Possible coexistence of Harmonia axyridis Pallas (Coleoptera: Coccinellidae) and Diaeretiella rapae M'Intosh (Hymenoptera: Braconidae) in the biological control of Lipaphis erysimi (Homoptera: Aphididae)

Highlights

• H. axyridis could discriminate against mummified aphids.

• H. axyridis preferred adult prey when aphids became mummies.

• D. rapae tended to parasitize younger nymphal aphids when H. axyridis was introduced.

• H. axyridis and D. rapae avoid competition by attacking different stages of aphids.

• H. axyridis and D. rapae can potentially coexist in the control of L. erysimi.

Abstract

To study the interactions between the aphidophagous predator Harmonia axyridis Pallas (Coleoptera: Coccinellidae) and the specialist aphid parasitoid Diaeretiella rapae M'Intosh (Hymenoptera: Braconidae) in the biological control of mustard aphid, Lipaphis erysimi (Homoptera: Aphididae), the prey discrimination by H. axyridis among unparasitized, non-mummified parasitized and mummified aphids was examined under laboratory conditions. Prey/host selections were also tested by offering L. erysimi at various developmental stages to assess the possibility of coexistence between the two species, so the prey preference of H. axyridis when D. rapae parasitize aphids, and the host preference of D. rapae when H. axyridis interfered with the parasitization were detected. We found that H. axyridis could discriminate against mummies rather than non-mummified parasitized aphids. The ladybug showed a significantly positive preference for adult prey when D. rapae turned aphids into mummies, while D. rapae tended to parasitize younger nymphal aphids when H. axyridis was introduced. The present study suggests the prey discrimination against mummies by H. axyridis, and indicates that H. axyridis and D. rapae can avoid resource competition by attacking different and non-overlapping developmental stages of aphid. Thus, H. axyridis and D. rapae can potentially coexist and establish a stable ecosystem in the biological control of L. erysimi.

Introduction

Various natural enemies existing in a biological control system are common (Snyder and Ives, 2003), and the interactions among the agents are important to evaluate the effectiveness of pest suppression (Denoth et al., 2002). Aphid populations are frequently controlled by both generalist predators and specialist aphid parasitoids (Bilu and Coll, 2007; Costamagna et al., 2007), so the competitive interactions between the predators and parasitoids are inescapable (Gontijo et al., 2015). Some views are presented that predators may damage predator-parasitoid-aphid systems by consuming parasitized prey containing parasitoid (Chacón and Heimpel, 2010; Arim and Marquet, 2004; Rosenheim et al., 1993; Holt and Polis, 1997), resulting in significant losses of parasitoids (Colfer and Rosenheim, 2001; Taylor et al., 1998; Brodeur and Rosenheim, 2000). However, others suggest parasitoids can coexist with predators in the biological control of aphids (Okuyama, 2009; Frago and Godfray, 2014). When both predator and parasitoid are introduced in an ecosystem, their interactions should be defined (neutral, positive or negative). Potential interactions in identical food webs may affect the practical results of intentional or accidental multi-species introduction, so the purpose of studying interactions between predator and parasitoid is to synergistically facilitate aphid suppression and maintain ecosystem stability.

The mustard aphid, Lipaphis erysimi (Homoptera: Aphididae) is one of the most harmful cruciferous crop pests, and is widespread across the world (Prasad and Phadke, 1988; Liu et al., 1997). The infestation rate in the field reaches occasionally up to 90% (Bakhetia, 1983; Malik and Anand, 1984; Rohilla et al., 1987). Since chemical pesticides would cause harm to both human and environment (Garratt and Kennedy, 2006; Youn et al., 2003), the release of biological control agents gains attention gradually (Leskey et al., 2012; Lee et al., 2013). Diaeretiella rapae M'Intosh (Hymenoptera: Braconidae) has a significant effect on controlling mustard aphid (Ohiman and Kunar, 1986; Desneux et al., 2005), and Harmonia axyridis Pallas (Coleoptera: Coccinellidae) is also widely used in the biological control of L. erysimi (Adachi-Hagimori et al., 2011). Both D. rapae and H. axyridis are regarded as biological control agents of mustard aphid, but H. axyridis always consume the parasitoid within aphids accidentally in predator-parasitoid-aphid systems (Pell et al., 2008). Therefore, the interactions between H. axyridis and D. rapae should be studied to properly use them in the biological control of L. erysimi.

Studies on the interactions between H. axyridis and D. rapae in stable ecosystems are meaningful from a IPM perspective as predator-parasitoid-aphid interactions may either disrupt existing ecological balance or create a more stable community. In this study, we addressed 3 main questions: 1) Whether H. axyridis can discriminate among unparasitized, non-mummified parasitized and mummified aphids. 2) Which developmental stages of aphids were preferred by H. axyridis when D. rapae turned them into mummies. 3) Which developmental stages of aphids were preferred by D. rapae when H. axyridis interfered with parasitization.