DOI: 10.1111/j.1570-7458.2008.00740.x

Blackwell Publishing Ltd Role of prey–host plant associations on Harmonia axyridis and balteatus reproduction and predatory efficiency

Ammar Alhmedi, Eric Haubruge & Frédéric Francis* Functional and Evolutionary Entomology, Gembloux Agricultural University, Passage des Déportés 2, B-5030 Gembloux, Belgium Accepted: 8 April 2008

Key words: host preference, integrated pest management, Coleoptera, Coccinellidae, Diptera, Syrphidae, , wheat, green pea, stinging nettle, hoverflies, ladybirds, tritrophic interactions, spatial distribution

Abstract In order to predict possible locations of Harmonia axyridis Pallas (Coleoptera: Coccinellidae) and Episyrphus balteatus DeGeer (Diptera: Syrphidae) in the field, we studied their oviposition and prey preferences in relation to several host plant–prey associations under laboratory conditions. Oviposi- tion preference of H. axyridis and E. balteatus females was determined for three (Homoptera: )–host plant associations: Microlophium carnosum Buckton on stinging nettle [Urtica dioica L. (Urticaceae)], Acyrthosiphon pisum Harris on green pea [Pisum sativum L. (Fabaceae)], and Sitobion avenae F. on wheat [Triticum aestivum L. (Poaceae)]. Prey preference of H. axyridis and E. balteatus larvae was determined with the aphids M. carnosum, A. pisum, and S. avenae. Harmonia axyridis females showed a strong oviposition preference for the stinging nettle– M. carnosum association. The preferred association for ovipostion by E. balteatus was pea-hosting A. pisum, on which fecundity was also highest. Feeding behaviour was less restricted in H. axyridis, in which the preferred preys were M. carnosum and S. avenae. A lower specificity of predation was observed in E. balteatus larvae with respect to A. pisum. These laboratory experiments may help us to understand the spatial distribution of H. axyridis and E. balteatus in the field.

fertility on a subsequent host (Jaenike, 1990; Cunningham Introduction et al., 1998). Other factors influencing oviposition preference In agroecosystems, the spatial distribution of species are competition for sites (Finch & Jones, 1987; Jaenike, is determined to a large extent by the oviposition behavior 1990; Dicke, 2000), presence of natural enemies (Root, of females, if their larvae have limited dispersal capabilities 1973; Ohsaki & Sato, 1994; Dicke, 2000), and distribution (Huignard et al., 1986; Hanks, 1999). Oviposition behavior of potential host plants (Wiklund, 1982; McLain, 1992; is central to many aspects of insect biology, for example, Päts et al., 1997). There is little information about how population dynamics and biological control. Female generalist predators, such as the aphidophagous multi- may show a preference for specific host plants as coloured Asian ladybird Harmonia axyridis Pallas (Coleoptera: oviposition sites. Such a preference can be influenced by Coccinellidae) and the hoverfly Episyrphus balteatus DeGeer various factors. For example, oviposition preference can be (Diptera: Syrphidae), decide which kind of prey to determined by experiences of the female as a . This has consume. Most insects are rather specific when choosing been demonstrated in some species (Jermy et al., 1968), their food (Hodek, 1993; Schoonhoven et al., 1998), and but not in others (Holopainen, 1989; Ntonifor et al., 1996). even generalist predators display a hierarchy of preferences Oviposition preference may also be influenced by early for different hosts (Sadeghi & Gilbert, 1999). adult experience (Traynier, 1984; Jaenike, 1990; Turlings Optimal foraging theory assumes that predators select et al., 1993), as experience on a previous host may affect prey in order to maximize their fitness through optimal choices based on the caloric and nutritive value of prey and *Correspondence: E-mail: [email protected] associated foraging costs (Stephen & Krebs, 1986). Several

© 2008 The Authors Entomologia Experimentalis et Applicata 128:49–56, 2008 Journal compilation © 2008 The Netherlands Entomological Society 49

