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. 2020 Oct 27;10(23):13334–13344. doi: 10.1002/ece3.6932

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

Ayse Gül Ünlü 1,✉, John J Obrycki 2, Roman Bucher 1
PMCID: PMC7713951  PMID: 33304541

Abstract

Novel predator–prey interactions can contribute to the invasion success of non‐native predators. For example, native prey can fail to recognize and avoid non‐native predators due to a lack of co‐evolutionary history and cue dissimilarity with native predators. This might result in a competitive advantage for non‐native predators. Numerous lady beetle species were globally redistributed as biological control agents against aphids, resulting in novel predator–prey interactions. Here, we investigated the strength of avoidance behavior of the pea aphid (Acyrthosiphon pisum) toward chemical cues of native lady beetles and non‐native Asian Harmonia axyridis and European Coccinella septempunctata and Hippodamia variegata in North America, hypothesizing that cues of non‐native lady beetles induce weaker avoidance behavior than cues of co‐evolved native lady beetles. Additionally, we compared aphid consumption of lady beetles, examining potential predation advantages of non‐native lady beetles. Finally, we compared cue avoidance behavior between North American and European pea aphid populations and aphid consumption of native and non‐native lady beetles in North America and Europe. In North America, pea aphids avoided chemical cues of all ladybeetle species tested, regardless of their origin. In contrast to pea aphids in North America, European pea aphids did not avoid cues of the non‐native H. axyridis. The non‐native H. axyridis and C. septempunctata were among the largest and most voracious lady beetle species tested, on both continents. Consequently, in North America non‐native lady beetle species might have a competitive advantage on shared food resources due to their relatively large body size, compared to several native American lady beetle species. In Europe, however, non‐native H. axyridis might benefit from missing aphid cue avoidance as well as a large body size. The co‐evolutionary time gap between the European and North American invasion of H. axyridis likely explains the intercontinental differences in cue avoidance behavior and might indicate evolution in aphids toward non‐native predators.

Keywords: coccinellidae, co‐evolution, cue avoidance, invasive species, predator–prey interactions

Here, we compared the role of cue avoidance behavior of pea aphids and lady beetle body size for the invasion success of lady beetles in North America and Europe. In contrast to North American pea aphids, European pea aphids did not avoid cues of the non‐native Harmonia axyridis; in addition, consumption rates were strongly correlated with body size of lady beetles. Thus, we suggest that predation advantages of non‐native predators due to missing antipredator behaviors of prey might diminish with time, whereas body size‐related competition advantages over smaller native and non‐native predators could sustainably benefit large, non‐native predators.

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1. INTRODUCTION

Predator–prey interactions shape ecosystems via density‐ and trait‐mediated effects (Murdoch et al., 2003; Preisser et al., 2005). Density‐mediated effects result in the elimination of prey individuals by a predator leading to reduced prey population densities (Murdoch et al., 2003). Prey adapt to the selection pressure of predators by evolving traits that increase the survival during predator attacks (i.e., antipredator behaviors). However, changes in these plastic traits can come at a fitness cost (i.e., non‐consumptive effects; Lima & Dill, 1990; Peacor & Werner, 2000). Fitness costs of trait‐mediated effects can reduce prey population densities to a similar extent as density mediated effects (Preisser et al., 2005). Both, density‐ and trait‐mediated effects can expand into adjacent trophic levels (i.e., trophic cascades or trait‐mediated indirect interactions; Ohgushi et al., 2012; Terborgh & Estes, 2010).

Predator‐induced changes in prey behavior (i.e., antipredator behavior) can enhance prey survival upon predator attacks, interfering with the detection, encounter, and/or capture of prey (Lima, 1998). Prey species have sensory mechanisms to detect and recognize cues of co‐evolved predators, to effectively respond to a predator attack (Lima & Dill, 1990; Rosier & Langkilde, 2011). Predator cues serve as sensory information for prey, to recognize co‐evolved predators and induce antipredator behaviors. Cues that are involved in interspecific communication can be visual, vibrational cues, and olfactory cues (Fischer et al., 2001; Hermann & Thaler, 2014). Chemical cues left by predators persist for some time in nature and can be an indicator of predator presence and predation risk (Bucher et al., 2014). Missing co‐evolution of predator and prey can lead to a lack of detection and recognition mechanisms of predator cues by prey (Cox & Lima, 2006). Non‐native predators can therefore benefit from a novelty advantage due to lacking or inappropriate antipredator response by prey, leading to higher predation pressure (Sih et al., 2010). Non‐native predators can consequently have stronger consumptive effects and weaker non‐consumptive effects on prey populations, compared to co‐evolved predators. If cues of non‐native and native predator species are similar then a similar response can be expected by prey, regardless of predator origin (Sih et al., 2010). Cue similarities between predator species can therefore lower the impact on prey densities compared to dissimilar non‐native predators (Sih et al., 2010). In addition, cues of closely genetically‐related species tend to be more similar compared to cues of distantly genetically related species, for example, chemical cues within lady beetle genera are more similar than between genera (Magro et al., 2010).

Lady beetles leave species‐specific chemical cues on the plant tissue, which are persistent and long‐lasting (Dixon and Dixon, 2000). 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).

The pea aphid Acyrthosiphon pisum Harris (Hemiptera: Aphididae) consists of numerous distinct biotypes, being adopted to host plants in its local range (Peccoud et al., 2009a; Peccoud, et al., 2009b). Originally of Palearctic origin, North American populations of pea aphids co‐evolved in agricultural fields with native predators for over a century (Thomas, 1878).

Lady beetles (Coleoptera: Coccinellidae) have a history of being globally introduced as biological control agents for decades (Harmon et al., 2007). Lady beetles are predators of several pest species (e.g., aphids and coccids), thus providing a valuable ecosystem service in agriculture (Caltagirone & Doutt, 1989; Obrycki & Kring, 1998). Among the introduced lady beetle species, the European species Coccinella septempunctata and Hippodamia variegata have been released for biological control of aphids in North America (Angalet et al., 1979; Ellis et al., 1999). The earliest establishment of C. septempunctata in North America dates back to 1973 (Angalet & Jacques, 1975). The establishment history of H. variegata began in 1984 in North America (Gordon, 1987). Similarly, the Asian Harmonia axyridis was introduced as a biological control agent in North America and Europe (Tedders & Schaefer, 1994; Trouve et al., 1997). The introduction of the Asian H. axyridis in North America started in 1916 (Gordon, 1985), but its earliest establishment was in 1988 (Chapin & Brou, 1991).

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). The contribution of cue avoidance behavior of aphids confronted with non‐native and native chemical lady beetle cues to the invasion success of non‐native lady beetles remains to be examined.

In this study, we deployed a multi‐species approach to compare differences in cue avoidance behavior of a North American population of pea aphid (Acyrthosiphon pisum) confronted with chemical cues of the Asian lady beetle species Harmonia axyridis, the European lady beetle species Coccinella septempunctata and Hippodamia variegata and three North American lady beetle species, Coleomegilla maculata, Coccinella novemnotata and Hippodamia convergens. Our species set consisted of two native and non‐native species of the same genus Coccinella and Hippodamia, referred to as congeneric, expecting similarities between chemical cues (Magro et al., 2010). In addition, we compared aphid consumption rates between all lady beetles tested. We hypothesized (a) missing avoidance behavior of A. pisum confronted with cues of the non‐native H. axyridis, intermediate avoidance behavior confronted with cues of congeneric non‐native species (Coccinella septempunctata and Hippodamia variegata), due to potential cue similarities and strongest avoidance behavior toward native lady beetle cues. (b) We expected higher aphid consumption of the larger non‐native lady beetle species H. axyridis and C. septempunctata compared to smaller lady beetle species, regardless of origin. In addition, cue avoidance and consumption experiments were conducted in Europe, using a European pea aphid population as prey and non‐native H. axyridis, native Coccinella septempunctata and Hippodamia variegata as predators. We subsequently compared cue avoidance behavior and consumption of North American and European pea aphids confronted with lady beetle species occurring on both continents. We expected (c) missing avoidance behavior toward H. axyridis cues in North America and Europe. Moreover, we expected the avoidance behavior of European pea aphids toward cues of C. septempunctata and H. variegata to be stronger in the native European range compared to avoidance behavior of North American aphids. (d) We expected no differences in aphid consumption of H. axyridis, C. septempunctata, and H. variegata between North America and Europe, due to body size‐related food demands.

