Predation Upon Adalia Bipunctata and Harmonia Axyridis Eggs by Chrysoperla Carnea Larvae and Orius Laevigatus Adults
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Bulletin of Insectology 59 (1): 53-58, 2006 ISSN 1721-8861 Predation upon Adalia bipunctata and Harmonia axyridis eggs by Chrysoperla carnea larvae and Orius laevigatus adults Fabrizio SANTI, Stefano MAINI Dipartimento di Scienze e Tecnologie Agroambientali - Entomologia, Università di Bologna, Italy Abstract Intra-guild predation (IGP) between sucking predators in relation to eggs of the exotic ladybird Harmonia axyridis (Pallas) and native Adalia bipunctata (L.) (Coleoptera Coccinellidae) was studied in laboratory. The green lacewing Chrysoperla carnea (Ste- phens) (Neuroptera Chrysopidae) and the pirate bug Orius laevigatus (Fieber) (Rhynchota Anthocoridae) may share the same niche as the two Coccinellidae species. Intra-guild predation may occur in glasshouses and crops when several predator species are used in integrated releases for the biocontrol of arthropod pests. In experimental arenas, the two sucking predators were individu- ally offered the choice between eggs of the two ladybird species. Adult O. laevigatus reared on frozen Ephestia kuehniella Zel- ler eggs were not seen to feed on ladybird eggs, and immediately rejected this kind of food. Conversely, C. carnea larvae at- tacked the ladybird eggs without showing a preference for either species, although we observed that the A. bipunctata eggs were either completely eaten or more shrivelled than those of H. axyridis. In prey suitability experiments, C. carnea larvae that were allowed to develop by being fed an ad libitum supply of A. bipunctata eggs took longer to develop and had a lower survivorship compared to data (from literature) on E. kuehniella frozen eggs. H. axyridis eggs were not suitable for the larval development of C. carnea. We discuss the relevance of these results and intra-guild predation to the use of these species as biocontrol agents. Key words: green lacewing, multicoloured Asian ladybird, two spotted ladybird, pirate bug, intra-guild predation, IGP, Ephestia kuehniella. Introduction teractions between polyphagous predators. Inoculative or augmentative releases and the side effects of intro- Intra-guild predation (IGP) represents an extreme form ducing exotic generalist predators are other issues that of competition between species (Polis et al., 1989). require accurate analyses (van Lenteren et al., 2003). In When an insect predator from a specific trophic level at- Italian agroecosystems, the biological and IPM control tacks another entomophagous arthropod from the same techniques recommend the use of the larvae of the green trophic level, and both species eat the same prey or fight lacewing Chrysoperla carnea (Stephens) (Neuroptera each other, we can define this interaction as intra-guild Chrysopidae) and several species of ladybirds (Coleop- predation (Polis and Holt, 1992). At low densities, poly- tera Coccinellidae) as a means of controlling aphids, phagous predators may eat common prey such aphids, combined with the pirate bug Orius laevigatus (Fieber) lepidopteran eggs, and larvae, but when prey and (Rhynchota Anthocoridae) as a means of controlling predator densities increase, the predators may also show thrips. These beneficial species are commercially avail- negative intraspecific interactions such as cannibalism able from European biofactories. The exotic Asian la- (Coderre et al., 1987; Majerus, 1994, Lucas et al., 1997; dybird Harmonia axyridis (Pallas) is a potential com- Hironori and Katsuhiro, 1997; Burgio et al., 2002; Santi petitor of native Coccinellidae, but is not yet established et al., 2003; Burgio et al., 2005). Within the community, in Italy (as far as we know), which may in part be be- predation risk of individuals depends upon a large range cause releases of this species in greenhouses and the of factors: the risk experienced may be reduced with an open field have been stopped. Recently, the flightless increase in body size as observed in Orius spp. by strain (Gil et al., 2004) has been reared and commer- Tommasini et al. (2002), but this risk is also dependent cially produced for the biological control of aphids in upon factors such as their mobility and the semiochemi- French greenhouses. The two spotted ladybird A. cals (allomones) that they produce as demonstrated in bipunctata is another candidate for augmentative re- Coccinellidae (Felix and Soares, 2004; Omkar et al., leases in Italy and other regions of Europe (Kehrli and 2004). The egg masses of ladybirds are generally not Wyss, 2001). The mouthparts of C. carnea larvae and O. protected externally, and therefore can be easily preyed laevigatus nymphs and adults allow these