556 _____________Mun. Ent. Zool. Vol. 3, No. 2, June 2008__________ SID E-EFFECTS OF TH REE ACARICID ES ON TH E PRED ATORY MITE, PH Y TOSEIU LU S PER SIM ILIS ATH IAS-H EN RIOT ( ACARI: PH YTOSEIID AE) U N D ER LABORATORY CON D ITION S Ah m ad N ad im i*, Karim Kam ali*, Mas o u d Arbabi** an d Fate m e Abd o li*** * Department of Entomology, Tarbiat Modares University, Tehran, Iran. E-mail: ahmad_nadimi@yahoo.com ** Department of Agricultural Research Zoology, Iranian Plant Protection Research Institute. *** Department of Biology, Guilan University, Rasht, Iran. [ N ad im i, A., Kam ali, K., Arbabi, M. & Abd o li, F. 2008. Side-effects of three Acarides on the predatory mite, Phy toseiulus persim ilis Athias-Henriot (Acari: Phytoseiidae) under laboratory conditions. Munis Entomology & Zoology 3 (2): 556-567] ABSTRACT: The predatory mite Phy toseiulus persim ilis Athias-Henriot is an economically important species in integrated mite pest management and biological control of spider mites in many countries throughout the world. For optimal biological mite management, it is important to know if acaricides have adverse undesirable effects on the predatory mites. The toxic effects of hexythiazox (Nisorun®, EC 10%), fenpyroximate (Ortus®, SC 5%) and abamectin (Vertimec®, EC 1.8%) on P. persim ilis were evaluated. The acaricides were applied on detached bean leaves using a Potter Tower spray which deposited 2 mg spray solution per cm2. Percent predator mortality was evaluated from the protonymph up to the adult stage including first five days of the oviposition period. The results showed that the total effect values of all concentrations of hexythiazox were below the lower threshold thus it could be considered a harmless acaricide to this predatory mite. In contrast, the total effect of all concentrations of fenpyroximate, and field, as well as, one half the field concentration of abamectin were found toxic to predatory mite and above upper threshold. KEY WORDS: Phy toseiulus persim ilis, Side effect, Acaricide, Predatory mite IN TROD U CTION The two spotted spider mite, Tetrany cus urticae (Koch), is one of the most important mite pest species with a wide range of host plants and world distribution (Bolland et al., 1998). In Iran it is found on a number of outdoor and indoor agriculture crops (Arbabi et al., 1997). Many efforts have been undertaken to manage T. urticae problems in agricultural crops such as the application of new acaricides with the lower concentrations and release of predacious mites such as Phy toseiulus persim lis in glasshouses on cucumbers (Arbabi, 2007) and in fields of beans, cotton as well as soybeans (Daneshvar & Abaii, 1994). Among glasshouse pests recorded in the world, spider mites are known for their high fecundity, short life span and several generations per season. Under these circumstances spider mites are quickly selected for pesticide resistance pesticides (Helle & Sabelis, 1985). It has gained increasing attention by research scientists in many parts of the world. Selective pesticides that can be used to control pests without adversely affecting important natural enemies are urgently needed. Testing programme _____________Mun. Ent. Zool. Vol. 3, No. 2, June 2008__________ 557 represented by IOBC (International Organization for Biological Control), is not only meant to provide valuable information on the side effects of pesticides on beneficial organisms but it also gives the testing members an opportunity to improve testing techniques, compare results and exchange experience with colleagues in the Working Group (Hassan et al., 1991). Mass rearing and releasing natural enemies mainly phytoseiid mites are one of the goals of biological control of these pests in indoor and outdoor conditions (McMurtry & Croft, 1997). Biological control of these pests is increasing because of the pressure on growers to find alternatives to chemical pesticides (van Lenteren, 2000). In the presence of chemical applications, biological control of spider mites may be achieved by the selective use of pesticides that are less toxic to natural enemies than to pest species (Zhang & Sanderson, 1990). Ruberson et al. (1998) suggested that selective pesticide were the most useful tool of integration of biological control agents into pest control programs. A strain of P. persim ilis was introduced into Iran from the Netherlands (Department of Entomology, Wageningen Agricultural University) in 1988 (Daneshvar, 1989) and it was effective in controlling spider mites under greenhouses and outdoor conditions (Daneshvar & Abaii, 1994). However, Biological control of spider mites using this predaceous mite is effective only against low population densities of the pest (Pralavorio et al., 1985). When the population densities are high an acaricide treatment is needed to reduce the pest population before release of beneficial mites (Malezieux et al., 1992). The effects of pesticides on T. urticae are being widely studied and its resistance to new products is frequently monitored (Castagnoli et al., 2005). Failures of chemical control of T. urticae caused by resistance have been reported in several countries for compounds, such as Hexythiazox (Herron & Rophail, 1993), Fenpyroximate (Sato et al., 2004) and Abamectin (Beers et al., 1998). Although various aspect of pesticide effects on P. persimilis have been studied by many workers in the past (Samsøe-Petersen, 1983; Zhang & Sanderson, 1990; Oomen et al., 1991; Blumel et al., 1993; Hassan et al., 1994; Shipp et al., 2000; Blumel and Gross, 2001; Cloyd et al., 2006). Only Kavousi & Talebi (2003) investigated side-effects of heptenophos, malathion and pirimiphosmethyl on P. persim ilis in Iran. Moreover, there is no information on the susceptibility of this introduced strain to other pesticides, especially acaricides. In this study, we report the effects of abamectin, fenpyroximate and hexythiazox on P. persim ilis used in biological control programs in glasshouses. The three acaricides are currently used for control of spider mites in Iran. The results will be used to develop IPM programs with P. persim ilis in agricultural crops. 558 _____________Mun. Ent. Zool. Vol. 3, No. 2, June 2008__________ MATERIALS AN D METH OD S 1. Origin an d re arin g o f m ite s The T. urticae strain originated from the glasshouse of the Department of Agricultural Zoology, Iran Plant Protection Res. Institute (IPPRI) and was reared on beans (Phaseolus vulgaris L. var. Lordegan) sown in earthen pots in several months. P. persim ilis strain originated from IPPRI that was reared on bean plants for 13 years without exposure to pesticides. The two species were mass reared on bean leaves placed upside down on a layer of water-saturated cotton in a Petri dish and surrounded by wet cotton-wool to prevent the mites from escaping and, at the same time, provide water. Mite cultures were maintained in a controlled climate chamber at 25 ± 2 0Ċ, 65 ± 10% RH with 16:8 h (L:D) photoperiod. 2 . Te s t U n its En viro n m e n t The test unit consisted of a detached bean leaf placed lower side on a layer of water-saturated cotton in a Petri dish (80-mm diameter) with a hole drilled in the center. The Petri dish was placed in another lager Petri dish (90-mm diameter) to provide a continuous water supply to the cotton layer. Thus predatory mites were provided with drinking water and a barrier that impeded their escape. It is very important that all leaves are of the same quality in tests that are to be compared. Young, dark green, primary leaves were chosen that were roughly 5.5 cm wide at the widest part near the base (Samsøe-Petersen, 1983). The bean leaves were excised with their petioles intact and placed upside down onto wet cotton, the petioles were immediately embedded in moist cotton to extend the high quality of leaves and initiate the growth of roots (Bernard et al., 2004). Test units were kept in a controlled climate chambers. 3 . Pre p aratio n o f th e p re d ato r The test was done with the most susceptible life stage, i.e. protonymphs (larvae are too fragile to be used). Protonymphs of uniform age obtained according to the procedure described by Bakker et al. (1992). 