2. MATERIAL AND METHODS

2.1. Study species North America

The North American pea aphid Acyrthosiphon pisum (Harris) (Hemiptera: Aphididae) colony consisted of individuals maintained in a colony, which started in 1985 at Iowa State University, Ames, Iowa, USA and individuals collected in Lexington, Kentucky in 2003. The colony was maintained in the laboratory (at Iowa State University and the University of Kentucky) on broad bean plants (Vicia faba, variety Windsor). They were kept in cages with six to eight pots containing five plants each. Plants were replaced weekly to guarantee a fresh food supply for aphids. Aphids were maintained in the laboratory in climate chambers (22°C ± 1 and a photoperiod of light 16 hr: dark 8 hr) and in a climatized laboratory (22°C ± 1 and a photoperiod of light 16 hr: dark 8 hr). The lady beetle species Coccinella septempunctata and Colleomegilla maculata were collected in April 2018 in alfalfa fields and in field margins at an agricultural research field station of the University of Kentucky in Lexington, Kentucky, USA. The overwintering generation of Hippodamia convergens was obtained from Rincon Vitova Insectaries, Ventura, CA, USA, in April 2018 and stored at low temperatures (5°C). Female and male beetles of these species were subsequently paired in 0.24‐liter paper cartons, provided with water and fed ad libitum with pea aphids, and frozen Ephestia kuehniella (Zeller) (Lepidoptera: Pyralidae) eggs (Beneficial Insectary, Redding, CA, USA). Egg clusters laid by individual females were collected and placed into a Petri dish. When larvae hatched, they were separated into glass vials, sealed with cotton, provided with water and fed ad libitum with pea aphids and frozen E. kuehniella eggs until pupation. Individuals of Harmonia axyridis were field collected in the pupal stage in May‐June and kept in Petri dishes (circumference: 9.4 cm × height: 1.6 cm) until the adult beetles emerged. Hippodamia variegata individuals were collected from an alfalfa field in Le Roy, IL, USA in May/June. In June, C. novemnotata was purchased in the larval stage (Lost Ladybug Project, Cornell University, Ithaca, New York 14,850), since no individuals were found in Kentucky and separately kept in glass vials (see above) until they developed to adults. The adult lady beetles were subsequently sorted by species and stored in plastic boxes. They were provided with water and fed ad libitum with pea aphids, A. pisum and frozen E. kuehniella eggs and kept at 22 ± 1°C, at a photoperiod of light 16 hr: dark 8 hr. Voucher specimens were preserved in Ethanol (70%) and stored under −7 ± 1°C at the Department of Entomology (Animal Pathology Building), at the University of Kentucky.

2.2. Study species Europe

The European pea aphid colony was obtained from the Julius‐Kühn Institut in Braunschweig, Germany, which had been maintained in the laboratory since at least 2007. The aphids were reared on broad bean V. faba (v. Sutton Dwarf, Kings Seeds, Manchester) in plastic containers (10.0 × 13.5 × 6.5 cm) covered with gaze for aeration in climate chambers (20 ± 1°C, L:D 16:8 and 65% relative humidity). Aphids were supplied with fresh plants, weekly. The lady beetle species H. axyridis and C. septempunctata were collected in June‐September 2017 and H. variegata in 2018 in grasslands around Marburg, Germany. Ladybeetles were kept in small groups, separated by species, in Petri dishes (circumference: 9.4 cm × height: 1.6 cm), fed ad libitum with A. pisum and were kept at (20 ± 1°C, L:D 16:8 and 65% relative humidity). The data for the European predation and cue avoidance experiments used for the intercontinental comparison are a subset of the European comparison published by Bertleff et al. (2020).

2.3. Cue avoidance experiments

Beetles were sexed prior to the experiments, to ensure a gender‐balanced design (ten male and ten female beetles). Lady beetles were sexed by the morphological differences on the terminal sternites of females and males (Costopoulos et al., 2014; Harmon et al., 2008; Hurst et al., 1999; Nichols & Neel, 1974; Riddick & Schaefer, 2005; Stellwag & Losey, 2014). Double leaflets of Vicia faba were cut in two halves, one control and one treatment leaflet, and separately placed into round Petri dishes (circumference: 3.5 cm × height: 1.0 cm). A single lady beetle adult was placed on the treatment leaflet in the Petri dish for cue deposition (e.g., footprints, feces) and subsequently removed after 12 hr. The control leaflet remained without a lady beetle. The control and the treatment leaflet were randomly assigned and placed into the center of each half of a round Petri dish (circumference: 9.4 cm × height: 1.6 cm); the treatment leaflet was placed into one half of the Petri dish, while the control leaflet was placed into the opposite half. Ten adult aphids were released into the center of each Petri dish, which were capped to prevent aphids from leaving the experimental arena. The duration of the preparation of the experimental set‐up (between removal of the lady beetle from the treatment leaf and the release of aphids) was 60 min. The number of aphids on the control and treatment leaflet was counted after 0.25, 0.5, 1.0, 1.5, 2.0, and 3.0 hr. Twenty replicates were conducted per species in the laboratory under 25.10 ± 0.20°C and artificial lightning. The leaf choice experiments in Europe were identical except that lady beetle individuals were not sexed prior to the experiments, but randomly chosen.

2.4. Predation experiments

Lady beetles were sexed by morphological differences prior to the experiments, accounting for potential intraspecific predation differences of female and male beetles. A single lady beetle adult was subsequently placed into a small round Petri dish (circumference: 3.5 cm × height: 1.0 cm) and starved for 24 hr prior to the experiment. Thirty pea aphids (second to third nymph stage) were counted and placed with a brush into a round Petri dish (circumference: 9.4 cm × height: 1.6 cm). A single lady beetle was randomly assigned to a Petri dish containing aphids, which was capped. Aphid predation was quantified by counting the remaining aphids in the Petri dish after 6 hr. In North America, we freeze‐killed (−7 ± 1°C) lady beetle individuals after the experiments and measured body width (widest horizontal distance of closed elytra) and body length (elytral apex to pronotal apex) of all beetles used for the predation experiments under a stereomicroscope. We followed the procedure of Obrycki et al. (1998) to obtain elliptical body area for individual beetles (body area (mm2) = (π × 0.5 × body length (mm) × 0.5 × body width (mm)). Overall, 20 replicates (ten females, ten males) were conducted per species, in the laboratory under 25.41 ± 0.19°C and artificial lightning. The predation experiments in Europe were identical, except that lady beetle individuals were randomly chosen and not sexed prior to the experiments.

2.5. Statistical analysis

For the cue avoidance experiments in North America and the intercontinental comparison, aphid counts on each leaflet were analyzed as proportions (aphids on control leaf versus treatment leaf). We only considered aphids that made a distinct choice of control or the treatment leaflet. We applied a GLMM with a binomial error distribution to analyze differences between cue donator species identity (i.e., different lady beetle species) on aphid leaf choice. We included cue donator species identity as fixed effects and experimental unit (Petri dish identity) and an observation level random effect (OLRE) as random effects (to account for repeated measurements and overdispersion). We obtained statistical parameters for the fixed effects via ANOVA (χ2‐test) from the R‐package car (Fox & Weisberg, 2019). Pairwise differences between cue donator species identity were analyzed with a Tukey's contrast test for comparison of means with a Holm correction, to account for familywise error rates, using the glht‐function from the multcomp R‐package (Hothorn et al., 2008). We subsequently tested for equal distribution of aphids on control versus. treatment leaf (i.e., if aphids avoid lady beetle cues of the respective cue donator), by applying a GLMM with binomial error distribution. Our fixed effects included species identity and experimental unit (i.e., repeated measurements) and ORLE (accounting for overdispersion) as random effects.