50 Alhmedi et al. factors affect prey selection: (i) prey features, such as that females may be able to discriminate between aphid species (Molles & Pietruszka, 1987; Roger et al., 2000), size species. If this is the case, females should lay eggs more (Allan et al., 1987; Roger et al., 2000), mobility (Clements readily near suitable than moderately suitable or unsuitable & Harmsen, 1990; Eubanks & Denno, 2000), nutritional aphids. quality (Houck, 1991; Eubanks & Denno, 2000), and The larvae of many hoverfly species, such as the common population density (Jeschke & Tollrian, 2000); and (ii) hoverfly E. balteatus, are also important natural enemies of predator characteristics, such as size (Allan et al., 1987; aphids (Chambers & Adams, 1986; Tenhumberg, 1995). Erickson & Morse, 1997), age (Sullivan, 1984; Cisneros & While E. balteatus larvae feed on a wide variety of aphid Rosenheim, 1997), and feeding state (e.g., Molles & Pie- species, even within a single habitat (e.g., Mizuno et al., 1997), truszka, 1987; Houck, 1991). there are clear indications of host preferences. Episyrphus Harmonia axyridis is used as a control agent against aphid balteatus is recorded as being more generalized than other populations, because its larvae are voracious, polyphagous, syrphids, such as Syrphus ribesii (e.g., Ninomyia, 1957), and easy to rear (Ferran et al., 1996; Koch, 2003). As an adult, but typically this species is found in various prey colonies it is known to have strong dispersal capacities (Osawa, within one habitat (Wnuk, 1972; Mizuno et al., 1997). In 2000; Koch, 2003) and studies in North America have the present study, we investigate oviposition and predation shown that it can rapidly colonize large areas (Tedders & preference of H. axyridis and E. balteatus in relation to host Schaefer, 1994). In Europe, it has spread very rapidly, plant–prey associations. particularly since 2002, and feral populations of the species now exist in 13 European countries (Brown et al., 2007). Materials and methods Since 1999, the Belgian Ladybird Working Group has mapped all Belgian Coccinellidae and recorded data on Plant and insect materials substratum plants and habitat. The first feral H. axyridis All aphidophagous predators, aphids, and host plants used population in Belgium was recorded in 2001, but it has in our tests were cultured and reared at 22 ± 2 °C and at now colonized the whole country. Recorded occupancy in L16:D8 photoperiod. Similar climatic conditions were Belgium showed an average rate of increase of 189% used for all experiments. Culture medium for plant growth between 2002 and 2006 (Adriaens et al., 2008). Laboratory consisted of a mix of vermiculite and perlite. Broad bean experiments showed that H. axyridis is frequently involved plants were sown in pots (12 cm in diameter × 10 cm high; in intraguild interactions with other aphidophagous 9 seeds per pot) in a culture room. The broad bean aphid, species, such as the ladybird species Adalia bipunctata (L.) Megoura viciae Buckton, mass-reared on potted broad bean and Coccinella septempunctata L., both native to western in the laboratory, was used as prey for the predator cultures. Europe (Hironori & Katsuhiro, 1997; Cottrell & Yeargan, Wheat, pea, and stinging nettle plants were grown in 1998; Yasuda et al., 2001). In a previous field study, where pots (12 cm in diameter × 10 cm high) in a rearing room, Microlophium carnosum Buckton, Sitobion avenae F., and and used as host plants for the three aphid species in the Acyrthosiphon pisum Harris (all Homoptera: Aphididae) were oviposition preference experiments. A culture of the cereal the main aphids recorded in high numbers on stinging aphid, S. avenae, obtained from the Walloon Center of nettle, wheat, and pea, respectively, a spatial distribution Agronomic Research of Gembloux, was established on for H. axyridis was found: throughout the observation potted wheat. The pea aphid, A. pisum, reared on broad period, it was most abundant on stinging nettle, less in a pea bean plants in the laboratory, was established on potted crop, and absent from a wheat field (Alhmedi et al., 2007). green pea. The stinging nettle aphid, M. carnosum, was Several factors may have an impact on the oviposition collected from a natural area of nettle in Gembloux and behavior of aphidophagous ladybirds, such as (i) aphid cultured on potted stinging nettle in the laboratory. The species (Blackman, 1967; Olszak, 1988; Kalushkov & aphids mentioned here were the main aphid species recorded Hodek, 2004; Provost et al., 2006), (ii) aphid density on nettle, pea, and wheat in fields (Alhmedi et al., 2007). (Dixon, 1959), (iii) aphid colony age (Dixon, 2000), and Multicoloured Asian ladybird adults, H. axyridis, were (iv) presence of intra- or inter-specific competitors/predators obtained from Eric Lucas’ laboratory in Montreal, Canada, (Mills, 1982; Osawa, 1993; Burgio et al., 2002). Many experi- reared in an incubator for several generations, at 22 ± 2 °C ments have demonstrated that aphids are not all equally and L16:D8 photoperiod, and provided with bee-collected suitable for the larval growth or adult reproduction of a , crystalline sugar, and water. Pollen and water were particular ladybird species (Blackman, 1967; Olszak, 1988; changed once per week and egg batches were collected Kalushkov & Hodek, 2004). For example, C. septempunctata regularly. Adults and larvae were fed with M. viciae aphids adults respond differently to the kairomones produced by and reared on broad bean leaves and pollen in boxes of different aphid species (Sengonca & Liu, 1994). This indicates 10 × 30 × 10 cm.

