Eur. J. Entomol. 109: 353–362, 2012 http://www.eje.cz/scripts/viewabstract.php?abstract=1718 ISSN 1210-5759 (print), 1802-8829 (online) Laboratory studies on intraguild predation and cannibalism among coccinellid larvae (Coleoptera: Coccinellidae) GABRIELE RONDONI, ANDREA ONOFRI and CARLO RICCI* Department of Agricultural and Environmental Sciences, University of Perugia, Borgo XX Giugno 74, 06121 Perugia, Italy; e-mail: [email protected] Key words. Coccinellidae, Harmonia axyridis, intraguild predation, biological control, invasive species, Italy, interval-censored survival analysis Abstract. Intraguild predation (IGP) and cannibalism occur in the field and could affect the dominance structure of guilds of cocci- nellid species. The exotic biological control agent Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) is now well established in most areas of Northern and Central Italy, but it is unclear what effect this species could have on native dominant and non-dominant coccinellids with which it co-occurs. In order to predict the trophic interactions in coccinellid guilds and the likely effect of H. axy- ridis, the incidence of IGP and cannibalism among the following six species were evaluated under laboratory conditions: H. axyridis, three native dominant species, Adalia bipunctata (L.), Oenopia conglobata (L.) and Coccinella septempunctata L. and two native non-dominant species, Platynaspis luteorubra (Goeze) and Scymnus apetzi (Mulsant). Unfed and fed fourth instar larvae of the above species were paired in an experimental arena and the incidence of predation recorded over a period of 24 h. In absence of aphids, the survival probabilities (SP) of A. bipunctata and O. conglobata were lowest when paired with either C. septempunctata or H. axyridis (< 0.20 SP after 24 h). The SP of C. septempunctata was similar if paired with either a conspecific larva or H. axyridis (< 0.34 SP after 24 h) and that of H. axyridis was reduced similarly if paired with either a conspecific larva or C. septempunctata (> 0.71 SP after 24 h). The SP of P. luteorubra was lower when paired with A. bipunctata and C. septempunctata (< 0.07 SP after 24 h) than with other species and that of S. apetzi was greatly reduced when paired with all the dominant and exotic species (< 0.27 SP after 24 h). In presence of aphids no predatory events occurred in most combinations. H. axyridis acted as a strong predator of native dominant and non-dominant coccinellids when the aphids are scarce. We did not find any evidence, however, that the incidence of IGP among exotic and native species is higher than either IGP or cannibalism in native species. The likelihood of IGP occurring in the field is discussed. INTRODUCTION 1996; Koch, 2003; Majerus et al., 2006). As H. axyridis is The exotic coccinellid Harmonia axyridis (Pallas) polyphagous it tends to co-occur with other ladybirds and (Coleoptera: Coccinellidae) was intentionally introduced compete for the same resources (Pell et al., 2008). Differ- into Northern Italy in the 1990s for the biological control ences in body size, mobility of the larvae and prey spe- of aphids and psyllids (Bazzocchi et al., 2004; Burgio et cific defences determine the outcome (Michaud, 2002; al., 2008). At present this species is established in several Lucas, 2005; Labrie et al., 2006; Provost et al., 2006; Pell areas of Northern and Central Italy and is spreading et al., 2008). (Burgio et al., 2008; Croci et al., 2010). The aim of this study is to describe in the laboratory the Several factors account for the success of the invasion predatory relationship in the new coccinellid guilds by H. axyridis (Majerus et al., 2006; Roy & Wajnberg, occurring in Central Italy. In particular, by comparing the 2008). Among these, the high incidence of intraguild pre- incidence of IGP by H. axyridis of native species with dation (IGP) by this species of native ladybirds is one of that of IGP and cannibalism among native species, in the most studied both in the Neartic (Kajita et al., 2000; order to assess the effect this exotic species may have on Michaud, 2002; Snyder et al., 2004; Yasuda et al., 2004) coccinellid guilds. and Palearctic regions (Burgio et al., 2002; Hautier et al., Due to their widespread occurrence and importance in 2008; Ware & Majerus, 2008). Laboratory and field suppressing aphid populations the native coccinellids assessments suggest that H. axyridis may be a top pre- selected for this study are, respectively, dominant [Adalia dator of several native species and the cause of a decrease bipunctata (L.), Oenopia conglobata (L.) and Coccinella in guild diversity (Nault & Kennedy, 2003; Roy et al., septempunctata L.] or non-dominant [Platynaspis luteo- 2006; Snyder & Evans, 2006; Pell et al., 2008; Brown et rubra (Goeze) and Scymnus apetzi (Mulsant)] species in al., 2011). agro-ecosystems in Central Italy. H. axyridis feeds on a wide range of different kinds of Under laboratory conditions, the incidence of IGP and prey (e.g. aphids, psyllids, coccids) in several habitats, cannibalism between fourth instar larvae of the above six such as trees and herbaceous crops (Hodek & Honek, species were quantified under two different feeding regimes, which were limiting or not limiting in terms of * GR and CR contributed to all the phases of the work and AO contributed to the statistical analysis. 