Differences of predation rates in North America after 6 hr and body area were respectively analyzed with a Games–Howell post hoc test, following a Welch's ANOVA (F test) accounting for heteroscedasticity. To test the effects of lady beetle species identity, gender and body area on predation rates, we conducted a GLM with lady beetle species identity, gender and body area as fixed effects with a quasi‐poisson error distribution. Statistical parameters for the fixed effects were obtained via ANOVA (χ2‐test). The intercontinental predation differences between lady beetle species were analyzed with a Games–Howell post hoc test, following a Welch's ANOVA (F test). All statistical analyses were performed with the statistical software R, Version 3.4.0 (R Development Core Team, 2017).

3. RESULTS

3.1. Cue avoidance in North America

Aphid leaf choice did not differ between cues of the different lady beetle species (GLMM; χ 2 = 5.80, df = 5, p = .33). Aphids avoided leaves previously occupied by all species (Figure 1; H. axyridis: z 95 = 4.03, p < .01; C. septempunctata: z 95 = 4.89, p < .01; C. novemnotata: z 95 = 3.13, p < .01; Col. maculata: z 95 = 4.63, p < .01; H. convergens: z 95 = 2.72, p < .01 and H. variegata: z 95 = 2.35, p = .02).

Figure 1.

Figure 1

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Proportion of pea aphids on cue‐free control leaflets (mean ± SE) in North America. Pea aphids avoided leaflets with chemical cues of the native lady beetle species (unfilled symbols) Coccinella novemnotata (C9), Coleomegilla maculata (C. mac), Hippodamia convergens (Hipc) and the non‐native lady beetle species (filled symbols) Harmonia axyridis (Hax), Coccinella septempunctata (C7) and Hippodamia variegata (Hipv) (p ≤ .02, respectively)

3.2. Aphid consumption by lady beetles in North America

The number of aphids consumed after 6 hr differed among lady beetle species (Welch's ANOVA; F = 26.13, df = 5, p < .01). Aphid consumption by C. septempunctata and H. axyridis did not significantly differ (Games–Howell post hoc test (GH); p = .97; Figure 2). There were no differences in aphid consumption between C. novemnotata and H. axyridis (GH, p = .48); Aphid consumption of C. novemnotata was lower compared to C. septempunctata (GH, p = .03). Aphid consumption of C. septempunctata and H. axyridis was respectively higher compared to H. convergens, Col. maculata, and H. variegata (GH; p ≤ .02).

Figure 2.

Figure 2

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Number of pea aphids consumed after 6 hr (mean ± SE) and body area (mm2; mean ± SE) of native (unfilled symbols) and non‐native lady beetle species (filled symbols): Different uppercase letters indicate statistical differences of aphid consumption and different lowercase letters indicate statistical differences in body area between species based on a Games–Howell post hoc test (p < .05, same letters do not differ significantly). Dotted regression line (y = 0.8133x − 0.4305; R 2 = 0.54) shows the linear relationship between aphid consumption and body area

Body area differed between lady beetle species (Welch's ANOVA; F = 248.34, df = 5, p < .01). There were no body area differences between C. septempunctata and H. axyridis (p = .11; Figure 2) The remaining species (C. novemnotata, H. convergens, Col. maculata, and H. variegata) were respectively smaller than C. septempunctata and H. axyridis (GH; p < .01).

Hippodamia convergens, Col. maculata, and H. variegata were smaller than C. novemnotata, (GH; p < .01). There were no size differences between H. convergens and Col. maculata (GH; p = 1.00). Hippodamia variegata was smaller than Col. maculata and H. convergens (GH; p < .01). Consumption rates of lady beetles can be explained by species identity (GLM; χ 2 = 23.18, df = 5, p < .01), beetle gender (GLM; χ 2 = 26.32, df = 5, p < .01), and beetle body size (GLM; χ 2 = 6.23, df = 5, p = .01).

3.3. Intercontinental comparison of aphid cue avoidance

Avoidance behavior of local pea aphids differed between cues of different lady beetle species (GLMM; χ 2 = 30.56, df = 5, p = .01). Avoidance behavior of European aphids was weaker when confronted with H. axyridis cues compared to avoidance behavior of North American aphids, C. septempunctata cues from both continents, and North American H. variegata cues (Tukey's contrasts test (TCT); p < .01, respectively; Figure 3). Avoidance behavior was marginaly higher when confronted with European H. variegata cues compared to European H. axyridis cues (TCT; p = .08). No differences of avoidance behavior were observed between the remaining species (TCT; p > .29, respectively).

Figure 3.

Figure 3

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Proportion of aphids on cue‐free control leaflets (mean ± SE) in North America (unfilled symbols) and Europe (filled symbols). Asterisk indicates significant avoidance behavior of leaflets with chemical cues of lady beetle species (p < .05). Different letters indicate statistical differences between species based on Tukey's contrast test (p < .05)

In Europe, A. pisum showed no avoidance confronted with cues of H. axyridis (z 95 = −1.12, p = .26; Figure 3), but avoidance of C. septempunctata cues (z 95 = 5.31, p < .01) and H. variegata cues (z 95 = 2.59, p < .01). In North America A. pisum showed avoidance to H. axyridis cues (z95 = 4.429, p < .01), C. septempunctata cues (z 95 = 3.85, p < .01), and H. variegata cues (z 95 = 2.44, p < .01).

3.4. Intercontinental comparison of lady beetle consumption rates

Predation rates differed among lady beetle species (Welch's ANOVA; F = 42.38, df = 5, p < .01). North American H. variegata consumed significantly fewer aphids than North American and European C. septempunctata (GH; p < .01, respectively) and North American and European H. axyridis (GH; p < .01, respectively). Moreover, European H. variegata showed lower consumption rates compared to North American and European C. septempunctata (GH; p < .01, respectively) and North American and European H. axyridis (GH; p < .01, respectively). European and North American aphids were consumed to a similar extent by H. axyridis from North America or Europe (GH; p = .52). Moreover, consumption rates did not differ between European C. septempunctata and North American C. septempunctata (GH; p = 1.00) as well as between European H. variegata and North American H. variegata (GH; p = .10). 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).

Figure 4.

Figure 4

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Number of pea aphids consumed after 6 hr (mean ± SE) of lady beetle species in North America (unfilled symbols) and Europe (filled symbols): Different letters indicate statistical differences of aphid consumption of different lady beetle species based on a Games–Howell post hoc test (p < .05, same letters do not differ significantly)

4. DISCUSSION

North American pea aphids avoided chemical cues of all lady beetle species tested, regardless of lady beetle origin. In contrast to North American pea aphids, European pea aphids did not avoid cues of the non‐native H. axyridis. Consumption rates were strongly correlated with body size of lady beetles. On both continents, C. septempunctata and H. axyridis were the largest species tested and consumed the most aphids.

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). By avoiding sides with chemical cues of predators, prey can increase its survival (Lima & Dill, 1990). According to the “landscape of fear,” prey shifts to sites with low predation pressure by avoiding sites with high predation risk (Laundré et al., 2001). A previous study on the avoidance behavior of the Asian citrus psyllid, Diaphorina citri, toward lady beetle trail chemicals demonstrated that chemical cues of lady beetles can not only interfere with the feeding activity of prey but additionally reduce oviposition (Seo et al., 2018). Another study confirms that prey can discriminate between risky and suitable feeding sides by demonstrating that the Colorado potato beetle, Leptinotarsa decemlineata reduces feeding on potato leaves covered with predator cues, compared to a cue‐free control (Hermann & Thaler, 2014). Moreover, prior studies showed that disturbances in pea aphid behavior induced by predator cues can lead to increased searching behavior for suitable feeding sides and consequently decreased feeding times, resulting in reproductive costs (Nelson, 2007; Nelson et al., 2004). However, predator cues, covering the surrounding area, can lead to aphid dispersal to sites with less predator pressure and consequently reduce survival costs through immediate predator consumption (Roitberg et al., 1979). Chemical cues deposited by lady beetles were trail chemicals and feces. According to Ninkovic et al. (2013), a similar avoidance response of aphids was observed, when feces were excluded from the experiments and only the trail chemicals of lady beetles were considered, suggesting that the effect of feces on the avoidance behavior of aphids is negligible (Ninkovic et al., 2013). Thus, our findings suggest that chemical lady beetle cues can equally repel aphids and might subsequently serve as a signal for predation risk. Future field studies should target the effects of lady beetle cues on aphid dispersal and the reproduction of aphids, to shed light on the non‐consumptive effects on aphid populations.

