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Importance of Feeding Behaviour on Life Cycle in the Zoophytophagous Bug Dicyphus Geniculatus

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Importance of Feeding Behaviour on Life Cycle in the Zoophytophagous Bug Dicyphus Geniculatus Bulletin of Insectology 69 (2): 173-180, 2016 ISSN 1721-8861 Importance of feeding behaviour on life cycle in the zoophytophagous bug Dicyphus geniculatus 1 2 2 3 2 Francisco BEITIA , Josep Daniel ASÍS , Luis DE PEDRO , Marta GOULA , José TORMOS 1Unidad Asociada de Entomología IVIA/CIB-CSIC, Instituto Valenciano de Investigaciones Agrarias, Spain 2Área de Zoología, Facultad de Biología, Universidad de Salamanca, Spain 3Departament de Biologia Animal, Facultat de Biologia, Universitat de Barcelona, Spain Abstract Dicyphus geniculatus (Fieber) (Heteroptera Miridae) is a Mediterranean mirid that has been observed in public green areas in towns of eastern and western provinces of Spain feeding on whiteflies and thrips on Dianthus caryophyllus L. carnations. In this article, the relative importance of feeding behaviour with respect to the duration of nymphal development and nymphal survival, as well as reproduction, was investigated. Nymphs of Bemisia tabaci (Gennadius), larvae of Frankliniella occidentalis (Pergande) and carnation plants introduced into a 50 × 50 × 50 cm methacrylate box, together with adults mirids, in a climate-controlled chamber (25 ± 1 °C, 60 ± 5% HR, 16:8 h L:D photoperiod) were used to analyse feeding behaviour. In particular, data on realised fecundity, sex ratio and adult longevity were analysed. Realised fecundity differed significantly with respect to prey availability (F1, 267 = 44504.92; p ≤ 0.001). The sex ratio did not differ from 1(♂♂):2(♀♀+♂♂) with respect to feeding regimes [“with B. tabaci prey” (37/53+37 = 0.41), χ2 = 1.434, df 1, p = 0.231, “with F. occidentalis prey” (42/50+42 = 0.46), χ2 = 0.200, df 1, p = 0.655] or prey type (B. tabaci or F. occidentalis, χ2 = 0.564, df 1, p = 0.453). Adult longevity differed significantly in terms of prey availability (F2, 534 = 58.89, p ≤ 0.001) and longevity differed for each sex within each feeding regime (F1, 534 = 14.13; p ≤ 0.001). D. geniculatus can survive on a host plant diet exclusively but could not complete its development in the absence of supplemental prey food, indicating that D. geniculatus requires an animal component in its diet. Other zoophytophagous dicy- phines are successfully used as beneficials in integrated pest management in horticultural crops. Thus, D. geniculatus has a poten- tial role in the biological control of carnation pests, and therefore may be a promising pest biological control agent, thus contribut- ing to urban area sustainability. Key words: Dicyphus geniculatus, Miridae, Caryophyllaceae, zoophytophagy, biological control, urban green areas. Introduction aphids, thrips, leafminers, spider mites (Malausa et al., 1987; Malausa, 1989; Arzone et al., 1990; Alomar et Although mirid bugs (Heteroptera Miridae) have been al., 1991; Calabrò and Nucifora, 1993) and the more traditionally considered as phytophagous and include recently introduced South American tomato pinworm several agricultural pests, many of them also eat prey Tuta absoluta (Meyrick) (Urbaneja et al., 2009; Ingegno and are known to be zoophytophagous (Wheeler, et al., 2013). These pests are frequently found on both 2000a). Because of this partly predatorial feeding be- horticultural and ornamental crops, where they have a haviour, there is currently increasing recognition of their very high economic impact. However, most of the re- potential for use in pest biological control (Albajes and search and subsequent implementation has been under- Alomar, 1999; Alomar, 2002; Lucas and Alomar, 2002; taken on horticultural crops, and much less attention has Wheeler, 2000b; Urbaneja-Bernat et al., 2013; Maselou been devoted to the potential use of dicyphine zoophy- et al., 2014; Pérez Hedo et al., 2015). Nevertheless, in tophagous mirid species with ornamental crops, mainly order to maximise benefits and to minimise plant injury, due to the very low damage thresholds in these crops it is necessary to obtain information about the relative (Enkergaard and Brødsgaard, 2006) when aiming to influence that the host plant and prey availability have achieve a high-quality product (Gullino and Wardlow, on the biology of the zoophytophagous species (Ur- 1999; Marsh and Gallardo, 2009). Emerging research is baneja et al., 2005), and thus the ultimate utility of these being developed at present in Europe to explore possible facultative predators in the biological control of pests control of whiteflies among greenhouse ornamental (Wheeler, 2001). crops by M. pygmaeus, D. errans, Dicyphus eckerleini Several mirid Dicyphine zoophytophagous species Wagner, D. maroccanus and D. tamaninii. Examples of have been collected among open-field and/or protected