Detection of phosphine resistance in major stored-product insects in Greece and evaluation of a field resistance test kit

https://doi.org/10.1016/j.jspr.2019.02.004Get rights and content

Highlights

  • Sampling of populations of stored product beetles from Greece, indicated notable variations in the susceptibility to phosphine.

  • From the species tested, Oryzaephilus surinamensis and Rhyzopertha dominica were more commonly found to be resistant to phosphine.

  • A quick diagnostic test, provided similar results in the evaluation of resistance with the Food and Agriculture Organization test.

Abstract

The use of phosphine has been effective against a wide range of stored-product pests in different types of commodities and facilities. However, its continuous and improper use has led to resistance development in -several major insect species. Although phosphine resistance has been reported from many countries across the globe, reports from Europe have been very limited. In the present study, we determined phosphine resistance in insect populations that had been collected from a range of storages across Greece, using two different diagnostic protocols. Apart from the traditional Food and Agriculture Organization (FAO) protocol, a field test kit (known as the Detia Degesch Tolerance Test Kit, DDTTPK) was utilized, for “same day” determination of the resistance status of field collected insects. In total, 53 populations belonging to Rhyzopertha dominica, Sitophilus oryzae, Sitophilus granarius, Cryptolestes ferrugineus, Tribolium confusum, Tribolium castaneum and Oryzaephilus surinamensis were tested. For the majority of the species and populations tested, both FAO and DDPTTK provided similar results, for the susceptibility to phosphine and thus, the quick test could be used with success for an initial same day screening of phosphine resistance. Among the tested species, the populations recorded with the most frequent survival at the FAO testing dose of phosphine was that of R. dominica. The dissimilar evaluation and characterization of resistance to phosphine between diagnostic protocols is particularly important, as it poses risks in the over or underestimation of the resistance status of a given population. Our data indicate that the DDPTTK could be used to determine resistance to phosphine in the field, before the initiation of fumigations to disinfest stored commodities.

Introduction

Phosphine gas, or hydrogen phosphide (PH3), is the most commonly used fumigant insecticide for the disinfestation of a wide range of durable commodities including grains, dried fruits and tobacco in warehouses and processing facilities globally (Benhalima et al., 2004; Daglish, 2004; Collins et al., 2005; Wang et al., 2006). The phase-out of methyl bromide (UNEP, 1995) has increased the reliance on phosphine significantly, as a fumigant for stored-product protection (Bell, 2000; Chandhry, 2000; Nayak et al., 2010). Phosphine has several advantages that are compatible with wide industrial use, including its relatively ease in application, low price, suitability for a wide range of storage types and commodities and global acceptance as a residue-free treatment (Emery et al., 2003; Nayak and Collins, 2008; Kaur and Nayak, 2015). Moreover, phosphine has been proved effective against most major stored product insect and mite pests (UNEP, 1995; Emery et al., 2003; Opit et al., 2012; Cato et al., 2017).

The dominance of phosphine as a disinfestant over several decades has led to the development of resistance in several pest species, that is posing a continuous threat to the sustainability of this key treatment (Rajendran and Gunasekaran, 2002; Nayak et al., 2003, 2013; Collins et al., 2005; Lorini et al., 2007). The first extensive global surveillance on phosphine resistance was undertaken by Champ and Dyte (1976). Later, Zettler and Cuperus (1990) investigated failure of phosphine fumigations in the US and correlated these to either development of phosphine resistance or inadequate fumigation practices. Many key pest species in Australia have now demonstrated resistance to phosphine, including the lesser grain borer, Rhyzopertha dominica (F.) (Coleoptera: Bostrychidae) (Collins et al., 2005), the psocid Liposcelis bostrychophila Badonnel (Psocoptera: Liposcelididae) (Nayak and Collins, 2008), the rice weevil, Sitophilus oryzae (L.) (Coleoptera: Curculionidae) (Holloway et al., 2016), the red flour beetle, Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae) (Jagadeesan et al., 2012) and the rusty grain beetle, Cryptolestes ferrugineus (Stephens) (Coleoptera: Laemophloeidae) (Nayak et al., 2013). Furthermore, detection of resistant populations of key pest species has also been reported from Brazil (Pimentel et al., 2009, Pimentel and Guedes, 2010; Lorini et al., 2007), China (Song et al., 2011), Morocco (Benhalima et al., 2004), India (Rajendran and Narasimhan, 1994; Kaur et al., 2015), Pakistan (Alam et al., 1999; Ahmad et al., 2013) and USA (Opit et al., 2012; Chen et al., 2015; Saglam et al., 2015; Cato et al., 2017; Afful et al., 2018). Compared to these reports from several continents across the globe, there is very limited information available on the existence of phosphine resistance in Europe. In a recent study, Aulicky et al. (2015) characterized a population of the confused flour beetle, Tribolium confusum Jacquelin Du Val (Coleoptera: Tenebrionidae) from Czech Republic to be far less susceptible than a laboratory population. Prior to this, the only report on any European resistance data was included in the global resistance survey by Champ and Dyte (1976) that showed resistance to phosphine in some major stored product insect species.