The avoidance of non‐native H. axyridis cues by North American pea aphids might be explained by the strong selection pressure by non‐native predators on native prey, leading to the evolution of antipredator behaviors (Carthey & Blumstein, 2018). In a maritime system, for example, the intertidal snail Littorina obtusata responded to the increasing predation pressure of the intertidal crab (Carcinus maenas), which was expanding its range, with rapid morphological change of shell forms (Seeley, 1986). Moreover, research on cue avoidance behavior in mammals showed that native common ringtail possum (Pseudocheirus peregrinus) recognized and subsequently avoided olfactory cues of the invasive European red fox (Vulpes vulpes), within a few generations of co‐evolution (Anson & Dickman, 2013).In addition, our results show that H. axyridis is among the largest and most voracious predators tested; since large predators can pose a greater thread for prey, this can result in stronger antipredator responses by prey (see Binz et al., 2014).

The cue avoidance experiments in North America and Europe revealed differences in avoidance behavior toward cues of the non‐native H. axyridis. In contrast to North America, the European pea aphids showed no avoidance behavior toward H. axyridis cues, indicating predator–prey naïveté (sensu Cox & Lima, 2006, Sih et al., 2010). North American and European pea aphid populations used for the experiments were maintained for more than 10 years in the laboratory and were expected to have experienced only low densities of established non‐native lady beetle species in the field. However, pea aphids and non‐native lady beetles coexisted prior to the establishment of non‐native lady beetle species in North America (Gordon, 1985; Harmon et al., 2007). According to regional studies, H. axyridis was first reported in 1992 in Kentucky (Cottrell & Yeargan, 1998). In contrast, pea aphids have a longer history in Kentucky, for example, a study on the parasitation rate of the non‐native parasitoid Aphidius smithi on pea aphids was conducted from 1967 to January 1970 confirming the pest status of pea aphids in agricultural environments (Pass & Parr, 1971). Although the regional co‐occurrence between H. axyridis and A.pisum might not exceed 10 years, the migration history of non‐native H. axyridis as well as pea aphids throughout North America must be considered (Brown et al., 2011; Lamb & MacKay, 1979), suggesting prior co‐evolutionary history in agricultural sides beyond Kentucky. Specifically, in North America, H. axyridis was released in multiple agricultural landscapes starting in 1916 (Gordon, 1985) and was repeatedly reintroduced as a biological control agent to control agricultural pest species (Gordon, 1985; Lombaert et al., 2014; Tedders & Schaefer, 1994). Thus, the frequency of predator–prey encounters and the length of co‐evolutionary time since introduction can be decisive for the evolution of antipredator behaviors (Gérard et al., 2014; Nelson, 2007). In North America, we suggest that North American pea aphid populations might have evolved cue avoidance behavior toward H. axyridis during the longer co‐evolutionary time spend in shared agricultural fields (Gordon, 1985). In contrast, co‐evolutionary history of A. pisum is shorter with H. axyridis populations in Europe, compared to that of North American populations (Brown et al., 2011; Gordon, 1985). In Europe, H. axyridis was introduced in the 1990s and the establishment period ranged from 2000–2007 (Brown et al., 2011; Klausnitzer, 2002). The European aphid laboratory colony was established, when spread and establishment of H. axyridis started in Central Europe (Brown et al., 2011). Consequently, the European aphid colony has experienced low H. axyridis densities, if any. Our results thus provide a snapshot of initial interactions between pea aphids and H. axyridis in Europe. To enhance our comprehension of evolutionary changes in non‐native predator–prey interactions, long‐term studies are required, starting with the initial introduction of the non‐native predator (Anton et al., 2020; Mallon et al., 2015).

The repelling substances within the chemical cues of lady beetles, inducing cue avoidance behavior in pea aphids, are unknown and remain to be identified. It might be possible that rather than evolutionary changes, cue similarities between chemical cues of H. axyridis and native lady beetles might have resulted in avoidance behavior of A. pisum when H. axyridis was introduced to North America. However, in Europe, chemical cues of the non‐native H. axyridis were not avoided, indicating dissimilarity to cues of native lady beetle species. Thus, similarly to chemical cues of H. axyridis in Europe, chemical cues of H. axyridis might differ from cues of native lady beetle species in North America.

In North America, pea aphids avoided chemical cues of non‐native C. septempunctata and H. variegata to a similar extend as cues of the congeneric native C. novemnotata and H. convergens. Chemical cue similarities between congeneric non‐native C. septempunctata and H. variegata and native C. novemnotata and H. convergens in North America might contribute to the equally strong avoidance behavior in pea aphids. Here, cues of non‐native and native lady beetle species of the same genera can be similar (Magro et al., 2010) and consequently a similar response can be expected in prey, regardless of predator origin (Sih et al., 2010). However, the degree of cue similarity between the tested lady beetle species remains open and needs further attention. In addition, according to the “multipredator hypothesis,” prey retains evolved antipredator behaviors toward extinct predators in the presence of remaining predators (Blumstein, 2006). Pea aphids in Europe avoided chemical cues of the co‐evolved C. septempunctata and H. variegata to a similar extent, as pea aphids in North America. Thus, in North America chemical cue avoidance toward non‐native European C. septempunctata and H. variegata might be a retained innate antipredator response of pea aphids, which evolved prior to the introduction of pea aphids to North America in the beginning of the 19th century and remained due to the presence of congeneric native predators with potentially similar cues (e.g., C. novemnotata and H. convergens). Overall, the “multipredator hypothesis” in combination with chemical cue similarities of congeneric species might explain cue avoidance of congeneric non‐native C. septempunctata and H. variegata and native C. novemnotata and H. convergens in North America, as well as the similar strength of avoidance behavior between European and American pea aphids. Still further studies are required to evaluate retained antipredator behaviors in non‐native insect species beyond their native range. Next to H. axyridis, C. septempunctata was the largest and most voracious non‐native lady beetle species in North America tested. The regional co‐occurrence of pea aphids and C. septempunctata used in the experiments might exceed 10 years, since, for example, Buchele et al. (1992) reported C. septempunctata appearing in research plots in Kentucky in 1987. Similar to H. axyridis, the introduction and establishment of C. septempunctata in North America dates decades back (Angalet & Jacques, 1975; Kajita et al., 2012). This alternatively suggests that avoidance behavior of pea aphids toward chemical cues of C. septempunctata might have newly evolved in North America, due to the increased predation pressure by this large and voracious predator (see Binz et al., 2014).

