Combining entomopathogenic fungi and parasitoids to control the green peach aphid Myzus persicae

Highlights

• Mummification rate was not affected when the fungus was applied 3 days after parasitization.

• About 82% of the parasitoid larvae that developed in fungus-treated aphids were free of fungal infection.

• Fecundity and longevity of A. colemani females emerged from untreated and fungus-treated aphids were similar.

• The presence of A. colemani increased the number of fungus-killed aphids.

• Fungus and parasitoids interact positively in controlling aphids under semi-field conditions.

Abstract

The green peach aphid, Myzus persicae, is a major insect pest worldwide. The parasitoid Aphidius colemani and more recently, the entomopathogenic fungus Lecanicillium muscarium strain KV01 (Mycotal®), have been considered as potential biological control against M. persicae. However, no studies have been carried out on the interaction between L. muscarium and A. colemani against M. persicae. This study, therefore, was conducted to determine the most effective timing of application of this fungal strain in combination with either naturally occurring or introduced parasitoids to control Myzus persicae in the laboratory and controlled field environments. In the laboratory, mummification, emergence of parasitoid adults from mummified aphids and female sex ratio of the emerging adults, were not affected when the fungus was applied 6 or 7 days after the parasitoids were added, compared with treatment with A. colemani only. Although a 40% reduction in the female sex ratio of emerging parasitoid adults was recorded when fungi applied 3 days after the parasitoids were added, fungal application had no significant effect on longevity and fecundity of the female A. colemani F1 generation that emerged from fungus-treated aphids. In the semi-field experiment, the mean number of aphids per leaf was significantly lower in the treatment involving A. colemani in combination with L. muscarium than those with A. colemani alone. However, aphid reduction in the treatments involving naturally occurring parasitoids alone and those in combination with L. muscarium was not significantly different. This study suggests that it is possible to combine L. muscarium with A. colemani to increase the level of aphid control. A more detailed knowledge of the effects of naturally occurring parasitoids on pest control and their interaction with other biological control agents will help to develop environmentally sound crop management strategies with reduced insecticide applications.

Introduction

Intraguild interactions are common among communities of biological control agents including interactions between parasitoids and entomopathogenic fungi (Mesquita and Lacey, 2001, Rashki et al., 2009). Ferguson and Stiling (1996) documented three possible outcomes of intraguild interactions in the context of biological control: (1) the natural enemies interact beneficially and their combined effects result in a higher level of control than the sum of their individual effects (a synergistic effect); (2) the natural enemies do not interact and their total effect is equivalent to the sum of their individual effects (an additive effect); or (3) the natural enemies may interact negatively, resulting in control either equivalent to or less than the control produced by one agent alone (an inhibitory effect).

Aphidius colemani (Hymenoptera: Braconidae) is a solitary koinobiont endoparasitoid of aphids and is one of the most successful commercial biological control agents used in greenhouse crops (Messing and Rabasse, 1995). It is mainly used to control the economically important aphids Myzus persicae and Aphis gossypii (Van Steenis and El-Khawass, 1995). In addition, naturally occurring parasitoid wasps (Hymenoptera: mainly Braconidae) are known to contribute to regulation of aphid populations in agroecosystems (Sigsgaard, 2002). Several species of aphidiine parasitoids such as Diaeretiella rapae, Aphidius ervi, A. colemani and Praon volucre have been reported parasitizing M. persicae in the field worldwide (Dixon, 2012). Another biological control agent, Lecanicillium muscarium (Hypocreales: Cordycipitaceae) is a well-known entomopathogenic fungus and possesses a wide insect host range that includes Bemisia tabaci (Cuthbertson and Walters, 2005), Trialeurodes vaporariorum (Pineda et al., 2007), and phytopathogenic fungi (Spencer, 1980). The strain KV01, commercially available as Mycotal® (Koppert Biological Systems, the Netherlands), has been reported as a promising biological control agent for use against M. persicae (Mohammed and Hatcher, 2016).