4 . Acaricid e s The toxicity of abamectin (Vertimec®, EC 1.8%), fenpyroximate (Ortus®, SC 5%) and hexythiazox (Nisorun®, EC 10%) were evaluated at N, 1/2N and 1/4N where N represents the field rate recommended in Iran. Tap water was used in the controls (Table 1). 5. Sp rayin g The experiment was carried out using the detached leaf method according to Oomen (1988). Single detached leaves were sprayed at day 0 of the experiment on the lower side with a potter spray tower (Burchard Manufacturing, Uxbridge, United kingdom) was calibrated to achieve a _____________Mun. Ent. Zool. Vol. 3, No. 2, June 2008__________ 559 wet deposit of 2 mg cm-2. The dry residue was used to test contact toxicity to juvenile predators. After the spray residue had dried, predator protonymphs of uniform age were placed on the leaf arena using a fine brush and a surplus of spider mites was added as food. 60 predator protonymphs (15 × 4 replicates) were used in each test unit. Finally, a plastic mesh was provided in the center of cover of the Petri dishes. 6 . As s e s s m e n t Mortality and escape of predators up to 5 days after the adult stage and reproduction per female during the first 5 days of the adult stage were assessed. All dead and live mites were counted, and dead mites were removed daily. Mites were considered dead when they failed to move after repeated gentle prodding with a brush. Predator eggs were counted and removed daily from 3 to 7 d after spraying. All assessments were made with a stereomicroscope. 7. An alys is To avoid overestimating mortality, cumulative mortality was calculated by summing dead mites and dividing this number by the total number of live and dead mites at each mortality assessment, excluding unaccounted escapees (Blumel et al., 1993). The escape rate was calculated as a portion of number of mites present at the start of experiment. Mortality rates were corrected for the control mortality with the following formula (Abbott, 1925): M a = ( M t – M c ) / ( 10 0 – M c ) × 10 0 % Ma: Mortality corrected according to Abbott Mt: Mortality in treatment Mc: Mortality in control Possible changes in the number of females present on the test units during the reproduction period were taken into account by the following formula: R ry = ( n E d 3 / n F d 3 ) + [ n E d 4 / ( ( n F d 3 + n F d 4 ) / 2 ) ] + [ n E d 5 / ( ( n F d 4 + n F d 5 ) / 2 ) ] + [ n E d 6 / ( ( n F d 5 + n F d 6 ) / 2 ) ] + [ n E d 7 / ( ( n F d 6 + n F d 7) / 2 ) ] d3 to d7: examples for evaluation days Rry: Reproduction in replicate number y nE dx: number of eggs (in replicate number y) on day x nF dx: number of females (in replicate number y) on day x Mean values of the escape rate, of the mortality rate and of the reproduction per female of the different treatments were analyzed statistically. Data were checked for normal distribution with AndersonDarling test (Minitab 13) and analyzed by univariate variance analysis 560 _____________Mun. Ent. Zool. Vol. 3, No. 2, June 2008__________ (ANOVA, Duncan-test; SPSS 13.0 for windows). Data were transformed before analysis (square root). Effect on reproduction was determined by: Er= R t/ R c Where: Er= Effect on reproduction Rt= Reproduction in treatment Rc= Reproduction in control Subsequently effect on survival and effect on reproduction were combined using the following formula (Overmeer & van Zon, 1982): E= 10 0 % - ( 10 0 % - M a ) × E r Where: Ma= Mortality corrected according to Abbott E= Total effect Based on total effects, rating of toxicity of acaricides was evaluated through the Working Group's joint pesticide testing programme in guideline IOBC (Bakker et al., 1992): Class 1: E<30% Class 2: 30<E<80 Class 3: 80<E<99 Class 4: E>99% (harmless) (slightly harmful) (moderately harmful) (harmful) RESU LTS There was a significant difference in 7 d cumulative mortality effects of all three acaricides at all three concentrations on P. persim ilis (Table 2). Mortality was highest after exposure to fenpyroximate at all concentrations and abamectin at field rate (100% mortality). Application at half and quarter of the field rate of abamectin resulted in 62.27 to 71.23% mortality (Table 2). In contrast, P. persim ilis exposed to dry residues of all three concentrations