In North America, the non‐native C. septempunctata and H. axyridis were the largest lady beetles tested and consumed the most aphids, compared to smaller lady beetle species. Food consumption increases with body mass, due to increasing metabolic requirements (Brose et al., 2008), confirming the positive relationship between lady beetle body area and aphid consumption rates. The successful establishment of a large predator can depend on, that is, predator size and prey availability (Crookes et al., 2019). In North America, C. septempunctata was primarily considered as a non‐native biological control agent on pest species, due to large size and voraciousness (Elliott et al., 1996). Predation advantages of invasive H. axyridis over the smaller native lady beetle species Cycloneda sanguinea on shared pest species were attributed to a dominance in intraguild interactions, wider dietary range, higher voracity, and larger size (Michaud, 2002). Moreover, we found that the smaller sized, non‐native H. variegata consumes a lower number of aphids, compared to C. septempunctata and H. axyirids in North America. Thus, asymmetric competition advantages over smaller native and non‐native species can benefit the larger non‐native H. axyridis on both continents and non‐native C. septempunctata in North America (Hoki et al., 2014; Michaud, 2002). Furthermore, a recent study found that the efficiency of resource utilization was comparatively higher in invasive H. axyridis than in native H. convergens, when allometric scaling was considered. In addition, aphid handling time was lower and maximum consumption rate was higher in H. axyridis, compared to native H. convergens, indicating that the invasive H. axyridis is the dominating competitor (Crookes et al., 2019). Additionally, C. septempunctata and H. axyridis are both successful intraguild predators of native coccinellids in their invaded range (Pell et al., 2008; Snyder et al., 2004), which is not only beneficial in dietary terms, but also reduces competition on shared resources (Yasuda et al., 2004, Dixon and Dixon, 2000). Overall, body size and correlated physiological and/or behavioral traits of invasive species can significantly contribute to a competition advantage toward native and non‐native predators (Hemptinne et al., 2012; Kajita & Evans, 2010; Michaud, 2002; Obrycki et al., 1998).

Based on the current status of H. axyridis and European lady beetle species in North America, the two larger species H. axyridis and C. septempunctata have spread all over the United States within few decades, compared to the smaller H. variegata, Propylea quatuordecimpuncata, and Adalia bipunctata, which kept a more local distribution in the North East (and North West for A. bipunctata; Gordon, 1985, Lost Ladybug Project 2020: www.lostladybug.org). Among other characteristics, we argue that a large body size can contribute to the invasion success of lady beetles due to increased food demands and thus stronger competition. Analyzes of a 24‐year dataset in southwestern Michigan revealed only significant declines in the relatively small Col. maculata and A. bipunctata (Bahlai et al., 2015). Likewise, A. bipunctata showed stronger declines in the presence of H. axyridis compared to other native lady beetle species, in Europe (Roy et al., 2012). In contrast, C. novemnotata maintained an ecological foothold in the face of invasion by the equally sized C. septempunctata (Evans, 2017). Thus, we suggest that lady beetle body size might be a good predictor for their invasion potential in areas beyond their native ranges.

In contrast to body size, differences in predator avoidance can diminish with time. Here, North American aphids but not European aphids avoided cues of the Asian H. axyridis. Such evolutionary adaptations can contribute to so called “boom‐bust dynamics”: invaders go through an initial outbreak before declining to a lower population size (Simberloff & Gibbons, 2004; Strayer et al., 2017). So far, evidence for a decline in H. axyridis populations is restricted to microsatellite effective population estimates (Sethuraman et al., 2018). In the long term, the adaptations of antipredator behaviors by aphids toward non‐native predators might result in a stable co‐existence within the native community and may consequently lead to a more harmless situation relative to the current impact of H. axyridis. Evolutionary responses to non‐native predators have important consequences for ecological studies aiming to elucidate the underlying mechanism of biological invasion such as a lack of avoidance behavior: Although lacking avoidance behavior toward non‐native predators during early stages of biological invasions benefits the non‐native predator, the mechanisms might no longer be detectable at later stages due to co‐evolution. Our results in concert with lady beetle distribution data in North America and in Europe indicate that relative lady beetle body size is a key predictor of the invasion success of non‐native lady beetle species, but also for native lady beetle species that are at particular risk if they co‐occur with non‐native lady beetles.

5. CONCLUSION

Missing avoidance behavior of European pea aphids toward chemical cues of non‐native H. axyridis suggests that non‐native predators can benefit from chemical cue novelty resulting in a lack of antipredator behavior of prey, during early stages of biological invasions. In contrast, North American pea aphids showed avoidance behavior toward H. axyridis cues, suggesting adaptations of avoidance behavior against voracious, non‐native predators. Overall, predation advantages of non‐native predators due to missing antipredator behaviors of prey might diminish with time, whereas body size‐related competition advantages over smaller native and non‐native predators could sustainably benefit large, non‐native predators.

CONFLICT OF INTEREST

None declared.

AUTHOR CONTRIBUTIONS

Ayse Gül Ünlü: Formal analysis (lead); investigation (lead); methodology (supporting); visualization (lead); writing–original draft (lead); writing–review and editing (equal). John Obrycki: Project administration (supporting); resources (supporting); supervision (supporting); writing–review and editing (supporting). Roman Bucher: Conceptualization (lead); funding acquisition (lead); methodology (lead); project administration (lead); supervision (lead); writing–review and editing (equal).

ACKNOWLEDGMENTS

We thank Nathan Mercer, Denise Bertleff, Jette Diekmann, and Sophia Brand for help with the maintenance and collecting of insects and the assistance with the experiments; the Department of Entomology at the University of Kentucky for the supply with technical equipment. We are grateful to the Julius Kühn‐Institut (Braunschweig, Germany) for providing pea aphids. We are thankful to the two anonymous reviewers for their valuable comments on earlier versions of the manuscript. The study was funded by the Deutsche Forschungsgemeinschaft (DFG) under grant number BU3382/1‐1 to RB. Open access funding enabled and organized by Projekt DEAL.

Ünlü AG, Obrycki JJ, Bucher R. Comparison of native and non‐native predator consumption rates and prey avoidance behavior in North America and Europe. Ecol Evol. 2020;10:13334–13344. 10.1002/ece3.6932

Funding information

The study was funded by the Deutsche Forschungsgemeinschaft (DFG) under grant number BU3382/1‐1 to RB.

DATA AVAILABILITY STATEMENT

We archived our data on the Dryad data repository: https://doi.org/10.5061/dryad.47d7wm3bt.

