Insecticide selectivity to the parasitic mite Acarophenax lacunatus (Cross & Krantz) (Prostigmata: Acarophenacidae) on Rhyzopertha dominica (Fabr.) (Coleoptera: Bostrichidae)

Seletividade de inseticidas para o ácaro parasita Acarophenax lacunatus (Cross & Krantz) (Prostigmata: Acarophenacidae) em Rhyzopertha dominica (Fabr.) (Coleoptera: Bostrichidae)

CROP PROTECTION

Insecticide selectivity to the parasitic mite Acarophenax lacunatus (Cross & Krantz) (Prostigmata: Acarophenacidae) on Rhyzopertha dominica (Fabr.) (Coleoptera: Bostrichidae)

Seletividade de inseticidas para o ácaro parasita Acarophenax lacunatus (Cross & Krantz) (Prostigmata: Acarophenacidae) em Rhyzopertha dominica (Fabr.) (Coleoptera: Bostrichidae)

José R. Gonçalves^I; Lêda R.D'A. Faroni^II; Raul N.C. Guedes^I; Carlos R.F. de Oliveira^I

^IDepto. Biologia Animal

^IIDepto. Engenharia Agrícola. Universidade Federal de Viçosa, 36571-000, Viçosa, MG e-mail: [e-mail]

ABSTRACT

The presence of natural enemies in stored grains and the need of pest control alternatives led to the assessment of the effect of insecticides on the mite species Acarophenax lacunatus (Cross & Krantz), an egg parasite of the stored grain pest Rhyzopertha dominica (Fabr.). The insecticides bifenthrin, deltamethrin, pirimiphos-methyl and fenitrothion were tested at 0.4, 0.5, 0.8 and 10 ppm, respectively. Insecticide treated wheat grains were spread in petri dishes and infested with 25 adults of R. dominica. Seven days later, three mites were added to each dish, in four replicates. The number of adults of R. dominica, grain weight loss and instantaneous rate of increase (r_i) of A. lacunatus were lower when the grain was treated with deltamethrin. Bifenthrin, fenitrothion, and pirimiphos-methyl were less effective in controlling the pest, but they were selective in favor of the mite, showed higher number of physogastric females and r_i of A. lacunatus. Therefore, deltamethrin was less selective in favor of the mite species. Nonetheless the parasitic mite was able to parasitize eggs of R. dominica on wheat treated with all the insecticides evaluated.

Key words: Stored grain pest, mite, pyrethroid, organophosphate, biological control

RESUMO

Diante da presença de inimigos naturais em massas de grãos armazenados e a necessidade de se buscar alternativas de controle de pragas, avaliou-se o efeito de inseticidas sobre o ácaro Acarophenax lacunatus (Cross & Krantz), um parasita de ovos de Rhyzopertha dominica (Fabr.). Os inseticidas bifentrina, deltametrina, pirimifós metílico e fenitrotiom foram testados a 0,4; 0,5; 0,8 e 10 ppm. As unidades experimentais consistiram de placas de Petri contendo grãos de trigo, infestados com 25 adultos de R. dominica. Sete dias após a infestação, foram inoculados três ácaros em cada placa, sendo utilizadas quatro repetições por tratamento. O número de adultos de R. dominica, a perda de matéria seca dos grãos e a taxa instantânea de crescimento (r_i) de A. lacunatus foram menores no tratamento com deltametrina. Os inseticidas bifentrina, fenitrotiom e pirimifós metílico apresentaram baixa eficácia na redução de R. dominica, mas foram seletivos em favor do ácaro, mostrando maior número de fêmeas fisogástricas e r_i para A. lacunatus. Com isso, conclui-se que deltametrina é o inseticida menos seletivo em favor de A. lacunatus. Entretanto, esse ácaro é capaz de parasitar ovos de R. dominica sob grãos tratados com todos os inseticidas avaliados.