of Hexythiazox suffered only 5.43 to 18.44% mortality. Acaricides differed significantly in their effects on female fecundity (Table 2). The lowest reproductive performance was caused by fenpyroximate at all three concentrations and abamectin at field rate. Fenpyroximate caused a complete cessation of egg lay. Application at half and quarter the field rate of hexythiazox increased the reproduction performance on P. persim ilis (Table 2). All three acaricides had no repellent attributes (Table 4). The results of total effects (E) of the product applications are listed in Table 3. When the toxic effects of the acaricides are classified according to IOBC classification, all three concentrations of hexythiazox were harmless _____________Mun. Ent. Zool. Vol. 3, No. 2, June 2008__________ 561 (class1, E<30). At one quarter the field rate, abamectin was moderately harmful (class 3, 80<E<99) and half the field rate, abamectin and all three concentrations of fenpyroximate were harmful (class 4, E>99). D ISCU SSION Among the 3 acaricides evaluated, only hexythiazox was harmless to P. persim ilis. Fenpyroximate at the 3 concentrations evaluated and abamectin at the field and one half the field rates were harmful to P. persim ilis. The use of these two compounds in the field would probably result in severe reduction of P. persim ilis. Thus they are incompatible in IPM programs using this species. Our results are consistent with results reported for fenpyroximate and abamectin (Blumel & Hausdorf, 2002). Even at one quarter the field rate, Abamectin was moderately harmful to P. persim ilis. Based on our observations these effects could be caused by a direct effect of these two acaricides on survival and reproduction of the predator mite. Although various phytoseiid species have responded differently to abamectin, a reduction in reproduction is common to all (Zhang & Sanderson, 1990). Kim et al. (2005) showed that application of abamectin was highly toxic to Am bly seius cucum eris (Oudemans) adult females causing 92% mortality at 168 h after treatment and the number of eggs deposited by adult female predators decreased to 5.4 compared to 131.6 in the control. Zhang and Sanderson (1990) believe that one reason of fewer egg produced is reducing mobility and thus consuming fewer prey. Also, they suggested that a lack of prey and quick elimination of spider mite by these acaricides may cause such effects. Application of Hexythiazox at different concentrations was harmless to P. persim ils. Our results are consistent with the results by Oomen et al. (1991), Hassan et al. (1987, 1991), van der Staay (1991) and Blumel & Gross (2001). It would be an appropriate substitute to fenpyroximate and abamectin in integrated pest management (IPM) programs. Our observations showed that exposure to hexythiazox at one half and one quarter the field rates increased fecundity of P. persim ilis. These results are not the first documented case of pesticide increasing fecundity in a phytoseiid mite. Kavousi & Talebi (2003) showed that heptenophos at the recommended concentration increased the fecundity of P. persim ilis. Also, James (1997) reported increased fecundity in Am bly seius victoriensis by imidacloprid. The fecundity-enhancing property of hexythiazox can make P. persim ilis an excellent choice as a biological control agent in greenhouses and other horticulture crops. Van de Vrie et al. (1972) believed that certain pesticides can stimulate mite reproductive physiology; therefore, positive effect of hexythiazox at these two concentrations on reproduction may be physiological. Our results indicated that further studies on the effect of hexythiazox on fecundity and reproduction of P. persim ilis and other phytoseiid species 562 _____________Mun. Ent. Zool. Vol. 3, No. 2, June 2008__________ are clearly warranted. For example, investigation of different concentrations of pesticides (especially lower rates) and comparative effects on the other stages should be assessed. The relative toxicity of pesticides to pests, predators and immature stages (e.g. neonates) of the predators should provide an adequate indication