REFERENCES

  1. Alyokhin, A. , & Sewell, G. (2004). Changes in a lady beetle community following the establishment of three alien species. Biological Invasions, 6, 463–471. 10.1023/B:BINV.0000041554.14539.74 [DOI] [Google Scholar]
  2. Angalet, G. W. , & Jacques, R. L. (1975). The establishment of Coccinella septempunctata L. in the continental United States. Cooperative Economic Insect Report, 25, 883–884. [Google Scholar]
  3. Angalet, G. W. , Tropp, J. M. , & Eggert, A. N. (1979). Coccinella septempunctata in the United States: Recolonizations and notes on its ecology. Environmental Entomology, 8, 896–901. [Google Scholar]
  4. Anson, J. R. , & Dickman, C. R. (2013). Behavioral responses of native prey to disparate predators: naiveté and predator recognition. Oecologia, 171, 367–377. 10.1007/s00442-012-2424-7 [DOI] [PubMed] [Google Scholar]
  5. Anton, A. , Geraldi, N. R. , Ricciardi, A. , & Dick, J. T. (2020). Global determinants of prey naiveté to exotic predators. Proceedings of the Royal Society B, 287, 20192978 10.1098/rspb.2019.2978 [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bahlai, C. A. , Colunga‐Garcia, M. , Gage, S. H. , & Landis, D. A. (2015). The role of exotic ladybeetles in the decline of native ladybeetle populations: Evidence from long‐term monitoring. Biological Invasions, 17, 1005–1024. 10.1007/s10530-014-0772-4 [DOI] [Google Scholar]
  7. Bertleff, D. , Diekmann, J. , Brand, S. , Ünlü, A. G. , & Bucher, R. (2020). Predation and avoidance behaviour in aphid‐ladybird interactions of native and invasive ladybirds in Europe. Ecological Entomology, 10.1111/een.12938 [DOI] [Google Scholar]
  8. Binz, H. , Bucher, R. , Entling, M. H. , & Menzel, F. (2014). Knowing the risk: Crickets distinguish between spider predators of different size and commonness. Ethology, 120, 99–110. 10.1111/eth.12183 [DOI] [Google Scholar]
  9. Blumstein, D. T. (2006). The multipredator hypothesis and the evolutionary persistence of antipredator behavior. Ethology, 112, 209–217. 10.1111/j.1439-0310.2006.01209.x [DOI] [Google Scholar]
  10. Brose, U. , Ehnes, R. B. , Rall, B. C. , Vucic‐Pestic, O. , Berlow, E. L. , & Scheu, S. (2008). Foraging theory predicts predator–prey energy fluxes. Journal of Animal Ecology, 77, 1072–1078. 10.1111/j.1365-2656.2008.01408.x [DOI] [PubMed] [Google Scholar]
  11. Brown, P. M. , Thomas, C. E. , Lombaert, E. , Jeffries, D. L. , Estoup, A. , & Handley, L. J. L. (2011). The global spread of Harmonia axyridis (Coleoptera: Coccinellidae): Distribution, dispersal and routes of invasion. BioControl, 56, 623–641. 10.1007/s10526-011-9379-1 [DOI] [Google Scholar]
  12. Bucher, R. , Binz, H. , Menzel, F. , & Entling, M. H. (2014). Spider cues stimulate feeding, weight gain and survival of crickets. Ecological Entomology, 39, 667–673. 10.1111/een.12131 [DOI] [Google Scholar]
  13. Caltagirone, L. E. , & Doutt, R. L. (1989). The history of the vedalia beetle importation to California and its impact on the development of biological control. Annual Review of Entomology, 34, 1–16. 10.1146/annurev.en.34.010189.000245 [DOI] [Google Scholar]
  14. Carthey, A. J. , & Blumstein, D. T. (2018). Predicting predator recognition in a changing world. Trends in Ecology & Evolution, 33, 106–115. 10.1016/j.tree.2017.10.009 [DOI] [PubMed] [Google Scholar]
  15. Chapin, J. B. , & Brou, V. A. (1991). Harmonia axyridis (Pallas), the third species of the genus to be found in the United States (Coleoptera: Coccinellidae). Proceedings of the Entomological Society of Washington, 93, 630–635. [Google Scholar]
  16. Costopoulos, K. , Kovacs, J. L. , Kamins, A. , & Gerardo, N. M. (2014). Aphid facultative symbionts reduce survival of the predatory lady beetle Hippodamia convergens . BMC Ecology, 14, 5 10.1186/1472-6785-14-5 [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Cottrell, T. E. , & Yeargan, K. V. (1998). Intraguild predation between an introduced lady beetle, Harmonia axyridis (Coleoptera: Coccinellidae), and a native lady beetle, Coleomegilla maculata (Coleoptera: Coccinellidae). Journal of the Kansas Entomological Society, 159–163. [Google Scholar]
  18. Cox, J. G. , & Lima, S. L. (2006). Naïveté and an aquatic‐terrestrial dichotomy in the effects of introduced predators. Trends in Ecology & Evolution, 21, 674–680. [DOI] [PubMed] [Google Scholar]
  19. Crookes, S. , DeRoy, E. M. , Dick, J. T. , & MacIsaac, H. J. (2019). Comparative functional responses of introduced and native ladybird beetles track ecological impact through predation and competition. Biological Invasions, 21, 519–529. 10.1007/s10530-018-1843-8 [DOI] [Google Scholar]
  20. Dixon, A. F. G. , & Dixon, A. E. (2000). Insect predator‐prey dynamics: Ladybird beetles and biological control. Cambridge University Press. [Google Scholar]
  21. Doumbia, M. , Hemptinne, J.‐L. , & Dixon, A. F. G. (1998). Assessment of patch quality by ladybirds: Role of larval tracks. Oecologia, 113, 197–202. 10.1007/s004420050368 [DOI] [PubMed] [Google Scholar]
  22. Elliott, N. , Kieckhefer, R. , & Kauffman, W. (1996). Effects of an invading coccinellid on native coccinellids in an agricultural landscape. Oecologia, 105, 537–544. 10.1007/BF00330017 [DOI] [PubMed] [Google Scholar]
  23. Ellis, D. R. , Prokrym, D. R. , & Adams, R. G. (1999). Exotic lady beetle survey in northeastern United States: Hippodamia variegata and Propylea quatuordecimpunctata (Coleoptera: Coccinellidae). Entomological News., 110, 73–84. [Google Scholar]
  24. Evans, E. W. (2017). Fates of rare species under siege from invasion: persistence of Coccinella novemnotata Herbst in Western North America alongside an Invasive Congener. Frontiers in Ecology and Evolution, 5, 152 10.3389/fevo.2017.00152 [DOI] [Google Scholar]
  25. Fischer, S. , Samietz, J. , Wäckers, F. , & Dorn, S. (2001). Interaction of vibrational and visual cues in parasitoid host location. Journal of Comparative Physiology A, 187, 785–791. 10.1007/s00359-001-0249-7 [DOI] [PubMed] [Google Scholar]
  26. Fox, J. , & Weisberg, S. (2019). An R companion to applied regression (3rd ed.). Sage. [Google Scholar]
  27. Gérard, A. , Jourdan, H. , Cugnière, C. , Millon, A. , & Vidal, E. (2014). Is naïveté forever? Alien predator and aggressor recognition by two endemic island reptiles. Naturwissenschaften, 101, 921–927. 10.1007/s00114-014-1233-8 [DOI] [PubMed] [Google Scholar]
  28. Gordon, R. D. (1985). The Coleoptera (Coccinellidae) of America north of Mexico. Journal of the New York Entomological Society, 93. [Google Scholar]
  29. Gordon, R. D. (1987). The first North American records of Hippodamia variegata (Goeze) (Coleoptera: Coccinellidae). Journal of the New York Entomological Society, 95, 307–309. [Google Scholar]
  30. Harmon, J. P. , Hayden, A. , & Andow, D. A. (2008). Absence makes the heart grow fonder: Isolation enhances the frequency of mating in Coleomegilla maculata (Coleoptera: Coccinellidae). Journal of Insect Behavior, 21, 495–504. 10.1007/s10905-008-9145-0 [DOI] [Google Scholar]
  31. Harmon, J. P. , Stephens, E. , & Losey, J. (2007). The decline of native coccinellids (Coleoptera: Coccinellidae) in the United States and Canada. Journal of Insect Conservation, 11, 85–94. 10.1007/s10841-006-9021-1 [DOI] [Google Scholar]
