Thaumastocoris Peregrinus, a Pest of Eucalyptus
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Mothers in the woods: Multitrophic interactions and oviposition preference in the bronze bug Thaumastocoris peregrinus, a pest of Eucalyptus. Gonzalo Martínez Thesis committee Promotor Prof. Dr Marcel Dicke Professor of Entomology Wageningen University & Research Co-promotor Dr Andrés González Associate Professor, Laboratory of Chemical Ecology Universidad de la República, Uruguay Other members Prof. Dr Jaap Bakker, Wageningen University & Research Prof. Dr Vanda H.P. Bueno, University of São Paulo, Brazil Dr Nina E. Fatouros, Wageningen University & Research Dr Astrid T. Groot, University of Amsterdam This research was conducted under the auspices of the C. T. de Wit Graduate School for Production Ecology & Resource Conservation. Mothers in the woods: Multitrophic interactions and oviposition preference in the bronze bug Thaumastocoris peregrinus, a pest of Eucalyptus. Gonzalo Martínez Thesis submitted in fulfilment of the requirements for the degree of doctor at Wageningen University by the authority of the Rector Magnificus, Prof. Dr A.P.J. Mol, in the presence of the Thesis Committee appointed by the Academic Board to be defended in public on Tuesday 17 October 2017 at 1:30 p.m. in the Aula. Gonzalo Martínez Mothers in the woods: Multitrophic interactions and oviposition preference in the bronze bug Thaumastocoris peregrinus, a pest of Eucalyptus, 176 pages. PhD thesis, Wageningen University, Wageningen, the Netherlands (2017) With references, with summaries in English and Spanish ISBN: 978-94-6343-678-6 DOI: 10.18174/421937 …um leve leviatã (Caetano Veloso, Manhatã) Table of contents 7 Chapter 1 Introduction and thesis outline 20 Chapter 2 Behavioral ecology of oviposition-site selection in herbivorous true bugs Gonzalo Martínez, Roxina Soler & Marcel Dicke 51 Chapter 3 Life-history analysis of Thaumastocoris peregrinus in a newly designed mass rearing strategy Gonzalo Martínez, Lesly López, Gissel Cantero, Andrés González &Marcel Dicke 63 Chapter 4 Oviposition preference but not adult feeding preference matches with offspring performance in the bronze bug Thaumastocoris peregrinus Gonzalo Martínez, María Victoria Finozzi, Gissel Cantero, Roxina Soler, Marcel Dicke & Andrés González 85 Chapter 5 Effect of the eucalypt lerp psyllid Glycaspis brimblecombei on adult feeding, oviposition-site selection and offspring performance by the bronze bug Thaumastocoris peregrinus Gonzalo Martínez, Andrés González & Marcel Dicke 99 Chapter 6 Rearing and releasing the egg parasitoid Cleruchoides noackae, a biological control agent for the bronze bug in Uruguay Gonzalo Martínez, Andrés González & Marcel Dicke 117 Chapter 7 Chemical cues exploited by Cleruchoides noackae to locate its host Gonzalo Martínez, Marcel Dicke & Andrés González 137 Chapter 8 General discussion: Integrating lessons from Thaumastocoris peregrinus oviposition preferences towards the improvement of pest management in Eucalyptus plantations 145 Summary 151 Sumario 157 About the author 161 Publications 165 Training and education statement 169 Acknowledgements Chapter 1 Introduction and thesis outline 10 Mothers in the woods From 1990 to 2015 global tree plantation area has increased from 167.5 million to 277.9 million hectares (Payn et al., 2015). Uruguay has accompanied this trend, experiencing an explosive growth after the passing of the Forestry Law (15.939) in 1988, leading to an increase of 1000 % of the area devoted to commercial tree plantations from this date to 2010 (Morey & Porcile, 2002; Ligrone, 2011). Currently, it reaches a million hectares, 800,000 of which are planted with monospecific stands of Eucalyptus (Boscana et al., 2016). Eucalyptus- based forestry benefited in the beginning from a relatively benign sanitary situation, given the distance from the area of origin of the genus (Jeffries & Lawton, 1984). However, the expanding area and the elapsed time have promoted the introduction of pests and diseases from the center of origin of Eucalyptus, threatening plantation productivity (Wingfield et al., 2008, 2013). Moreover, the introduction of invasive pests has been further enhanced in the last two decades by an increased global trade of seeds, plants and wood packaging material (Humble, 2010; Paine et al., 2011; Wingfield et al., 2013). Common pest management practices in forestry plantations include tree breeding, silvicultural management and chemical and biological control. Above all these strategies, classical biological control, defined as ‘the intentional introduction of an exotic, usually co- evolved, biological control agent for permanent establishment and long-term pest control’ (Eilenberg et al., 2001) represents one of the major ways forward for managing the global problem of