Palavras - chave: Praga de grãos armazenados, ácaro, piretróide, organofosforado, controle biológico

Insecticide use is considered the only control option when a pest population in stored grains reaches the economic threshold (White & Leesch 1996). However, due to the development of resistance in many pests to the majority of the insecticides (organophosphates and pyrethroids) commonly used for their control (Collins et al. 1993, Guedes et al. 1996, Lorini & Galley 1999), insecticide use is becoming increasingly unviable (Arthur 1996). Because few insecticides are registered for controlling stored grain pests and the registration of new products requires a long time and at a high cost (White & Leesch 1996), alternative methods such as integration of natural enemies and insecticides need to be developed (King & Nordlund 1992).

The majority of mites infesting stored grains are pests, but some of them are natural enemies of stored grain-pests (Cross & Krantz 1964). Interest in the efficacy and applicability of mites for integrated pest management systems has been increasing. Mites are small, have a short life cycle, and high reproductive potential (Scholler et al. 1997, Faroni et al. 2001). Integrating the use of predatory/parasitic mites and insecticides for stored-grain pest management requires knowledge of the impact of the insecticides on the natural enemies or, in other words, their selectivity to natural enemies (Baker & Arbogast 1995, Gonçalves et al. 2002).

The egg parasite Acarophenax lacunatus (Cross & Krantz) is studied aiming its use as biocontrol agent of stored-grain pests. The whitish-colored small (0.14 mm x 0.09 mm) adults have a phoretic behavior (uses the pests to spread in the grain mass). This mite develops over a wide temperature range, from 18°C to 41°C, with an optimum at about 30°C. The female adults are responsible for egg parasitism. They suck the egg contents and distend to a bright, spherical form. The body size increases by about five times, which characterizes progeny development (physogastry). The mite progeny emerge as adults ready to parasitize new host eggs. The mite A. lacunatus significantly reduces the population of Rhyzopertha dominica (Fabr.) (Faroni et al. 2000), which is an important pest of stored products (Rees 1996). The following study was carried out to assess the insecticide selectivity to A. lacunatus and to determine the possibility of integrating the use of this mite species with some insecticides commonly used for stored-grain pest control.

Material and Methods

Mass Rearing of R. dominica. R. dominica was reared on non-treated whole wheat grain in petri dishes in an environmental chamber at 30 ± 1°C, 65 ± 5% relative humidity (RH) and 24h scotophase. The insects originated from a laboratory colony maintained at the same conditions for four consecutive years without insecticide exposure. Each petri dish containing the whole wheat was infested with 50 adults of R. dominica and seven days later the eggs were collected by sieving through an 1-mm aperture sieve. The collected eggs were placed on the fresh diet in petri dishes. This period was sufficient for the pest to lay its eggs. Eggs of a known age were periodically collected in a similar way (Faroni et al. 2000).

Mass Rearing of A. lacunatus. Individuals of A. lacunatus were obtained from cultures of R. dominica infested with this parasite for more than four years. The mites were reared on the R. dominica at 30 ± 1°C, 65 ± 5% RH, but in a different room from uninfested insects (Faroni et al. 2000).

Insecticide Application. The insecticides used were bifenthrin (Prostore 25 CE), deltamethrin (K-Obiol 25 CE), pirimiphos-methyl (Actellic 500 CE) and fenitrothion (Sumigran 500 CE) applied at the concentrations of 0.4, 0.5, 8.0 and 10.0 ppm, respectively (doses within the range recommended by the manufacturers and commonly used in wheat stores). The experimental procedure followed the general guidelines standardized by the International Organization for Biological Control/West Paleartic Regional Section (IOBC/WPRS) for laboratory tests on the susceptible stages of arthropods (Hassan et al. 1994). Thus, the insecticides were tested at recommended rates using one-day old mites. The insecticide was dissolved in distilled water and, using a manual atomizer with the spray-nozzle turned downwards, 1 ml of solution was sprayed from a height of 20 cm on 1 kg of wheat grains within a wind protected container similar to a spray tower. To avoid cross-contamination among the insecticides, separate atomizers were used for each treatment. The control was sprayed with the same amount of distilled water. The atomizer was calibrated in a preliminary test, on 10 kg of wheat spread over a 1 m² surface area, receiving 1 ml of the solution for each kg of the grain.