for selectivity of pesticides, which is essential for development of pest management programs (Jeppson et al., 1975). Nevertheless, few populations consist of one life stage in nature and a true estimate of effect will not be gained by testing neonates only. If there is differential susceptibility among life stage, population toxicology is warranted (Stark & Banken, 1999). Furthermore, less susceptible stages can compensate for the loss of young and an accurate estimate of the toxic effect is therefore not obtained when toxicological studies are conducted with neonates only (Stark & Wennergren, 1995; Kareiva et al., 1996; Walthall & Stark, 1997; Stark et al., 1997). Ultimately, Stark & Banken (1999) suggested that to conduct more realistic toxicological studies, it is probably best to test a mixed age population. Blumel et al. (2000) suggested that studies should be focused on the protonymph the most susceptible developmental stage, we suggest that side-effects of hexythiazox and other pesticides should be studied on other life stages. There were no differences in the number of P. persim ilis that escaped in treatments, but percentage was higher in control (25% escapes). The predatory mite, P. persim ilis is a highly motile active predator, so higher escape levels are not surprising. Also, escaping from the treated test surface is a common problem in this method (Kavousi & Talebi, 2003). However, escape is a change in the behavior of the test mites, which as a test parameter should be addressed at higher test tiers (i.e. semi field and field trials) (Blumel et al., 2000). It seems likely that several factors are affected on estimating the escape rate under laboratory conditions: a) lethal effect of acaricides may conceal their repellent effects b) handling of test units including adding food, removing eggs and dead mites and even light produced by stereomicroscope may cause overestimation in escape rates as repellent effects. Thanks to the reasons cited above, as well as the high escape rates observed in the control block, it was not possible to estimate this parameter. CON CLU SION Of the three acaricides evaluated in the laboratory, hexythiazox may be incorporated in IPM programs based on P. persim ilis without any additional studies. 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Acaricides Active ingredient Brand name hexythiazox abamectin fenpyroximate Nisorun, EC 10% Vertimec, EC 1.8% Ortus, SC 5% field rate recommended (N) (ml/l) 2.5 0.2 0.5 Table 2. Effect of three acaricides at different concentrations on the survival and fecundity of P. persim ilis atments Concentrations ontrol ythiazox ythiazox ythiazox amectin amectin amectin yroximate yroximate yroximate N 1/2N 1/4N N 1/2N 1/4N N 1/2N 1/4N % Mortality rates* (Mean±SE) 18.44±2.86a 4.49±3.19a 5.43±2.46a 100±00c 71.23±4.21b 62.27±3.33b 100±00c 100±00c 100±00c Total eggs/female* (Mean±SE) 15.61±0.33b 15.53±0.27b 19.12±0.28a 20.00±0.78a no surviving female 0.13±0.47d 3.01±0.03c no surviving female no surviving female no surviving female *Means in columns followed by different letters are significantly different; Duncan-test; P < 0.05 _____________Mun. Ent. Zool. Vol. 3, No. 2, June 2008__________ 567 Table 3. Total effect and toxicity of three acaricides at different concentrations on P. persim ilis (IOBC evaluation categories). Treatments Concentrations Total effects Toxicity class Control hexythiazox N 23.7 1 hexythiazox hexythiazox abamectin abamectin abamectin fenpyroximate fenpyroximate fenpyroximate 1/2N 1/4N N 1/2N 1/4N N 1/2N 1/4N -15.29 -9.11 100 99.73 92.24 100 100 100 1 1 4 4 3 4 4 4 Table 4. Repellency of P. persim ilis after exposure to fresh residues of acaricides at different concentrations Treatments Concentrations Control hexythiazox hexythiazox hexythiazox abamectin abamectin abamectin fenpyroximate fenpyroximate fenpyroximate - *Means N 1/2N 1/4N N 1/2N 1/4N N 1/2N 1/4N % Escape rates* (Mean±SE) 25.00±94a 21.66±0.83a 10.83±1.56a 20.00±3.33a 15.00±0.83a 23.33±2.88a 21.66±0.83a 15.00±0.83a 16.66±2.88a 16.66±2.15a in columns followed by the same letter are not significantly different; Duncan-test; P > 0.05