The protocols to determine the resistance in key storage pests have evolved significantly from the first recommendations put forward by the FAO Method (Food and Agricultrure Organization, 1975). Basically, the FAO method involves a bioassay that simply discriminates between susceptible and resistant individuals, when adults of a field population are exposed for 20 h exposure to roughly 30–50 ppm (depending on the species) of phosphine, followed by mortality assessments at the end of the exposure period and 14 days post-fumigation. This method has been used recently with slight modification to diagnose resistance in field populations in the USA (Opit et al., 2012; Cato et al., 2017; Afful et al., 2018). With the characterization of two levels of resistance (weak and strong) in the major pest species, researchers in Australia have significantly modified the FAO method and established two discriminating dosages for their regular monitoring (Daglish and Collins, 1999; Nayak et al., 2013; Holloway et al., 2016). More recently, a ‘quick knock down test’ was specifically established to detect strong resistance in C. ferrugineus that involves a 5 h exposure to the very high concentration of 1436 ppm of phosphine (Nayak et al., 2013). In similar line, the company Detia Degesch GmbH (Laudenbach, Germany) has developed the Detia Degesch Phosphine Tolerance Test Kit (DDPTTK), which is based on a rapid knock down bioassay that can diagnose resistance in a pest population in less than 30 min. This protocol has been modified from knock down tests developed by previous researchers (Mills, 1986; Chandhry, 2000; Reichmuth, 1992). In an effort to obtain data for Europe, the aim of the current study was to survey stored product insect populations from several storage and processing facilities in Greece; in order to evaluate and quantify the potential existence of phosphine resistance. While determining the resistance frequency in key stored product pests for the first time in some Greek storages, we have attempted to evaluate the utility of the commercial test kit (DDPTTK) compared with the traditional FAO method.

Section snippets

Insects

A total of 53 stored product insect populations were sampled from a range of storage facilities across different geographic regions in Greece (Fig. 1). These include flour mills, feed mills, pasta factories, silos and farm warehouses. The populations were collected over the period November 2014–June 2017. The distance of these storage sites from our laboratory (Laboratory of Entomology and Agricultural Zoology, Department of Agriculture Crop Production and Rural Environment, University of

DDPTTK

Based on this protocol, all laboratory populations tested were classified as susceptible (Table 2). Among the 53 field populations tested, two populations of O. surinamensis, two of S. oryzae, five of T. confusum and one of T. castaneum were found to be susceptible to phosphine (Table 2). Based on the kit diagnosis, one field population of S. granarius was diagnosed as resistant to phosphine, whereas two populations of O. surinamensis, four of S. oryzae, 22 of T. confusum, four of T. castaneum,

Discussion

To our knowledge, this is the first study in which extensive sampling has been conducted in a European country, in order to estimate resistance to phosphine of several stored product insects. In this study, our field samples covered the whole species spectrum that generally infest the stored products in an attempt to estimate the spread of resistance in these species along the stored commodity value chain across a wide geographic landscape in Greece. Simultaneously, we used two established

Acknowledgements

This research is co-financed by Greece and the European Union (European Social Fund- ESF) through the Operational Programme «Human Resources Development, Education and Lifelong Learning» in the context of the project “Strengthening Human Resources Research Potential via Doctorate Research” (MIS-5000432), implemented by the State Scholarships Foundation (IKY).

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