invasive pests in tree plantations (Garnas et al., 2012), with many successful examples in forestry systems (Hanks et al., 1996; Cordero Rivera et al., 1999; Hodkinson, 1999; Protasov et al., 2007). However, implementing a classical biological control program is not exempt of difficulties, arising from many complex interacting factors (Hokkanen & Sailer, 1985; Hokkanen & Lynch, 2003). In order to establish a successful biological control program, research efforts must be invested in understanding the biology of both the pest and the potential biocontrol agents, as well as in developing effective rearing systems for both (Etzel & Legner, 1999). In recent years, an increasing number of studies have demonstrated that, because individuals species are embedded in a multitrophc context, behaviors such as oviposition-site selection by insects, are affected by bottom-up factors such as the quantity and quality of the host plant, and top-down factors such as the availability of enemy-free oviposition sites (Turlings et al., 1990; Bernays & Chapman, 1994; Dicke, 2000; Dicke & van Loon, 2000; Dicke et al., 2009). Chemical cues play an important role in these interactions, transferring information within the multitrophic system to organisms of the same or different trophic levels (Turlings et al., 1990, 1995; Dicke, 2000; Arimura et al., 2005; Dicke et al., 2009). For instance, marking and/or oviposition deterring pheromones can regulate egg distribution in herbivorous insects (Ditrick et al., 1983; Hilker & Klein, 1989; Blaakmeer et al., 1994; Hilker & Meiners, 2002), while parasitoid-attractive synomones can be released by the host plant in response to egg deposition (Vinson, 1976; Strand & Vinson, 1982, 1983; Colazza et al., 2004; Hilker & Fatouros, 2015). Despite the fact that such interactions among trophic levels may be of great importance in long-term systems such as plantation forestry, multitrophic studies in forestry systems are scarce. The characterization of the cues involved, and the understanding of their roles in regulating multitrophic interactions, may increase the probability of success of a biological control program. Chapter 1 11 The aim of this thesis was to investigate the factors affecting the oviposition behavior of an herbivorous true bug (Thaumastocoris peregrinus), within a multitrophic system comprised 1 of its host plant (Eucalyptus spp.), a common co-occurring sap-feeder (Glycaspis brimblecombei) and a specialist egg parasitoid (Cleruchoides noackae). Based on the information obtained, this study also pursued potential improvements in the management of T. peregrinus in Eucalyptus plantations. To achieve this, I focused on the preference-performance hypothesis, and tested preference-performance correlations assessing the effects of host-plant quality, the presence of conspecifics, or the infestation by a potential competitor. I also investigated host-selection behavior of the parasitoid, testing its responses towards different contact cues. I addressed the following research questions: (1) Is oviposition behavior of Thaumastocoris peregrinus affected by host-plant characteristics? (2) Is oviposition behavior of T. peregrinus affected by conspecifics? (3) Is oviposition affected by the presence of a co-occurring sap-feeder? (4) What cues does the egg parasitoid Cleruchoides noackae exploit to locate its host? Figure 1.1. Eucalyptus: (A) Commercial plantation of E. grandis; (B) Clonal plantation of E. grandis; (C) E. tereticornis. 12 Mothers in the woods Study system The Plant (Figure 1.1) The genus Eucalyptus, contains more than 500 species all endemic to Australia and New Guinea, more than 200 of which occur in Southeast Australia (Brooker & Kleinig, 1990). Eucalypts, also known as gum trees in Australia, are the most important dicotyledon species planted in forestry worldwide, particularly in the southern hemisphere (Paine et al., 2011). Eucalypts used in forestry are not deciduous species, so leaves may remain on a mature tree for two or even three years before falling (Brooker & Kleinig, 1990). Heteroblasty, i.e. the simultaneous presence of different leaf developmental stages, such as juvenile or adult leaves, is a remarkable characteristic of Eucalyptus species (Gras et al., 2005). Juvenile leaves usually differ in their morphology, phyllotaxy and wax content relative to adult leaves, providing an extra niche differentiation to herbivores (Brennan et al., 2001; Nahrung & Allen, 2003; Gras et al., 2005; Velikova et al., 2008). In Uruguay, 68% of the total area occupied by eucalypt plantations is planted as a source of fiber for the growing pulp industry (Boscana et al., 2016). The extant area is planted for timber, energy, or serve as shade and shelter for cattle. In the latter case, red gums such as Eucalyptus tereticornis Smith are usually