Phosphine resistance in saw-toothed grain beetle, Oryzaephilus surinamensis in the United States

Highlights

• Phosphine discriminating dose (DD) for eggs of O. surinamensis previously unknown.

• DD of phosphine for O. surinamensis eggs is 28.4 ppm over a 72-hour fumigation.

• Phosphine resistance is present in O. surinamensis in the United States.

• Eggs of O. surinamensis required higher phosphine concentrations than adults.

Abstract

Phosphine (PH₃) fumigation resulting in sub-lethal exposure has led to the development of phosphine resistance in many stored-product insect species worldwide and is a major challenge to the continued effective use of phosphine. In 2016 phosphine resistance was found in Tribolium castaneum (Herbst) and Plodia interpunctella (Hübner) collected from California dried fruit and nut processing facilities. Although Oryzaephilus surinamensis (L.) infests grain, dried fruit, and nuts in storage and processing facilities, phosphine resistance in this species has not been studied in the United States. In this study, the discriminating dose of phosphine for O. surinamensis eggs was estimated using a laboratory susceptible strain; it was found to be 28.4 ppm over a 72-h fumigation period (1 mg/L of phosphine = 714.18 ppm or 1 ppm = 0.0014 mg/L). Discriminating dose bioassays were used to determine phosphine resistance in both eggs and adults of 14 different populations collected from California and Oklahoma. Resistance to phosphine was detected in four out of 14 populations in adults and nine out of 14 populations in eggs and ranged from 2 to 100%. Phosphine percent survival values in both adults and eggs of three populations, namely, Box BR, Box BF, and OKWat were >90%. Lethal concentration values required to kill 99% of individuals in samples for adults of these three populations were predicted as 320.5, 290.7, and 263 ppm, respectively, and those for eggs were 1030.7, 1055.9, and 564.5 ppm, respectively, over a 72-h fumigation period. This study confirms that phosphine resistance is present in O. surinamensis in the United States.

Introduction

Phosphine is the most widely used fumigant on grain, dried fruits and nuts, and other durable commodities and value-added products to control stored-product insect pests worldwide (Collins et al., 2001; Johnson et al., 2009; Hagstrum et al., 2012). Phosphine is a popular choice as it is relatively inexpensive, easy to apply, and leaves minimal residues on treated commodities (Hagstrum et al., 2012). However, the rapid development of phosphine resistance by stored-product insect pests is a major challenge for the continued and effective use of phosphine (Collins et al., 2001; Opit et al., 2012). Heavy reliance on phosphine coupled with leaky storage facilities, the practice of overdosing to compensate for leakage, and higher frequency of application resulting from fumigation failures lead to sublethal exposures and high selection pressure for phosphine-resistant genes that consequently facilitates phosphine resistance (Benhalima et al., 2004; Emery et al., 2011; Opit et al., 2012). Following the initial report on phosphine resistance by Champ and Dyte (1976), many stored-product insects around the world have been reported to have developed resistance to phosphine (Rajendran, 1999; Collins et al., 2001; Benhalima et al., 2004; Pimental et al., 2009, 2010; Lorini et al., 2007; Opit et al., 2012; Ahamd et al., 2013; Nayak et al., 2013; Jittanun and Chongrattanameteekul, 2014; Chen et al., 2015; Koçak et al., 2015; Sağlam et al., 2015; Gautam et al., 2016; Cato et al., 2017; Konemann et al., 2017; Afful et al., 2018). In the United States, phosphine resistance has been reported in Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae), Rhyzopertha dominica (F.) (Coleoptera: Bostrichidae), Cadra cautella (Hübner) (Lepidoptera: Pyralidae), Tribolium confusum Jacuelin du Val (Coleoptera: Tenebrionidae), Lasioderma serricorne (F.) (Coleoptera: Anobiidae), Plodia interpunctella (Hübner) (Lepidoptera: Pyralidae), and Cryptolestes ferrugineus (Stephens) (Coleoptera: Laemophloidae) (Zettler et al., 1989; Zettler and Cuperus, 1990; Zettler, 1991; Zettler and Keever, 1994; Opit et al., 2012; Sağlam et al., 2015; Gautam et al., 2016; Konemann et al., 2017; Afful et al., 2018). FAO global survey conducted in 1975 indicated phosphine resistance may be present in Saw toothed grain beetle (STGB), Oryzaephilus surinamensis (L.) (Coleoptera: Silvaniidae) (Champ and Dyte, 1976). There are no published studies on phosphine resistance in O. surinamensis in the United States, but it has been reported in Australia, Brazil, and Bangladesh (Emery et al., 2003; Pimentel et al., 2008; Mills, 1983).