353 TABLE 1. Number of replicates (n = 15) in which predation occurred when either unfed or fed larvae of Adalia bipunctata (L.), Oenopia conglobata (L.), Coccinella septempunctata L., Harmonia axyridis (Pallas), Platynaspis luteorubra (Goeze) and Scymnus apetzi (Muls.) were paired with one another for 24 h. For the prey species in each combination (columns) the different superscripts indicate significantly different survival curves (see Fig. 1) when paired with different predator species (rows). The difference between survival curves was assessed using logrank tests and Holm’s procedure to adjust for multiplicity, setting the family wise error rate to 0.05. Combinations where a species was never the prey (–) were excluded from the comparison. Prey species Treatment Predator species C. septem- A. bipunctata O. conglobata H. axyridis P. luteorubra S. apetzi punctata A. bipunctata 5 b 5 b – – 15 a 11 b O. conglobata 3 b 9 b – – 5 b 14 ab C. septempunctata 15 a 15 a 11 a 2 a 14 a 15 a Unfed larvae H. axyridis 12 a 15 a 9 a 4 a 5 b 14 ab P. luteorubra – – – – – – S. apetzi – – – – 4 b – A. bipunctata – – – – 1 3 a O. conglobata – – – – – – C. septempunctata – – – – – 6 a Fed larvae H. axyridis – – – – – 6 a P. luteorubra – – – – – – S. apetzi – – – – – – larval development. Larvae of these species overlap both species were collected in the hills near Perugia, Italy during temporally and spatially throughout spring and summer in 2009. a variety of crops in Central Italy (Ricci & Rondoni, Adults of the six species were reared in plexiglass cages (13 × unpubl. data). 20 × 30 cm), with holes in the walls covered with fine mesh to permit gas exchange, containing a pot (10 cm diam.) with 30–40 There are reports of H. axyridis adults and larvae Vicia faba minor L. sprouts moderately infested with A. fabae feeding on the eggs of other coccinellids (Cottrell & and absorbent paper or cotton as a substrate for oviposition. The Yeargan, 1998). While adults are highly mobile and fre- eggs were collected daily and transferred to clean Petri dishes. quently move between different habitats, the larvae are The larvae of all the species were reared in smaller cages (10 × more likely to remain in the same place in the field, which 12 × 20 cm) and fed horse bean sprouts infested with aphids. makes it more likely they will compete for food resources Insects were kept in a climatic chamber (25 ± 1°C, 70 ± 5% RH, and be involved in the IGP of other coccinellids (Obrycki 14L : 10D). The seeds of horse bean were sown in pots con- et al., 1998). Among the coccinellid developmental taining horticultural soil, watered daily and grown under the stages, the fourth instar larvae are known to be the most same controlled environmental condition as above. 2–3 days voracious (Yasuda & Ohnuma, 1999; Lee & Kang, 2004; after the emergence of the seedlings the plants were infested with A. fabae. Cabral et al., 2006), so this instar was used in the experi- ments reported here. Both adults of H. axyridis and larvae Experimental set up of C. septempunctata have been recorded eating conspe- To assess how the feeding status of larvae affects the inci- cifics in the field (Rondoni & Ricci, pers. observ.), so we dence of IGP between coccinellids, pairs of larvae that were included it in the experiments. The presence or absence of either starved or well fed were placed in an arena in one of the extraguild prey influences the intensity of the interactions 21 possible combinations of the six species including a conspe- cific one for each species, with each replicated 15 times. (Agarwala & Dixon, 1992; Rosenheim et al., 1995; Lucas The experimental arena used was a Petri dish (14 cm diam.) et al., 1998; Hindayana et al., 2001; Meyhöfer, 2001). in the lid of which there was a hole covered with netting for The black bean aphid, Aphis fabae Scop., was selected as ventilation. The bottom of the dish was lined with absorbent the extra-guild prey because it is a moderately suitable paper (14 cm diam.) moistened with tap water on which there prey for the larval development of the species studied or a were three clean sprouts of V. faba minor. common prey item in the habitats studied (Hodek & In the first experiment (unfed larvae) recently moulted (5 ± 4 Honek, 1996; Stathas et al., 2001; Soares et al., 2004; h) fourth-instar larvae of the six species were kept singly and Barbagallo & Ricci, 2006).