticide resistance management as a set of strategies in which the basic premise is to preserve susceptibility to pesticides through their rational use and to restrict treatments in order to prevent the selection of resistant individuals, and extend the useful life of the products. Although bioassay results cannot be used to determine which dose to apply in the field -because a laboratory determination does not take into consideration dragging, photodecomposition, thermoregulation, and insect escape (^{Lagunes-Tejeda et al., 2009})-, it is indeed possible to compare the evaluated acaricides’ toxicity for the organisms under study (^{De Assis et al., 2013}). According to our results, fenazaquin, abamectin, milbemectin, and dicofol could be included in a chemical handling program for R. indica in Tabasco, Mexico.

Under field conditions, dicofol was considered as an effective acaricide to reduce the R. indica population in coconut palms in Rio Piedras, Puerto Rico; abamectin and milbemectin sprinkling controlled the R. indica presence in coconut palms in Florida, USA (^{Rodrigues and Peña, 2012}). In 2013, abamectin was temporarily authorized by COFEPRIS in the campaign against red mite in Mexico (^{SENASICA, 2013}). We consider that fenazaquin, milbemectin, abamectin, and dicofol could be authorized for the emerging chemical control of R. indica, because these acaricides are used against other phytophagous mite species with economic importance in Mexico (^{COFEPRIS, 2015}). Biological effectiveness of these acaricides should be proven in the field, in order to identify the proper application timing and how minimize the impact on R. indica’s natural antagonists.

Conclusions

Fenazaquin and milbemectin were the most toxic acaricides against R. indica adults, followed by abamectin and dicofol. The least toxic acaricides, in descending order were acequinocyl, fenpyroximate, propargite, formetanate hydrochloride, sulfur, and bifenthrin