Prey–host plant–Harmonia axyridis associations 51

The native hoverfly E. balteatus was cultured in wooden Statistical analysis cages (60 × 100 × 100 cm) with a sliding door. Adults were The results of the experiments were analyzed using maintained in a constant environment of 22 ± 2 °C and Minitab 15 and SAS (SAS Institute, 1998). Prior to the L16:D8 photoperiod, and they were provided with bee- analyses, data were checked for equal variances and collected pollen, crystalline sugar, and water. Pollen and normality, and log(n + 1) transformed if necessary. water were refreshed every 2 days. In the mass culture, Oviposition rates of H. axyridis and E. balteatus adult females were stimulated to oviposit by presenting females (non-choice) for plant + aphid were analyzed pots of broad bean infested with M. viciae. A batch of using one-way analysis of variance (ANOVA). Student– eggs that was laid over a 2–3-h period provided a cohort Newman–Keuls tests were run to compare the means of flies with synchronous larval emergence within 48– among treatments. Data on preference were analyzed 72 h. Emerged larvae were fed with M. viciae cultured on using χ2-test. broad bean.

Oviposition preference of Harmonia axyridis and Episyrphus balteatus Results Oviposition preference experiments were performed in Oviposition preference of Harmonia axyridis and Episyrphus balteatus the laboratory with 4-week-old adult females of H. axyridis and E. balteatus. The fertility of all females used was Non-choice experiment. Without an alternative option, assessed 3 days prior to the preference test by counting the H. axyridis females oviposited more on aphid-infested eggs laid on pots of broad bean infested with M. viciae. nettle than on other plants after 2 h (ANOVA: F2,27 = 11.58, All H. axyridis (1 day before ovipositional tests) and P<0.001). From 2–24 h after start, egg numbers did not

E. balteatus females (3 days before ovipositional tests) used differ among plants (F2,27 = 2.92, P = 0.071). For E. balteatus, had no previous exposure to aphids. Oviposition preference there was no significant difference (F2,27 = 1.87, P = 0.173) of adult females was tested in single- and dual-choice in the number of eggs laid after 2 h, but from 2–24 h after experiments. Three aphid/host plant associations (namely, the start of the experiment more eggs were laid on wheat with S. avenae, pea with A. pisum, and stinging aphid-infested pea (F2,27 = 10.33, P<0.001) than on either nettle with M. carnosum; in short ‘plant + aphid’) were aphid-infested wheat or nettle. Overall, H. axyridis offered. Ten replicates were run simultaneously for each laid more eggs on aphid-infested nettle (F2,27 = 16.61, test. Great care was taken to ensure that all replicate plants P<0.001) than on either aphid-infested wheat or pea, were the same size and contained the same number of while E. balteatus laid more eggs on aphid-infested pea aphids (200 aphids per plant). (F2,27 = 10.97, P<0.001) than on either aphid-infested wheat or nettle (Figure 1). Non-choice experiment. One day after the start of aphid infestation, a single gravid female was introduced into a Dual-choice experiment. After 2 h, H. axyridis females had plastic bottle (9 cm in diameter × 25 cm high), containing laid more eggs on nettle + aphid than on the other plants the potted plant + aphids. Eggs laid after 2 and 24 h were (χ2 = 56.0 for wheat + aphid; χ2 = 26.0 for pea + aphid; recorded in each replicate. both comparisons: d.f. = 1, P<0.001; Figure 2). From 2–24 h, a similar result was obtained: oviposition was highest on Dual-choice experiment. One day after the start of aphid nettle + aphid (χ2 = 112.8 for wheat + aphid; χ2 = 136.0 infestation, a single gravid female was introduced into a for pea + aphid; both comparisons: d.f. = 1, P<0.001). cage (25 × 25 × 35 cm), containing two different potted Comparing the two least preferred aphid/host plant plants and aphids. Eggs laid after 2 and 24 h were recorded combinations, oviposition was lowest on wheat + aphid in each replicate. (after 2 h: χ2 = 6.0, d.f. = 1, P = 0.014; 2–24 h: χ2 = 55.7, d.f. = 1, P<0.001). Predation preference of Harmonia axyridis and Episyrphus balteatus females laid significantly more eggs Episyrphus balteatus larvae on aphid-infested pea than on wheat + aphid (after 2 h: Second instars of H. axyridis and E. balteatus were starved χ2 = 182.0; 2–24 h: χ2 = 384.3; both: d.f. = 1, P<0.001) or overnight before their predation preference was tested in nettle + aphid (after 2 h: χ2 = 148.9; 2–24 h: χ2 = 121.6; dual-choice experiments, using the three aphid species as both: d.f. = 1, P<0.001). After 2 h, oviposition on wheat prey. Twenty aphid individuals per species were offered in + aphid and nettle + aphid did not differ (χ2 = 0.02, a Petri dish (9 cm in diameter). Ten replicates were run d.f. = 1, P = 0.881), but from 2–24 h more egges were simultaneously for each test. Aphids eaten were recorded laid on wheat + aphid (χ2 = 5.2, d.f. = 1, P = 0.022) after 2, 6, and 24 h. (Figure 2). 52 Alhmedi et al.