Each experimental unit encompassed a 140 mm x 10 mm petri dish (diameter x height) containing 25 g of treated or non-treated wheat grain. Grains in each petri dish were infested with 25 non-sexed, three- to seven-day old adults of R. dominica (Faroni et al. 2000). Seven days after infestation with the pest, which allowed a suitable period for oviposition, three non-physogastric females of A. lacunatus were added to each experimental unit, with four replicates. The dishes and their contents were wrapped in a PVC plastic film to avoid insect or mite escape and to prevent possible contamination with individuals of other species. Four holes were made with entomological pins for air exchange in the PVC film covering the petri dishes.

The petri dishes were stored for 23 days in environmental chambers at 30 ± 1°C, 65 ± 5% relative humidity (RH) and 24h scotophase. A second generation of the pest did not complete development during this test period. The wheat weight loss (%) was determined through the changes in the weight at the beginning and at the end of the experiment. The grain mass from each dish was sieved through a 1 mm aperture sieve to separate the grains from the insects and the powder containing the eggs of R. dominica and the mites. The number of live and dead adults of R. dominica, parasitized eggs and mites in the physogastric process were determined in each experimental unit using a stereomicroscope.

The instantaneous rates of increase of A. lacunatus (r_i) were calculated using the equation: r_i = [Ln(N_f/N_o)]/Dt; where N_f = final number of live mites; N_o = initial number of live mites; Dt = time variation (duration of the experiment in days) (Walthall & Stark 1997). All data were subjected to analysis of variance and the means were compared using Duncan's multiple range test at 5% probability level whenever appropriate.

Results

The number of physogastric females of A. lacunatus was significantly different among insecticides with higher numbers for bifenthrin and fenitrothion (df_error = 15; F = 4.84; P = 0.01). Similar trend was observed for instantaneous rate of increase of A. lacunatus (r_i) (df_error = 15; F = 49.91; P < 0.001), with lower population growth of A. lacunatus when deltamethrin was used (Table 1).

There were also significant differences in parasitism of R. dominica eggs with the different insecticides (df_error = 15; F = 5.61; P = 0.006). Pirimiphos-methyl drastically compromised egg parasitism, which was significantly different from the others insecticides that allowed parasitism levels over 89% (Table 1).

There was no significant interaction between insecticides and A. lacunatus in reducing the number of adults of R. dominica (df_error = 30; F = 0.77; P > 0.05) and the effect of the parasitic mite alone was also non-significant for this parameter (df_error = 30; F = 0.14; P > 0.05). Only insecticides affected significantly the number of adults of R. dominica (df_error = 30; F = 90.25; P < 0.001).

The same trend was observed for wheat weight loss (%), where the insecticide-mite interaction (df_error = 30; F = 1.33; P = 0.28) and the mite effect (df_error = 30; F = 0.003; P > 0.05) were not significant. Deltamethrin showed the greatest reduction of adults of R. dominica and consequently the lowest wheat weight loss (Table 2).

The number of eggs of R. dominica was affected not only by the insecticide applied (df_error = 30; F = 5.46; P = 0.002), but also by the mite presence (df_error = 30; F = 4.45; P = 0.04). Nonetheless, the interaction between insecticides and mite presence was not significant (df_error = 30; F = 0.71; P > 0.05). The lowest numbers of R. dominica eggs were observed with deltamethrin use and the mite presence also significantly reduced the number of eggs of R. dominica (Table 3).