  32. Hemptinne, J. L. , Lognay, G. , & Dixon, A. F. G. (1998). Mate recognition in the two‐spot ladybird beetle, Adalia bipunctata: Role of chemical and behavioural cues. Journal of Insect Physiology, 44, 1163–1171. 10.1016/S0022-1910(98)00081-X [DOI] [PubMed] [Google Scholar]
  33. Hemptinne, J. L. , Magro, A. , Evans, E. W. , & Dixon, A. F. G. (2012). Body size and the rate of spread of invasive ladybird beetles in North America. Biological Invasions, 14, 595–605. 10.1007/s10530-011-0101-0 [DOI] [Google Scholar]
  34. Hermann, S. L. , & Thaler, J. S. (2014). Prey perception of predation risk: Volatile chemical cues mediate non‐consumptive effects of a predator on a herbivorous insect. Oecologia, 176, 669–676. 10.1007/s00442-014-3069-5 [DOI] [PubMed] [Google Scholar]
  35. Hoki, E. , Losey, J. , & Ugine, T. A. (2014). Comparing the consumptive and non‐consumptive effects of a native and introduced lady beetle on pea aphids (Acyrthosiphon pisum). Biological Control, 70, 78–84. 10.1016/j.biocontrol.2013.12.007 [DOI] [Google Scholar]
  36. Horn, D. J. (1991). Potential impact of Coccinella septempunctata on endangered Lycaenidae (Lepidoptera) in Northwestern Ohio, USA In Behaviour and Impact of Aphidophaga (pp. 159–162). SPB Academic Publishing. [Google Scholar]
  37. Hothorn, T. , Bretz, F. , & Westfall, P. (2008). Simultaneous inference in general parametric models. Biometrical Journal: Journal of Mathematical Methods in Biosciences, 50, 346–363. 10.1002/bimj.200810425 [DOI] [PubMed] [Google Scholar]
  38. Hurst, G. D. D. , Bandi, C. , Sacchi, L. , Cochrane, A. G. , Bertrand, D. , Karaca, I. , & Majerus, M. E. N. (1999). Adonia variegata (Coleoptera: Coccinellidae) bears maternally inherited Flavobacteria that kill males only. Parasitology, 118, 125–134. [DOI] [PubMed] [Google Scholar]
  39. Kajita, Y. , & Evans, E. W. (2010). Relationships of body size, fecundity, and invasion success among predatory lady beetles (Coleoptera: Coccinellidae) inhabiting alfalfa fields. Annals of the Entomological Society of America, 103, 750–756. 10.1603/AN10071 [DOI] [Google Scholar]
  40. Kajita, Y. , O'Neill, E. M. , Zheng, Y. , Obrycki, J. J. , & Weisrock, D. W. (2012). A population genetic signature of human releases in an invasive ladybeetle. Molecular Ecology, 21, 5473–5483. 10.1111/mec.12059 [DOI] [PubMed] [Google Scholar]
  41. Kats, L. B. , & Dill, L. M. (1998). The scent of death: Chemosensory assessment of predation risk by prey animals. Ecoscience, 5, 361–394. 10.1080/11956860.1998.11682468 [DOI] [Google Scholar]
  42. Klausnitzer, B. (2002). Harmonia axyridis (Pallas, 1773) in Deutschland (Col., Coccinellidae). Entomologische Nachrichten Und Berichte, 46, 177–183. [Google Scholar]
  43. Koch, R. L. (2003). The multicolored Asian lady beetle, Harmonia axyridis: A review of its biology, uses in biological control, and non‐target impacts. Journal of Insect Science, 3 10.1093/jis/3.1.32 [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Kosaki, A. , & Yamaoka, R. (1996). Chemical composition of footprints and cuticula lipids of three species of lady beetles. Japanese Journal of Applied Entomology and Zoology, 40, 47–53. 10.1303/jjaez.40.47 [DOI] [Google Scholar]
  45. Lamb, R. J. , & MacKay, P. A. (1979). Variability in migratory tendency within and among natural populations of the pea aphid, Acyrthosiphon pisum . Oecologia, 39, 289–299. 10.1007/BF00345440 [DOI] [PubMed] [Google Scholar]
  46. Laundré, J. W. , Hernández, L. , & Altendorf, K. B. (2001). Wolves, elk, and bison: Reestablishing the" landscape of fear" in Yellowstone National Park, USA. Canadian Journal of Zoology, 79, 1401–1409. 10.1139/z01-094 [DOI] [Google Scholar]
  47. Lima, S. L. (1998). Nonlethal effects in the ecology of predator‐prey interactions. BioScience, 48, 25–34. 10.2307/1313225 [DOI] [Google Scholar]
  48. Lima, S. L. , & Dill, L. M. (1990). Behavioral decisions made under the risk of predation: A review and prospectus. Canadian Journal of Zoology, 68, 619–640. 10.1139/z90-092 [DOI] [Google Scholar]
  49. Lombaert, E. , Guillemaud, T. , Lundgren, J. , Koch, R. , Facon, B. , Grez, A. , Loomans, A. , Malausa, T. , Nedved, O. , Rhule, E. , Staverlokk, A. , Steenberg, T. , & Estoup, A. (2014). Complementarity of statistical treatments to reconstruct worldwide routes of invasion: The case of the Asian ladybird Harmonia axyridis . Molecular Ecology, 23, 5979–5997. [DOI] [PubMed] [Google Scholar]
  50. Magro, A. , Ducamp, C. , Ramon‐Portugal, F. , Lecompte, E. , Crouau‐Roy, B. , Dixon, A. F. G. , & Hemptinne, J. L. (2010). Oviposition deterring infochemicals in ladybirds: The role of phylogeny. Evolutionary Ecology, 24, 251–271. 10.1007/s10682-009-9304-6 [DOI] [Google Scholar]
  51. Mallon, C. A. , Van Elsas, J. D. , & Salles, J. F. (2015). Microbial invasions: The process, patterns, and mechanisms. Trends in Microbiology, 23, 719–729. 10.1016/j.tim.2015.07.013 [DOI] [PubMed] [Google Scholar]
  52. Menzel, F. , Morsbach, S. , Martens, J. H. , Räder, P. , Hadjaje, S. , Poizat, M. , & Abou, B. (2019). Communication versus waterproofing: The physics of insect cuticular hydrocarbons. Journal of Experimental Biology, 222, 1–11. 10.1242/jeb.210807 [DOI] [PubMed] [Google Scholar]
  53. Michaud, J. P. (2002). Invasion of the Florida citrus ecosystem by Harmonia axyridis (Coleoptera: Coccinellidae) and asymmetric competition with a native species, Cycloneda sanguinea . Environmental Entomology, 31, 827–835. [Google Scholar]
  54. Murdoch, W. W. , Briggs, C. J. , & Nisbet, R. M. (2003). Consumer‐resource dynamics (Vol. 36). Princeton University Press. [Google Scholar]
  55. Nelson, E. H. (2007). Predator avoidance behavior in the pea aphid: Costs, frequency, and population consequences. Oecologia, 151, 22–32. 10.1007/s00442-006-0573-2 [DOI] [PubMed] [Google Scholar]
  56. Nelson, E. H. , Matthews, C. E. , & Rosenheim, J. A. (2004). Predators reduce prey population growth by inducing changes in prey behavior. Ecology, 85, 1853–1858. 10.1890/03-3109 [DOI] [Google Scholar]
  57. Nichols, P. R. , & Neel, W. W. (1974). Sexing Coleomegilla maculata. Journal of Economic Entomology, 67, 136. [Google Scholar]
  58. Ninkovic, V. , Feng, Y. , Olsson, U. , & Pettersson, J. (2013). Ladybird footprints induce aphid avoidance behavior. Biological Control, 65, 63–71. 10.1016/j.biocontrol.2012.07.003 [DOI] [Google Scholar]
  59. Obrycki, J. J. , Giles, K. L. , & Ormord, A. M. (1998). Interactions between an introduced and indigenous coccinellid species at different prey densities. Oecologia, 117, 279–285. 10.1007/s004420050659 [DOI] [PubMed] [Google Scholar]
  60. Obrycki, J. J. , & Kring, T. J. (1998). Predaceous Coccinellidae in biological control. Annual Review of Entomology, 43, 295–321. 10.1146/annurev.ento.43.1.295 [DOI] [PubMed] [Google Scholar]
  61. Ohgushi, T. , Schmitz, O. , & Holt, R. D. (2012). Trait‐mediated indirect interactions: Ecological and evolutionary perspectives. Cambridge University Press. [Google Scholar]
  62. Pass, B. C. , & Parr, J. C. (1971). Seasonal occurrence of the pea aphid and a Braconid parasite, Aphidius smithi, in Kentucky. Journal of Economic Entomology, 64, 1150–1153. [Google Scholar]
  63. Peacor, S. D. , & Werner, E. E. (2000). Predator effects on an assemblage of consumers through induced changes in consumer foraging behavior. Ecology, 81, 1998–2010. 10.1890/0012-9658(2000)081[1998:PEOAAO]2.0.CO;2 [DOI] [Google Scholar]