Phosphine percent survival values and resistance levels in insects have been shown to substantially increase over time if not detected and resistance management implemented (Emery et al., 2011; Opit et al., 2012). Besides, resistant insects may spread to newer facilities and new geographic areas spreading resistance. Between 1990 and 2012, phosphine resistant populations of T. castaneum in Oklahoma reportedly increased from 13 to 89% and that of R. dominica from 67 to 100% (Zettler and Cuperus, 1990; Opit et al., 2012). Recent studies have reported resistance in a new species, C. ferrugineus in Oklahoma and (Konemann et al., 2017) and newer geographic regions (Alabama, California, Florida, and Kansas) for R. dominica (Afful et al., 2018). The levels of resistance of the most resistant populations of R. dominica, T. castaneum, and C. ferrugineus from Oklahoma were, 1519 × , 119 × , and 134 × , respectively, more resistant than their susceptible counterparts (Opit et al., 2012; Konemann et al., 2017). California populations of T. castaneum were found to be 49 × more resistant than their susceptible counterparts (Gautam et al., 2016). Despite these reports, phosphine remains a useful pest control tool for the US grain industry and California dried fruit and nut industries (Opit et al., 2012; Gautam et al., 2016; Konemann et al., 2017). It is noteworthy that insect contaminated food samples received from California almond storage and processing facilities used in the Gautam et al. (2016) study were repetitively contaminated with O. surinamensis.

There are currently no detailed published studies on phosphine resistance in O. surinamensis collected in the United States. FAO survey reported low percent survival values, 1 and 4%, respectively, in populations, collected from Fresno California and Ft. Meade Maryland (Champ and Dyte, 1976). It is well documented that phosphine resistance in different species may develop independently and that the levels of resistance in different populations and different species may vary (Collins et al., 2003; Opit et al., 2012; Konemann et al., 2017). Moreover, previous phosphine resistance studies have used adults or larvae (moths) probably because these two life stages are isolated easily and screening tests for phosphine resistance could be done rapidly (Bell et al., 1977). However, adults are the most susceptible life stage and resistance monitoring and management strategies focusing on adults may not effectively control eggs (Gautam et al., 2016), which are usually the most fumigant tolerant life stage (Bell, 1976). In fact, eggs of a phosphine resistant T. castaneum populations collected from California required 1.8–5.3-fold higher concentration of phosphine than adults (Gautam et al., 2016).

Oryzaephilus surinamensis is an important pest of dried fruit and nuts and cereal grains (Johnson et al., 2009; Hagstrum et al., 2012). This study was initiated to provide information on phosphine resistance in O. surinamensis eggs and adults collected from California almond storage and processing facilities and from wheat storage facilities in Oklahoma. There is currently no published discriminating dose for eggs of O. surinamensis. Therefore, the first objective was to estimate the discriminating dose for eggs of a laboratory-susceptible strain of O. surinamensis. We then estimated percent survival values of both adults and eggs in 11 different populations collected from California and 3 populations collected from Oklahoma. A third objective was to determine levels of resistance found in each of the two life stages, in cases where percent survival values were ≥40%. Differences in percent survival values, lethal concentrations required to kill different life stages of the same population, and possible implications for the phosphine resistance management strategies to control O. surinamensis are discussed.