Discussion

The insecticides affected the number of physogastric females of A. lacunatus, with the greatest impact occurring with deltamethrin, followed by fenitrothion and pirimiphos-methyl. The number of A. lacunatus females was higher in grains treated with bifenthrin and fenitrothion indicating the selectivity of these insecticides in favor of the mite A. lacunatus. Similar results were reported for predatory mites with other insecticides and acaricides used in the management of stored product pests (Zdarkova & Horak 1984) and in the field (Croft et al. 1982). Zdarkova & Horak (1984) observed that none of the eight acaricides evaluated by them caused 100% mortality of the predatory mite Cheyletus eruditus (Schrank).

The instantaneous rates of increase of A. lacunatus (r_i) was low in the presence of deltamethrin, which may be either because of the non-selectivity of this insecticide or because of low numbers of host eggs that resulted from the reduced population of R. dominica. Similar results were found for the predators Androlaelaps casalis (Berl.), Blattisocius keegani Fox and C. eruditus, whose numbers were significantly reduced by chlorpyriphos-methyl at 6 ppm on stored oats (White & Sinha 1990).

Many of the insecticides used for pest control can be detrimental to populations of natural enemies (Baker et al. 1995). However, some insecticides that have low negative impact on the biocontrol agent can be successfully used to control stored-grain pests (White & Leesch 1996). A similar strategy can be applied if insecticide resistant lines of these biocontrol agents are available (Baker & Arbogast 1995, Baker et al. 1995), thus allowing an integrated pest management approach for stored grains (Zdarkova 1994).

The high levels of parasitism observed with the insecticides bifenthrin, deltamethrin and fenitrothion suggest the possibility of integrating A. lacunatus with these insecticides for controlling R. dominica. This integration of these two methods of insect-pest control in a storage environment is important, especially in cases where the pests have already acquired resistance to most insecticides used in this ecosystem (Arthur et al. 1988, Collins 1990, Collins et al. 1993).

The number of R. dominica adults and eggs and wheat weight loss caused by insect-pest infestation was lowest in deltamethrin-treated grains. The efficacy of bifenthrin, fenitrothion and pirimiphos-methyl against R. dominica was lower, which suggests its tolerance (or more likely, resistance) to these products. Several authors have reported stored-products insect resistance to organophosphates such as malathion, pirimiphos-methyl and chlorpyriphos-methyl (Zettler & Cuperus 1990, Guedes et al. 1996) and also to pyrethroids such as bioresmethrin, fenvalerate (Collins et al. 1993) and deltamethrin (Collins et al. 1993, Lorini & Galley 1999). Other pests of stored products such as Acanthoscelides obtectus (Say), Cadra cautella (Walker), Oryzaephilus surinamensis (L.), Plodia interpunctella (Hubner), Sitophilus oryzae (L), Sitophilus zeamais Motschulsky and Tribolium castaneum (Herbst) also have developed resistance to organophosphates and pyrethroids (Arthur et al. 1988, Collins 1990, Collins et al. 1993).

To increase the feasibility of combining biological and chemical control agents, the selected or existing populations of natural enemies effective against stored-grain pests should have their tolerance to stored-grain protectants determined (Baker et al. 1995). Combining the two control methods is important because the indiscriminate use of insecticides can lead to serious problems, including pest resistance, which is even more likely in this case because there are few registered products for stored-product protection and the cost of registering a new insecticide is very high (Woodhead et al. 1990, Hagstrum & Flinn 1996).

The parasitic mite A. lacunatus is an important biological control agent because besides having showed tolerance to the insecticides and high rates of parasitism on R. dominica eggs, its presence inhibits oviposition by this insect-pest. Deltamethrin was the most effective insecticide for reducing R. dominica populations resulting in reduced grain loss and for maintaining the mite population at low but effective levels (90.6 ± 9.38% egg parasitism). Although the efficacy of bifenthrin, fenitrothion and pirimiphos-methyl was low in reducing R. dominica adult populations, it resulted in greater availability of the host eggs and allowed faster mite population growth. The mite population growth is not likely to compromise grain quality because these arthropods are easily removed from the grain mass in their regular cleaning process before processing (Scholler & Flinn 2000). Flinn & Hagstrum (2001) showed that augmentative releases of the Theocolax elegans wasp in wheat decreased in 89% the damage caused by R. dominica besides reducing in 92% the insect fragments in the final product (flour).