Figure 1 Oviposition rate (mean + SE number of eggs) of Harmonia axyridis and Episyrphus balteatus in a non-choice experiment according to host plant–prey association (gray bars represent green pea–Acyrthosiphon pisum association, black bars represent wheat–Sitobion avenae association, and white bars represent stinging nettle–Microlophium carnosum association). Bars capped with the same letter during each observation period are not significantly different (one-way ANOVA and Student–Newman–Keuls test: P<0.05).

Predation preference of Harmonia axyridis and 2 h: χ2 = 13.4; 6–24 h: χ2 = 20.8; both: d.f. = 1, P<0.001). Episyrphus balteatus larvae Harmonia axyridis larvae consumed more S. avenae than Overall, the consumption rate of second instars of M. carnosum during the first and second period (χ2 = 11.5, H. axyridis differed among aphid species: equal numbers d.f. = 1, P = 0.001 and χ2 = 4.5, d.f. = 1, P = 0.034, respectively), of S. avenae and M. carnosum were consumed (χ2 = 0.4, but more M. carnosum than S. avenae during the third d.f. = 1, P = 0.548), but fewer of A. pisum (compared with period (χ2 = 12.4, d.f. = 1, P<0.001). Ladybird larvae ate S. avenae: χ2 = 85.9; with M. carnosum: χ2 = 45.4; both: consistently more S. avenae than A. pisum (after 2 h: d.f. = 1, P<0.001). Consumption rates varied among χ2 = 23.9; 2–6 h: χ2 = 16.4; 6–24 h: χ2 = 26.2; all: d.f. = 1, observation intervals, where aphids eaten were counted P<0.001). after 2 h (0–2 h), 6 h (2–6 h), and 24 h (6–24 h) (Figure 3). Overall, the consumption rate of E. balteatus larvae also When M. carnosum and A. pisum were offered simultaneously, differed among aphid species: M. carnosum was eaten most H. axyridis larvae ate more M. carnosum than A. pisum (compared with S. avenae: χ2 = 14.4, d.f. = 1, P<0.001) and during the first and third period of the experiment (after equal numbers of S. avenae and A. pisum were consumed

Figure 2 Oviposition preference (mean + SE number of eggs) of Harmonia axyridis and Episyrphus balteatus in a dual-choice experiment for different host plant–prey associations (gray bars represent green pea–Acyrthosiphon pisum association, black bars represent wheat–Sitobion avenae association, and white bars represent stinging nettle–Microlophium carnosum association). Bars capped with the same letter during each observation period are not significantly different (χ2-test for observed and expected frequencies, null hypothesis: number of eggs laid is equal in all plants: P>0.05). Prey–host plant–Harmonia axyridis associations 53

Figure 3 Prey preference (mean + SE number of aphid consumed) of Harmonia axyridis and Episyrphus balteatus for different aphid species (gray bars represent Acyrthosiphon pisum, black bars represent Sitobion avenae, and white bars represent Microlophium carnosum). Bars capped with the same letter during each observation period are not significantly different (χ2-test for observed and expected frequencies, null hypothesis: number of eggs laid is equal in all plants: P>0.05).