  64. Peccoud, J. , Ollivier, A. , Plantegenest, M. , & Simon, J. C. (2009a). A continuum of genetic divergence from sympatric host races to species in the pea aphid complex. Proceedings of the National Academy of Sciences, 106, 7495–7500. 10.1073/pnas.0811117106 [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Peccoud, J. , Simon, J. C. , McLaughlin, H. J. , & Moran, N. A. (2009b). Post‐Pleistocene radiation of the pea aphid complex revealed by rapidly evolving endosymbionts. Proceedings of the National Academy of Sciences, 106, 16315–16320. 10.1073/pnas.0905129106 [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Pell, J. K. , Baverstock, J. , Roy, H. E. , Ware, R. L. , & Majerus, M. E. (2008). Intraguild predation involving Harmonia axyridis: A review of current knowledge and future perspectives. BioControl, 53, 147–168. 10.1007/s10526-007-9125-x [DOI] [Google Scholar]
  67. Preisser, E. L. , Bolnick, D. I. , & Benard, M. F. (2005). Scared to death? The effects of intimidation and consumption in predator–prey interactions. Ecology, 86, 501–509. 10.1890/04-0719 [DOI] [Google Scholar]
  68. R Development Core Team (2017). R: A language and environment for statistical computing. R Foundation for Statistical Computing; Retrieved from https://www.R‐project.org/ [Google Scholar]
  69. Riddick, E. W. , & Schaefer, P. W. (2005). Occurrence, density, and distribution of parasitic fungus Hesperomyces virescens (Laboulbeniales: Laboulbeniaceae) on multicolored Asian lady beetle (Coleoptera: Coccinellidae). Annals of the Entomological Society of America, 98, 615–624. [Google Scholar]
  70. Roitberg, B. D. , Myers, J. H. , & Frazer, B. D. (1979). The influence of predators on the movement of apterous pea aphids between plants. The Journal of Animal Ecology, 111–122. 10.2307/4104 [DOI] [Google Scholar]
  71. Rosier, R. L. , & Langkilde, T. (2011). Behavior under risk: How animals avoid becoming dinner. Nature Education Knowledge, 2, 8. [Google Scholar]
  72. Roy, H. E. , Adriaens, T. , Isaac, N. J. B. , Kenis, M. , Onkelinx, T. , San, M. G. , Brown, P. M. J. , Hautier, L. , Poland, R. , Roy, D. B. , Comont, R. , Eschen, R. , Frost, R. , Zindel, R. , Van Vlaenderen, J. , Nedved, O. , Ravn, H. P. , Gregoire, J. C. , de Biseau, J. C. , & Maes, D. (2012). Invasive alien predator causes rapid declines of native European ladybirds. Diversity and Distributions, 18, 717–725. 10.1111/j.1472-4642.2012.00883.x [DOI] [Google Scholar]
  73. Roy, H. E. , & Brown, P. M. (2015). Ten years of invasion: Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) in Britain. Ecological Entomology, 40, 336–348. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Roy, H. E. , Rhule, E. , Harding, S. , Handley, L. J. L. , Poland, R. L. , Riddick, E. W. , & Steenberg, T. (2011). Living with the enemy: Parasites and pathogens of the ladybird Harmonia axyridis . BioControl, 56, 663–679. 10.1007/s10526-011-9387-1 [DOI] [Google Scholar]
  75. Seeley, R. H. (1986). Intense natural selection caused a rapid morphological transition in a living marine snail. Proceedings of the National Academy of Sciences, 83, 6897–6901. 10.1073/pnas.83.18.6897 [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Seo, M. , Rivera, M. J. , & Stelinski, L. L. (2018). Trail chemicals of the Convergens ladybird beetle, Hippodamia convergens, reduce feeding and oviposition by Diaphorina citri (Hemiptera: Psyllidae) on Citrus Plants. Journal of Insect Behavior, 31, 298–308. 10.1007/s10905-018-9680-2 [DOI] [Google Scholar]
  77. Sethuraman, A. , Janzen, F. J. , Rubio, M. A. , Vasquez, Y. , & Obrycki, J. J. (2018). Demographic histories of three predatory lady beetles reveal complex patterns of diversity and population size change in the United States. Insect Science, 25, 1065–1079. 10.1111/1744-7917.12481 [DOI] [PubMed] [Google Scholar]
  78. Sih, A. , Bolnick, D. I. , Luttbeg, B. , Orrock, J. L. , Peacor, S. D. , Pintor, L. M. , Preisser, E. , Rehage, J. S. , & Vonesh, J. R. (2010). Predator–prey naïveté, antipredator behavior, and the ecology of predator invasions. Oikos, 119, 610–621. 10.1111/j.1600-0706.2009.18039.x [DOI] [Google Scholar]
  79. Simberloff, D. , & Gibbons, L. (2004). Now you see them, now you don’t! – population crashes of established introduced species. Biological Invasions, 6, 161–172. 10.1023/B:BINV.0000022133.49752.46 [DOI] [Google Scholar]
  80. Snyder, W. E. , Clevenger, G. M. , & Eigenbrode, S. D. (2004). Intraguild predation and successful invasion by introduced ladybird beetles. Oecologia, 140, 559–565. 10.1007/s00442-004-1612-5 [DOI] [PubMed] [Google Scholar]
  81. Stellwag, L. , & Losey, J. E. (2014). Sexual Dimorphism in North American Coccinellids: Sexing methods for species of Coccinella L. (Coleoptera: Coccinellidae) and Implications for Conservation Research. The Coleopterists Bulletin, 68, 271–281. 10.1649/0010-065X-68.2.271 [DOI] [Google Scholar]
  82. Strayer, D. L. , D’Antonio, C. M. , Essl, F. , Fowler, M. S. , Geist, J. , Hilt, S. , Jarić, I. , Jöhnk, K. , Jones, C. G. , Lambin, X. , Latzka, A. W. , Pergl, J. , Pyšek, P. , Robertson, P. , von Schmalensee, M. , Stefansson, R. A. , Wright, J. , & Jeschke, J. M. (2017). Boom‐bust dynamics in biological invasions: Towards an improved application of the concept. Ecology Letters, 20, 1337–1350. 10.1111/ele.12822 [DOI] [PubMed] [Google Scholar]
  83. Tedders, W. L. , & Schaefer, P. W. (1994). Release and establishment of Harmonia axyridis (Coleoptera: Coccinellidae) in the southeastern United States. Entomological News, 105, 228–243. [Google Scholar]
  84. Terborgh, J. , & Estes, J. (2010). Trophic Cascades: Predators, Prey and the Changing Dynamics of Nature. Island Press. [Google Scholar]
  85. Thomas, C. (1878). A list of the species of the tribe Aphidini, family Aphidae, found in the United States, which have been heretofore named, with descriptions of some new species. Bulletin of the Illinois State Laboratory of Natural History, 2, 3–16. [Google Scholar]
  86. Trouve, C. , Ledee, S. , Ferran, A. , & Brun, J. (1997). Biological control of the damson‐hop aphid, Phorodon humuli (Hom.: Aphididae), using the ladybeetle Harmonia axyridis (Col.: Coccinellidae). Entomophaga, 42, 57–62. 10.1007/BF02769880 [DOI] [Google Scholar]
  87. Ünlü, A. G. , Terlau, J. F. , & Bucher, R. (2020). Predation and avoidance behavior of the pea aphid Acyrthosiphon pisum confronted with native and invasive lady beetles in Europe. Biological Invasions, 22, 1647–1656. 10.1007/s10530-020-02209-5 [DOI] [Google Scholar]
  88. Ware, R. , Yguel, B. , & Majerus, M. (2009). Effects of competition, cannibalism and intra‐guild predation on larval development of the European coccinellid Adalia bipunctata and the invasive species Harmonia axyridis . Ecological Entomology, 34, 12–19. [Google Scholar]
  89. Yasuda, H. , Evans, E. W. , Kajita, Y. , Urakawa, K. , & Takizawa, T. (2004). Asymmetric larval interactions between introduced and indigenous ladybirds in North America. Oecologia, 141, 722–731. 10.1007/s00442-004-1680-6 [DOI] [PubMed] [Google Scholar]

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Data Availability Statement

We archived our data on the Dryad data repository: https://doi.org/10.5061/dryad.47d7wm3bt.

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