These results provide support for the possible use of a biological control agent for stored grain pest management even with insecticide use. However, additional studies are still necessary, extending the investigation to other common pests in the stored-grain ecosystem and determining the effect of these insecticides on the biology of A. lacunatus in association with these pests.

Literature Cited

Received 15/07/03.

Accepted 10/10/03.

• Arthur, F.H. 1996. Grain protectants: current status and prospects for the future. J. Stored Prod. Res. 32: 293-302.
• Arthur, F.H., J.L. Zetter & W.R. Halliday. 1988. Insecticide resistance among populations of almond moth and Indian meal moth (Lepidoptera: Pyralidae) in stored peanuts. J. Econ. Entomol. 81: 1283-1287.
• Baker, J.E., D.K. Weaver, J.E. Throne & J.L. Zetter. 1995. Resistance to protectant insecticides in two field strains of the stored-product insect parasitoid Bracon hebetor (Hymenoptera: Braconidae). J. Econ. Entomol. 88: 512-519.
• Baker, J.E. & R.T. Arbogast. 1995. Malathion resistance in field strains of the warehouse pirate bug (Heteroptera: Anthocoridae) and a prey species Tribolium castaneum (Coleoptera: Tenebrionidae). J. Econ. Entomol. 88: 241-245.
• Collins, P.J. 1990. New resistance to pyrethroids in Tribolium castaneum (Herbst). Pestic. Sci. 28: 101-115.
• Collins, P.J., T.M. Lambkin, B.W. Bridgeman & C. Pulvirenti. 1993. Resistance to grain-protectant insecticides in coleopterous pests of stored cereals in Queensland, Australia. J. Econ. Entomol. 86: 239-245.
• Croft, B.A., S.W. Wagner & J.G. Scott. 1982. Multiple and cross resistance to insecticides in pyrethroid resistant strains of the predatory mite, Amblyseius fallacis Environ. Entomol. 11: 161-164.
• Cross, E.A. & G.W. Krantz. 1964. Two new species of the genus Acarophenax Newstead and Durvall 1918 (Acarina: Pyemotidae). Acarology 6: 287-295.
• Faroni, L.R.D'A., R.N.C. Guedes & A.L. Matioli. 2000. Potential of Acarophenax lacunatus (Prostigmata: Acarophenacidae) as a biological control agent of Rhyzopertha dominica (Coleoptera: Bostrichidae). J. Stored Prod. Res. 36: 55-63.
• Faroni, L.R.D'A., R.N.C. Guedes & A.L. Matioli. 2001. Effect of temperature on development and population increase of Acarophenax lacunatus (Cross & Krantz) (Prostigmata: Acarophenacidae) on Rhyzopertha dominica (F.) (Coleoptera: Bostrichidae). Biocontrol Sci. Technol. 11: 7-14.
• Flinn, P.W. & D.W. Hagstrum. 2001. Augmentative releases of parasitoid wasps in stored wheat reduces insect fragments in flour. J. Stored Prod. Res. 37: 179-186.
• Gonçalves, J.R., L.R.D'A. Faroni & R.N.C. Guedes. 2002. Pyrethroid-Acarophenax lacunatus interaction in suppressing the beetle Rhyzopertha dominica on stored wheat. Exp. Appl. Acarol. 26: 231-242.
• Guedes, R.N.C., B.A. Dover & S. Kambhampati. 1996. Resistance to chlorpyriphos-methyl, pirimiphos-methyl, and malathion in Brazilian and U.S. populations of Rhyzopertha dominica (Coleoptera: Bostrichidae). J. Econ. Entomol. 89: 27-32.
