Feeding Preferences of the Aphidophagous Hoverfly

BioControl (2014) 59:427–435 DOI 10.1007/s10526-014-9577-8 Feeding preferences of the aphidophagous hoverfly Sphaerophoria rueppellii affect the performance of its offspring Rocco Amoro´s-Jimeńez • Ana Pineda • Alberto Fereres • M. A´ ngeles Marcos-Garcıá Received: 4 September 2013 / Accepted: 28 March 2014 / Published online: 11 April 2014 Ó International Organization for Biological Control (IOBC) 2014 Abstract Provision of additional floral resources in Keywords Syrphidae Á Transgenerational the crop is a successful strategy of conservation effects Á Floral resources Á Sweet alyssum Á biological control for attracting several natural ene- Coriander Á Sweet pepper mies including predatory syrphids. However, the selection of flower species is mainly based on visiting preferences, paying little attention to the link between Introduction preference and performance. In this study, we assess the influence of feeding on flowers of two insectary Habitat management through the addition of flowering plants (sweet alyssum and coriander) and flowers of a plants in and around crops is a strategy of conservation crop species (sweet pepper) on performance of the biological control that enhances the performance of parental and first generation of the syrphid Sphaero- natural enemies (Landis et al. 2000). The importance phoria rueppellii (Wiedemann) (Diptera: Syrphidae). of floral resources for a large number of natural We found that floral preference of the adults was enemies such as many parasitoid species as well as linked to developmental performance of their off- predators like Coccinellidae, Chrysopidae and Syr- spring. Sweet alyssum was the flower most frequently phidae have been widely reported (Jervis et al. 1993; visited by syrphid adults, enhancing adult body size Al-Doghairi and Cranshaw 1999). Predatory hover- and egg-to adult survival of the F1 generation. flies (Diptera: Syrphidae) have a high potential as biocontrol agents against aphids (Tenhumberg and Poehling 1995; Brewer and Elliott 2004; Freier et al. 2007; Haenke et al. 2009). Several studies have shown Handling Editor: Patrick De Clercq. that this family of Diptera responds positively to the R. Amoro´s-Jimeńez (&) Á M. A´ . Marcos-Garcıá addition of flowering plants to the crop, which can Associated Unit IPAB CSIC-UA, CIBIO (University of increase their residence time and their efficiency as Alicante), San Vicente del Raspeig, Alicante, Spain biocontrol agents, resulting in a lower aphid density e-mail: [email protected] and crop damage (Hickman and Wratten 1996; Pineda A. Pineda and Marcos-Garcıá 2008b; Haenke et al. 2009). Laboratory of Entomology, Wageningen University, Floral resources may have a significant effect on Wageningen, The Netherlands egg production of females and other fitness-related parameters of syrphids (Scholz and Poehling 2000), A. Fereres Associated Unit IPAB CSIC-UA, Instituto de Ciencias since adults rely on proteins from pollen and saccha- Agrarias (ICA-CSIC), Madrid, Spain rides from nectar to mature their ovaries and sustain 123 428 R. Amoro´s-Jimeńez et al. egg production and to obtain energy, respectively climatic conditions occurring in these agricultural (Chambers 1988; Gilbert 1993). Therefore, under- areas (Amoro´s-Jimeńez et al. 2012), and it has standing the effect that different species of flowers previously shown a positive response to habitat have on syrphids is crucial when applying habitat management strategies including the provision of management strategies for aphid control (Macleod additional floral resources (Pineda and Marcos-Garcıá 1992; Cowgill et al. 1993). When evaluating floral 2008c) and banker plants (Pineda and Marcos-Garcia resources for habitat management in outdoor crops, 2008). traits that enhance attractiveness are desired. How- ever, when introducing flowering plants in green- houses, enhancing the performance and fitness of Materials and methods natural enemies can be as desirable as improving their attraction. Surprisingly, very little work has paid Plant material, aphids and syrphids attention to the effects of flowering plants on syrphid performance (Laubertie et al. 2012; Pinheiro et al. Sweet pepper (cv. California Wonder), sweet alyssum 2013), and even fewer studies have been performed on and coriander plants were grown from seed in plastic the link between performance and syrphid foraging pots (5 9 5 9 6 cm) in a glasshouse under controlled behaviour (Laubertie et al. 2012). Due to this fact, conditions and natural light (25 ± 2 °C, 60 ± 10 % criteria for selecting flower resources to enhance RH, 12L:12D photoperiod). Flowering plants were syrphid populations have been based mainly on the sown weekly to assure there were fresh flowers floral preferences of syrphid adults. In addition, these throughout the experiment. Due to the fact that time preferences may differ between syrphid species (Has- to flowering varies among species, time of sowing was lett 1989), highlighting that for the success of habitat different for each flower species in