Predation and avoidance behavior of the pea aphid Acyrthosiphon pisum confronted with native and invasive lady beetles in Europe

Abstract

Invasive species are a major driver of global biodiversity loss. However, we often lack a mechanistic understanding why some non-native species become invasive. Missing coevolutionary history between invasive predators and native prey can lead to a lack of predator avoidance by native prey and consequently higher consumption rates by invasive predators. We compared predation rates of four native European lady beetle species and the invasive lady beetle species Harmonia axyridis Pallas (Coleoptera: Coccinellidae), using the native pea aphid Acyrthosiphon pisum Harris (Hemiptera: Aphididae) for prey. Here, we also quantified initial dropping of A. pisum from host plants. In an additional plant-choice experiment, we tested for aphid avoidance of plants bearing lady beetle cues. Differences in predation were determined by predator body size. Initial dropping of aphids did not differ between the invasive lady beetle species H. axyridis and the remaining native lady beetle species. However, A. pisum showed no avoidance behavior towards H. axyridis cues, but to cues of the most voracious native species. Thus, relatively large body size and missing chemical cue avoidance by aphids can benefit the invasive H. axyridis.

Comparison of native and non‐native predator consumption rates and prey avoidance behavior in North America and Europe

“…Pea aphids in Europe and North America avoided chemical cues of native lady beetles. These findings are in line with previous studies on predator–prey interactions showing that chemical cues of predators induce avoidance behavior in herbivores (Ninkovic et al., 2013; Seo et al., 2018; Ünlü et al., 2020). Chemical cues of predators can persist in the environment and indicate potential predation risk of a nearby predator (Kats & Dill, 1998).…”

“…Coccinella septempunctata and H. axyridis consumption rates did not differ significantly in North America (GH; p = .97) and in Europe (GH; p = .94; Figure 4). (Ninkovic et al, 2013;Seo et al, 2018;Ünlü et al, 2020). Chemical cues of predators can persist in the environment and indicate potential predation risk of a nearby predator (Kats & Dill, 1998).…”

“…In Europe, H. axyridis was introduced in 1995 and the establishment period started in (Brown et al, 2011. Coccinella septempunctata and the Asian H. axyridis are relatively large and highly voracious compared to common native aphidophagous species (Elliott et al, 1996;Hoki et al, 2014;Ünlü et al, 2020).…”

“…The species‐specific chemical cues left in the tracks of lady beetles consist of cuticular hydrocarbons (Kosaki & Yamaoka, 1996) that serve for water proofing (Menzel et al., 2019) and mediate intra‐ and interspecific communication (Doumbia et al., 1998; Hemptinne et al., 1998; Menzel et al., 2019; Ninkovic et al., 2013). Recent studies revealed that the presence of lady beetle chemical cues on host plants can induce avoidance behavior in herbivores; for example, the Asian citrus psyllid Diaphorina citri (Hemiptera: Psyllidae) (Seo et al., 2018), the bird cherry‐oat aphid Rhopalosiphum padi (Ninkovic et al., 2013), as well as the pea aphid Acyrthosiphon pisum (both Hemiptera: Aphididae) (Ünlü et al., 2020).…”

“…In Europe, H. axyridis was introduced in 1995 and the establishment period started in 2000–2001 (Brown et al., 2011). Coccinella septempunctata and the Asian H. axyridis are relatively large and highly voracious compared to common native aphidophagous species (Elliott et al., 1996; Hoki et al., 2014; Ünlü et al., 2020). Moreover, both species interfere with native trophic interactions associated with a lady beetle species decline in the non‐native range, due to resource competition and intraguild predation (Alyokhin & Sewell, 2004; Ware et al., 2009), absence of natural enemies (Roy et al., 2011), high abundance (Horn, 1991; Koch, 2003) and high fecundity (Kajita & Evans, 2010) and are therefore classified as invasive species (Roy & Brown, 2015).…”