• Hagstrum, D.W. & P.W. Flinn. 1996. Integrated pest management, p. 399-408. In B. Subramanyam & D.W. Hagstrum (eds.), Integrated management of insects in stored products. Marcel Dekker, New York, USA, 426p.
• Hassan, S.A., F. Bigler, H. Bogenschutz, E. Boller, J. Brun, J.N.M. Calis, J. Coremans-Pelseneer, C. Duso, A. Grove, U. Heimbach, N. Helyer, H. Hokkanen, G.B. Lewis, F. Mansour, L. Moreth, L. Polgar, L. Samsoe-Petersen, B. Sauphanor, A. Staubli, G. Sterk, A. Vainio, M. Van de Veire, G. Viggiani & H. Vogt. 1994. Results of the sixth joint pesticide testing programme of the IOBC/WPRS- Working Group ŤPesticides and Beneficial Organismsť. Entomophaga 39: 107-119.
• King, E.G. & D.A. Nordlund. 1992. Propagation and augmentative releases of predators and parasitoids to control of arthropod pests. Pesq. Agropec. Bras. 27: 239-254.
• Lorini, I. & D.J. Galley. 1999. Deltamethrin resistance in Rhyzopertha dominica (F.) (Coleoptera: Bostrichidae), a pest of stored grain in Brazil. J. Stored Prod. Res. 35: 37-45.
• Rees, D.P. 1996. Coleoptera, p. 1-40. In B. Subramanyam & D.W. Hagstrum (eds.), Integrated management of insects in stored products. Marcel Dekker, New York, USA, 426p.
• Scholler, M. & P.W. Flinn. 2000. Parasites and Predators, p. 229-271. In B. Subramanyam & D.W. Hagstrum (eds.), Alternatives to pesticides in stored product IPM. Kluwer Academic Publishers, Boston, 437p.
• Scholler, M., S. Prozell, A.G. Al-Kirshi & C. Reichmuth. 1997. Towards biological control as a major component of integrated pest management in stored product protection. J. Stored Prod. Res. 33: 81-97.
• Walthall, W.K. & J.D. Stark. 1997. Comparison of two population level ecotoxicological endpoints: The intrinsic (r_m) and instantaneous (r_i) rates of increase. Environ. Toxicol. Chem. 16: 1068-1073.
• White, N.D.G. & J.G. Leesch. 1996. Chemical control, p. 287-330. In B. Subramanyam & D.W. Hagstrum (eds.), Integrated management of insects in stored products. Marcel Dekker, New York, USA, 426p.
• White, N.D.G. & R.N. Sinha. 1990. Effect of chlorpyriphos-methyl on oat ecosystems in farm granaries. J. Econ. Entomol. 83: 1128-1134.
• Woodhead, S.D., A.L. O'Leary, D.J. O'Leary & S.C. Rabatin. 1990. Discovery, development and registration of a biological agent from an industrial perspective. Can. J. Plant Pathol. 12: 328-331.
• Zdarkova, E. 1994. The effectiveness of organophosphate acaricides on stored product mites interacting in biological control. Exp. Appl. Acarol. 18: 747-51.
• Zdarkova, E. & E. Horak. 1984. Resistance of predator Cheyletus eruditus (Schrank) to organophosphates and its use for biological control, p. 311-312. In Proceedings of 9^th Czechoslovakian Plant Protection Conference, Brno.
• Zettler, J.L. & G.W. Cuperus. 1990. Pesticide resistence in Tribolium castaneum (Coleoptera: Tenebrionidae) and Rhyzopertha dominica (F.) (Coleoptera: Bostrichidae) in wheat. J. Econ. Entomol. 83: 677-1681.

Publication Dates

• Publication in this collection
  14 July 2004
• Date of issue
  Apr 2004

History

• Received
  15 July 2003
• Accepted
  10 Oct 2003