(χ2 = 3.8, d.f. = 1, P = 0.050). When M. carnosum and Differential consumption rate might be indicative of the A. pisum were offered in combination, A. pisum was eaten ability of H. axyridis and E. balteatus larvae to differentiate more during the first 2 h (χ2 = 13.4, d.f. = 1, P<0.001), but between aphid species, and also shows differences in aphid thereafter it was eaten less (from 2–6 h: χ2 = 6.7, d.f. = 1, palatability, which may be due to differences in morphol- P = 0.010; 6–24 h: χ2 = 9.8, d.f. = 1, P = 0.002). During the ogy, behavior, and chemical constitution (Okamoto, 1966; first and third period, equal numbers of M. carnosum and Liepert & Dettner, 1996; Dixon, 2000). The oviposition S. avenae were consumed. Only from 2–6 h, M. carnosum and consumption preference observed in H. axyridis and was eaten more (χ2 = 8.6, d.f. = 1, P = 0.003). E. balteatus females and larvae in the present study may be explained by optimal foraging theory, which states that the female is likely to select oviposition sites harboring prey Discussion that will best support the development and survival of her When H. axyridis and E. balteatus females had no choice progeny (Kindlmann & Dixon, 1993). between aphid/host plant combinations, they oviposited Females and larvae of E. balteatus were found to be less on the plants offered. However, these generalist predators specific in comparison with H. axyridis: females preferred displayed significant differences in egg distribution and A. pisum on pea for oviposition, but larvae preferred prey consumption among the various aphid species. This M. carnosum for predation. Previous research by Röder result supports literature data that suggest selectivity of (1990) and Torp (1994) reported E. balteatus in equal oviposition (Mitchell, 1962; Niemczyk & Pruska, 1986; abundance in all biotypes. This finding also supports field Budenberg & Powell, 1992). When H. axyridis females observations by Alhmedi et al. (2007) of similar abundance were offered a choice, they oviposited preferably on stinging of E. balteatus in different habitats, in association with the nettle infested with M. carnosum, and least on wheat infested occurrence and abundance of aphids. Sadeghi & Gilbert with S. avenae. Similarly, H. axyridis larvae preferred to (1999) found that feeding preferences differed among prey on M. carnosum, whereas pea aphid was least eaten. female E. balteatus, indicating that part of a population These preferences of H. axyridis match with our field may be specialized, whereas the other part may consist observation that this predator was found most often on of generalist females. stinging nettle, and (much) less on pea or wheat (Alhmedi The oviposition and predation preference of H. axyridis et al., 2007). observed in the laboratory, as well the specific distribution 54 Alhmedi et al. previously recorded in the field (Alhmedi et al., 2007), may Brown PMJ, Adriaens T, Bathon H, Cuppen J, Goldarazena A help us to understand its invasion of agroecosystems. et al. (2007) Harmonia axyridis in Europe: spread and distri- For example, the introduction of stinging nettle in pest- bution of a non-native coccinellid. Biocontrol 53: 5–21. management strategies, as shelter for important natural Budenberg WJ & Powell W (1992) The role of honeydew as an enemies, could lead to undesirable increases of the top ovipositional stimulant for two species of syrphids. Entomologia Experimentalis et Applicata 64: 57–61. predator H. axyridis and subsequently enhance the negative Burgio G, Santi F & Maini S (2002) On intra-guild predation and interactions with native ladybirds, such as C. septempunctata cannibalism in Harmonia axyridis (Pallas) and Adalia bipunctata (Yasuda et al., 2004) and A. bipunctata (Burgio et al., 2005). L. (Coleoptera: Coccinellidae). Biological Control 24: 110– However, because H. axyridis will likely become perma- 116. nently established in many of the areas it has invaded, we Burgio G, Santi F & Maini S (2005) Intra-guild predation and must continue to advance our knowledge on how to reap cannibalism between Harmonia axyridis and Adalia bipunctata benefits in situations where H. axyridis is a potential adults and larvae: laboratory experiments. Bulletin of Insectology biological control agent and mitigate its effects in situations 58: 135–140. where it is a potential pest. Chambers RJ & Adams THL (1986) Quantification of the impact In conclusion, although H. axyridis is considered a poly- of hoverflies (Diptera: Syrphidae) on cereal aphids in winter phagous ladybird, ovipositing females seem to prefer the wheat: an analysis of field populations. Journal of Applied Ecology 23: 895–904. stinging nettle–M. carnosum complex. Future research is Cisneros JJ & Rosenheim JA (1997) Ontogenetic change of prey needed to study the orientation of H. axyridis movement preference in the generalist predator Zelus renardii and its from nettle zones toward crop field and vice versa. To this influence on predator-predator interactions. Ecological Ento- end, a laboratory and field study using kairomones for mology 22: 399–407. H. axyridis will be initiated. The aphid alarm pheromone Clements DR & Harmsen R (1990) Predatory behavior and prey- (E)-β-farnesene has already been found to attract stage preference of stigmaeid and phytoseid mites and their C. septempunctata (Al Abassi et al., 2000), A. bipunctata, potential compatibility in biological control. Canadian and E. balteatus (Francis et al., 2001, 2005). Entomologist 122: 321–328. 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