As M. persicae is a polyphagous insect with a high reproductive capacity, and short generation time, it can be difficult to achieve a high level of control using only a single biological control agent (Martins et al., 2014). In the recent years, there has been increasing interest in exploring the possibility of achieving greater control of M. persicae by using combinations of natural enemies such as parasitoids and entomopathogenic fungi (Rashki et al., 2009, Emami et al., 2013, Martins et al., 2014). However, the combined effects of A. colemani and L. muscarium (Mycotal®) on M. persicae populations under greenhouse or field conditions have been not investigated. Some laboratory studies have, however, shown that A. colemani and L. muscarium could be used as a part of integrated pest management (IPM) programmes against the cotton aphid, Aphis gossypii (Aiuchi et al., 2012) and cereal aphids (Aqueel and Leather, 2013). L. muscarium causes highest mortality in older aphids (Mohammed and Hatcher, 2016), while A. colemani causes highest mortality in young stages of M. persicae (Perdikis et al., 2004), thus we would hypothesize that the combined application of the parasitoids and entomopathogenic fungi would cause an additive mortality in the aphids

The introduction of parasitoids to control aphids on field crops is particularly problematic, not only do large numbers of parasitoids have to be introduced (Coll and Hopper, 2001), but there is no means of preventing them moving away from the crop. Therefore, it is not surprising that there has been a low success rate of this biocontrol method in the past (Van Driesche et al., 2008, Nagasaka et al., 2010). Although M. persicae is often attacked by a large number of naturally occurring parasitoids, their efficacy in controlling M. persicae is not sufficiently understood (Sunderland et al., 1997). Most of the studies investigated the abundance, seasonal occurrence and distribution of aphidiine parasitoids of M. persicae through modification of the environment or existing practices. This known as conservation biological control (Barbosa, 1998), which is appropriate in organic agriculture because there is minimal use of disruptive broad-spectrum pesticides and other biological control agents that otherwise may constrain the action of natural enemies (Barry et al., 2005). Some field studies have, however, shown that the efficacy of several naturally occurring aphid parasitoids in reducing aphid populations was low (≤5%) (Feng et al., 1991, Wraight et al., 1993, Tóth et al., 2009). Therefore, increasing the efficacy of naturally occurring parasitoids by combining them with other biological control agents such entomopathogenic fungi could provide a cost-effective, safe and sustainable method for aphid control, which could be the central component of an integrated aphid control program. This is the first study on using a combination of naturally occurring parasitoids and L. muscarium in biological control programs of M. persicae.

Entomopathogenic fungi, especially Hypocreales fungi with a generalist nature, can infect non-target insects, including parasitoids, which can result in direct deleterious effects in the parasitoids (Brooks, 1993). As the intra-host development time for Hypocreales fungi is generally shorter than that of parasitoids, if a entomopathogenic fungus infects a host insect before a parasitoid, then the fungus will usually exclude the parasitoids because the competition is skewed in favor of the fungus (Furlong and Pell, 2005). Thus, one important way avoid inhibition between these biological control agents is to apply the entomopathogenic fungus when the parasitoid is less susceptible to it (van Lenteren and Fransen, 1994). For example, Kim et al. (2005) found that the percentages of mummification and A. colemani emergence were not affected when Verticillium lecanii was applied 5 days after parasitization. Aqueel and Leather (2013) showed that the percentage of aphids mummified was not significantly affected when aphids exposed to V. lecanii 3 days after parasitization.

The objectives of the current study were, therefore, to determine the optimal time of fungal application that will reduce competition between L. muscarium and A. colemani and thus enhance their additive interactions against M. persicae, and to evaluate the effects of L. muscarium on the percentage of aphids mummified, emergence rate, sex ratio, and fecundity and longevity of F1-generation parasitoids under laboratory conditions. A choice experiment evaluated mummification rates when A. colemani was offered both fungus-treated and untreated aphids. We also investigated the effect of the separate and combined efficacy of L. muscarium and either added A. colemani or natural parasitoid populations on a population of M. persicae in a controlled field experiment. This is the first study on the combined use of these biological control agents for the control of M. persicae under field conditions.