species to per- upon (Polis et al., 1989). However, Hemptinne et al. forate the egg chorion, and then suck the contents from (2000) found that some alkaloids are present in Adalia the egg. In commercial insectaries, C. carnea larvae and bipunctata (L.) and Coccinella septempunctata L. eggs, O. laevigatus are usually reared on the same artificial which may contribute to reducing intra-guild predation prey, i.e. the frozen eggs of Ephestia kuehniella Zeller. as in other ladybird species (Omkar et al., 2004). The intra-guild predation between C. carnea and O. When beneficial insects are released as biocontrol laevigatus has not been investigated previously because agents into agroecosystems and habitats such as pro- they rarely interact in the environment, due to their dif- tected crops, it is important to evaluate the possible in- fering modes of egg deposition (i.e. inside the vegetal Class 1 Class 2 A B Class 3 Class 4 Figure 1. Classes of feeding effects by C. carnea larvae on ladybird eggs (A: H. axyridis; B: A. bipunctata). tissues the pirate bugs and on stalk the green lacewing), The experimental arena was a 12 cm diameter glass but these species may be competitors for opportunities Petri dish. The border of the dish was treated with 5 mm to feed upon eggs. In the open field, O. laevigatus, C. of Teflon to stop the predators escaping. Inside the dish, carnea and A. bipunctata are found in the same weeds 10 fresh eggs of A. bipunctata and 10 of H. axyridis and shrubs nearest to the crops, and therefore these were placed alternately on a filter paper grid of 20 predators are the major contributors to the natural con- points (5 x 4 points separated at 16 x 14 mm distance). trol of insect pests in Italian agroecosystems (Burgio et The eggs were gently removed from a fresh egg cluster al., 2004; Tommasini, 2004). using a smooth brush. The aim of this study was to investigate in the labora- 25 second instar and 25 third instar C. carnea larvae tory the intra-guild predation between sucking generalist were individually released into the arena after being predators (C. carnea and O. laevigatus) in relation to starved for 24 hours. After introduction, the behaviour the exotic species H. axyridis and the indigenous spe- of the larvae was observed for two hours under a bin- cies A. bipunctata. ocular microscope. The behaviour of the larvae to the eggs was designated using the following categories (figure 1): Materials and methods Class 1: the egg was rejected without mouth parts being inserted; The two ladybird species were reared in the laboratory Class 2: mouth parts were inserted, but the egg was under the conditions described by Burgio et al. (2002) immediately rejected; and Santi et al. (2003). The predators C. carnea and O. Class 3: mouth parts were inserted, with some of the laevigatus were supplied by a commercial producer egg contents eaten; (Bioplanet, Cesena, Italy). Class 4: mouth parts were inserted, with most or all of the egg contents eaten, or the egg ended up totally Choice tests of C. carnea larvae and ladybird egg shrivelled. species The number of rejected and attacked eggs (including Experiments were performed as choice tests in a rear- the eggs partially or totally eaten) according to the ing room at temperature of 25 °C ± 2, 60-70 RH, and above mentioned classes, was analysed using a signed light 300-400 lux. rank Wilcoxon non-parametric test. 54 1.2 2.5 Adalia eggs ns Adalia eggs Harmonia eggs 1.0 z=0.48 Harmonia eggs 2.0 0.8 ns gs g gs ns e g z=0 51 . 1.5 e z=0.52 o . o 0.6 N N n a 1.0 e an e 0.4 M M ns 0.5 0.2 z=0.40 0.0 0.0 Attacked Class1 Attacked Class1 rejected rejected Figure 2a. Choice test between the two species of lady- Figure 3a. Choice test between the two species of lady- bird eggs (A. bipunctata and H. axyridis) and second bird eggs (A. bipunctata and H. axyridis) and third in- instar larvae of C. carnea. star larvae of C. carnea. n.s.: P > 0.05 (Wilcoxon signed rank non-parametric n.s.: P > 0.05 (Wilcoxon signed rank non-parametric test, data given as mean ± S.E.). test, data given as mean ± S.E.). 0.6 1.6 Adalia eggs Adalia eggs Harmonia eggs 1.4 Harmonia eggs * 0.5 * z=3,2 z=2.12 * 1.2 z=2,66 gs * gs g z=2,07 0.4 g e 1.0 e . o o N ns 0.3 N 0.8 z=0 an an e ns e 0.6 M 0.2 M z=1,24 0.4 0.1 0.2 0.0 0.0 Class 2 Class 3 Class 4 Class 2 Class 3 Class 4 Figure 2b. Choice test between the two species of lady- Figure 3b. Choice test between the two species of lady- bird eggs attacked (A. bipunctata and H. axyridis) and bird eggs attacked (A. bipunctata and H. axyridis) and second instar larvae of C. carnea. third instar larvae of C. carnea. *: P < 0.05; n.s.: P > 0.05 (Wilcoxon signed rank non- *: P < 0.05; n.s.: P > 0.05 (Wilcoxon signed rank non- parametric test, data given as mean ± S.E.).