successful IPM in ornamentals may be found in Gullino horticultural and ornamental crops in the Mediterranean and Wardlow (1999) and Murphy et al. (2011). Basin: Macrolophus pygmaeus (Rambur), Nesidiocoris Dicyphus geniculatus (Fieber) is widespread in tenuis (Reuter), Dicyphus errans (Wolff), Dicyphus ta- Europe, and its presence is also signalled in Turkey and maninii Wagner (Albajes and Alomar, 1999; Wheeler, Azerbaijan (Kerzhner and Josifov, 1999). Compared to 2001), Dicyphus hyalinipennis (Burmeister) (Ceglarska, other Dicyphus species, little information is known 1999), Dicyphus cerastii Wagner (Carvalho and Mexia, about D. geniculatus biology. Wagner and Weber 2000) and Dicyphus maroccanus Wagner (Abbas et al., (1964) name Salvia glutinosa L. (Lamiaceae) and Silene 2014). These species have been implicated in the bio- baccifera L. (Caryophyllaceae) as host plants. Éhanno logical control of several pests, such as whiteflies, (1987) reports observations of the species in grasslands in France, and S. baccifera. D. geniculatus has been re- D. geniculatus has been recorded among the Digitalis ported in northern Italy in horticultural areas in Pied- grandiflorum Miller (Ingegno et al., 2008) glabrous up- mont and Liguria regions, on Mentha sp. (Lamiaceae), side and sparsely pubescent underside (Tutin et al., Parietaria officinalis L. (Urticaceae) and Silene spp. 1972). Thus, several examples of dicyphine that do not (Tavella and Goula, 2001), as well as on S. glutinosa colonise hairy host plants may be found. In this context, and Digitalis grandiflorum Miller (Plantaginaceae) in D. geniculatus living on Dianthus caryophyllus should the Piedmont Alpine valley (Ingegno et al., 2008). As it not be surprising. occurs with other dicyphines, a mirid subtribe including D. caryophyllus has been appreciated as ornamental species that specialise in sticky plants (Wheeler, 2001; since ancient times, and it is the wild species from Wheeler and Krimmel, 2015), most D. geniculatus host which most commercial ornamental carnations have plant species are provided with trichomes, either glan- been derived (Chacón et al., 2013). Aside from its use dular or not; among vascular plants, 30% are sticky or as a cut flower and flower pot plant, D. caryophyllus has hairy (Duke, 1994). This latter group includes con- a long and strong reputation for medical use in the Far spicuous crops such as cotton, tomato and tobacco. The East (Chandra et al., 2016). Carnation cropping is effects of plant trichomes on predator efficacy have largely implemented. For example, in 2013 in Spain, been tested in many studies, and a good synthesis may more than 40% of flower crop surfaces were devoted to be found in Riddick and Simmons (2014a). Most studies growing carnations; exports of the crop increased nearly have shown that plant hairiness is detrimental to most 70% in 2013 (COAG, 2014). Unfortunately, production predatory insects; others have demonstrated a neutral is frequently at risk due to diseases and pests. In Spain, effect. A certain number of predatory insects adapt main carnation crop pests are thrips, mainly F. occiden- (Riddick and Simmons, 2014b). Plant trichomes make talis; aphids, mainly Myzus persicae Sulzer; leaf- herbivore locomotion more difficult and entrap pollen miners, Liriomyza dianthicola (Venturi); caterpillars, as well as insects (either tourist or not), providing a di- Cacoecimorpha pronubana (Hubner) and Epichoristo- versity of leaf surface resources (phylloplane) to insects des acerbella (Walker) (Belda and Moerman, 2008; that specialise in hairy plants (Krimmel, 2014). Entan- INFOAGRO, 2016). The presence of mites, spider mites, gled insects transform into carrion, which is attractive to scales, leaf miners and cutworms has also been reported dicyphine predators (Wheeler, 2001) in an interaction and some require quarantine (Trujillo et al., 1989; Aus- that is not very different from the mirid-spider interac- tralian Government, 2006). As is the rule for ornamen- tion (Wheeler and Krimmel, 2015). Stickiness may tals (Gullino and Wardlow, 1999), carnation crop pest therefore be interpreted as an indirect plant defence management usually relies on pesticides, although pre- (Krimmel and Pearse, 2013). ventive measures such as the sanitation of crop areas In the present work, D. geniculatus was observed on and seed certification or monitoring, together with IPM, carnations (Dianthus caryophyllus L.), which have are increasing (Belda and Moerman, 2008), with the aim leaves that are hairless and waxy, thus contrasting with of reducing the environmental pollution and pesticide most trichogenous host plants inhabited by dicyphines. exposure experienced by growers, labourers and appli- Voigt and Gorb (2010) hypothesise that dicyphine lo- cators, among others (Marsh and Gallardo, 2009). comotion on hairy plant surfaces may be carried out ac- For
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