order to synchro- management implementation it is crucial to under- nise their flowering. A stock colony of Myzus persicae stand the effects of floral resources for the targeted (Sulzer) (Hemiptera: Aphididae) was maintained on natural enemy. sweet pepper plants in mesh netting cages (30 9 30 9 The hypotheses of the present study are that 60 cm) in a climate room under controlled conditions syrphids use their floral resources selectively (1), (25 ± 1 °C, 60 ± 10 % RH, 14L:10D photoperiod). feeding on different flowers has a differential effect on S. rueppellii cohorts were reared in plastic cages (30 9 performance of these insects (2) and there is a relation 30 9 60 cm), with a fine mesh on their top under the between the attractiveness of these floral foods and same environmental conditions. The rearing cages their effect on performance of hoverfly adults but also contained bee pollen from various flowers, sucrose, on that of their offspring (3). To address these water, and a sweet pepper plant infested with M. questions, we compared two of the most commonly persicae to stimulate oviposition. Same-aged syrphid used species of flowers that have been successfully eggs were periodically removed from the adult applied in habitat management strategies to enhance cultures and the emerged larvae were reared until the populations of natural enemies: sweet alyssum pupation on sweet pepper plants infested with M. [Lobularia maritima (L.) Desv. (Brassicaceae)] and persicae. coriander [Coriandrum sativum L. (Umbelliferae)]. Furthermore, we included sweet pepper [Capsicum Syrphid floral preference annuum L. (Solanaceae)] as an additional non-host resource, to evaluate the importance that its flowers, Relative attractiveness of the three flowering species regularly exploited by syrphids that visit this horticul- was evaluated in a multiple-choice experiment. The tural crop (Pineda and Marcos-Garcıá 2008d), may arena consisted on an insect-proof cage (40 9 40 9 have on conservation biological control. The syrphid 50 cm) located inside a rearing chamber under the species we chose to conduct this work was Sphaero- same conditions as explained above. One flowering phoria rueppellii (Wiedemann) (Diptera: Syrphidae) plant of each of the three species was placed in one of the most abundant predatory hoverfly in Mediterra- the corners of the cage. The relative position of each nean greenhouse crops (Pineda and Marcos-Garcıá plant was randomised for every replicate to account 2008c). This species is well adapted to the extreme for possible differences in light intensity caused by the 123 Feeding preferences of the aphidophagous hoverfly 429 structure of the chamber. A 2–4 day old adult syrphid Adult lifespan, time to sexual maturation (e.g. was placed in the centre of the cage, inside a glass tube number of days until the first egg is laid), total covered with black adhesive tape to help orientate the fecundity and fertility were measured as components syrphid towards the tube opening. Each fly was used of syrphid performance. only once and had never experienced the test conditions before. Using the behavioural observation Performance of the F1 generation programme Etholog (Ottoni 2000), the time devoted to feeding on each flower species and the frequency of To evaluate a possible effect of adult feeding habits on visits to each flower were recorded. Observations the performance of their offspring, three different lasted for 10 min. Adults that did not exhibit any rearing cages were prepared, one for each flowering recognition behaviour (i.e. the syrphid performs a plant species. Each cage contained approximately 100 suspended flight near the plant or lands on it) during mature adults, water and two to four plants of one of this time were discarded. Twenty replicates were the tested flower species (alyssum, coriander or sweet performed releasing females and 20 replicates were pepper), which were periodically replaced by fresh done with males. Tests were always conducted from 9 ones. An aphid-infested sweet pepper plant was placed to 11 a.m. in each cage for two hours in order to obtain eggs of the same age. After this time, aphid-infested plants Performance of the parental generation carrying eggs were removed from the cages. Syrphid eggs were reared under optimal conditions (see ‘‘Plant To assess the effect of feeding on different flower material, aphids and syrphids’’), and checked daily for resources on the performance of S. rueppellii, one larval emergence. From each flowering plant cage, a newly-emerged female and two males were placed in a total of 50 newly-born syrphid larvae were isolated plastic cage (30 9 30 9 60 cm), with a fine mesh on its (i.e. 50 replicates) in a Petri dish (90 9 15 mm) with a top and under the same conditions as for the insect piece of a sweet pepper leaf (1 cm2) and a wet disk of cultures. Each cage contained a non-flowering sweet paper to provide moisture, and sealed with ParafilmÒ. pepper plant infested with approximately 300 individ- Ad libitum food (M.

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