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Alkaloid Concentration of the Invasive Plant Species Ulex Europaeus in Relation to Geographic Origin and Herbivory

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Alkaloid Concentration of the Invasive Plant Species Ulex Europaeus in Relation to Geographic Origin and Herbivory Naturwissenschaften (2012) 99:883–892 DOI 10.1007/s00114-012-0970-9 ORIGINAL PAPER Alkaloid concentration of the invasive plant species Ulex europaeus in relation to geographic origin and herbivory Benjamin Hornoy & Anne Atlan & Michèle Tarayre & Sébastien Dugravot & Michael Wink Received: 3 July 2012 /Revised: 10 September 2012 /Accepted: 13 September 2012 /Published online: 25 September 2012 # Springer-Verlag Berlin Heidelberg 2012 Abstract In the study of plant defense evolution, invasive genistae-tinctoriae were negatively correlated to concentration plant species can be very insightful because they are often of the QA lupanine. Quinolizidine alkaloid concentration was introduced without their enemies, and traits linked to defense very variable between individuals, both within and among can be released from selective pressures and evolve. Further, populations, but it was not different between native and invaded studying plant defense evolution in invasive species is impor- regions, suggesting that no evolution of decreased resistance tant for biological control and use of these species. In this study, occurred after gorse lost its enemies. Our study also suggests we investigated the evolution of the defensive chemicals qui- that QA concentrations are traits integrated into seed predation nolizidine alkaloids (QAs) in the invasive species gorse, Ulex avoidance strategies of gorse, with plants that mass-fruit in europaeus. Using a common garden experiment, our goals were spring but do not escape pod infestation in time being richer to characterize the role of QAs relative to specialist enemies of in QAs. gorse and to investigate if QA concentration evolved in invaded regions, where gorse was introduced without these enemies. Keywords Biological invasions . Defense syndrome . Our results showed that pod infestation rate by the seed predator Gorse . Plant–insect interaction . Quinolizidine alkaloids Exapion ulicis and infestation by the rust pathogen Uromyces Communicated by: Sven Thatje Introduction Electronic supplementary material The online version of this article (doi:10.1007/s00114-012-0970-9) contains supplementary material, Plants have developed a large diversity of defense mechanisms which is available to authorized users. to cope with herbivores. Among these mechanisms, defensive B. Hornoy (*) : A. Atlan : M. Tarayre chemicals such as secondary metabolites are widespread and ECOBIO, Université de Rennes 1, can confer resistance to a wide spectrum of enemies, from Campus de Beaulieu, microorganisms to vertebrates. For example, alkaloids have 35042 Rennes Cedex, France been shown to be feeding deterrent and/or toxic to bacteria, e-mail: [email protected] fungi, plants, insects, nematodes, mollusks, and vertebrates S. Dugravot (Wink 1998). Many other traits may also be involved in resis- BIO3P, Université de Rennes 1, tance, such as physical defenses (e.g., thorns), escape in time Campus de Beaulieu, (e.g., fruiting phenology), and indirect defenses (e.g., volatiles 35042 Rennes Cedex, France attracting natural enemies of herbivores; Wink 1988; Agrawal M. Wink and Fishbein 2006). Plant defense strategies are thus better Institut für Pharmazie und Molekulare Biotechnologie, viewed as a suite of traits that act together against herbivory Universität Heidelberg, (i.e., a defense syndrome), rather than single traits (Agrawal and Im Neuenheimer Feld 364, 69120 Heidelberg, Germany Fishbein 2006; Carmona et al. 2011). The expression and evolution of these defensive traits are driven by environmental Present Address: factors such as resource availability and the composition of the B. Hornoy herbivore community. In particular, the reciprocal selection Institut de Biologie Intégrative et des Systèmes, Université Laval, 1030 Avenue de la Médecine, pressure between a plant species and an associated herbivore Québec, QC, Canada can lead to coevolution (Janzen 1980;Thompson2005), 884 Naturwissenschaften (2012) 99:883–892 especially when their relationship is very specific and the impact other reduce seed predation by a mass flowering resulting in of the two species on each other is strong (Gandon 2002). For predator satiation (Tarayre et al. 2007; Atlan et al. 2010). example, Berenbaum and Zangerl (1998) found a very close However, these flowering strategies do not explain all the match between populations of wild parsnip (Pastinaca sativa, variation observed in pod infestation rates (Atlan et al. Apiaceae) to produce defense compounds and the ability of the 2010). Other defenses must therefore be involved, and they parsnip webworm Depressaria pastinacella (Oecophoridae) to likely include quinolizidine alkaloids (QAs), which are char- metabolize them. The absence or loss of herbivores can thus acteristic of some tribes of the Fabaceae (Wink 1993; Wink et greatly affect the evolution of plant traits that are part of a al. 2010). Indeed, these compounds are known to have a defense strategy (e.g., Janzen 1975; Benkman 1995). defensive role against a wide array of herbivores, including An evolutionary decrease of costly defense traits is expected pathogens and phytophagous insects (reviewed in Wink 1992, in the absence of herbivores and pathogens (Blossey and 1998). In addition, QAs are produced in green parts of the Nötzold 1995; Müller-Schärer et al. 2004; Orians and Ward plant, are transported through the phloem, and accumulate in 2010). This situation is often observed in invasive plants be- epidermal cells and in fruits, thus being strategically posi- cause most of them have been introduced without their herbi- tioned to act against herbivores, among which phloem sap vores and pathogens, experiencing the so-called enemy release feeders, pathogens, and seed predators (Wink 1992;Winkand (Keane and Crawley 2002; Mitchell and Power 2003;Liuand Roberts 1998). Outside its native range, U. europaeus was Stiling 2006). The evolution of chemical defenses in invasive introduced without its herbivores and pathogens and is not plants depends on their cost and on the relative abundance of attacked by any local herbivore. Seed predators and other specialist and generalist enemies in the introduced range com- specialist herbivores from the native range were introduced pared to the native range (Müller-Schärer et al. 2004;Orians later for biological control in some invaded regions, such as in and Ward 2010). As a consequence, a decrease of defense traits New Zealand, where U. europaeus was present before 1835 has been observed in some but not all invasive species and where E. ulicis was introduced in 1931 and C. succedana (reviewed in Bossdorf et al. 2005, and Orians and Ward 2010). in 1992 (Hill and Gourlay 2002). In other regions (e.g., In this context, the evolution of plant defensive chemistry in Reunion Island), there is no biological control program, and invasive species is not only an important topic in the study of gorse plants are still free from their specialist enemies. evolution of defense and plant–herbivore interactions but also The main goal of the study was to investigate if QA concen- for biological control (Müller-Schärer et al. 2004)oruseof tration in gorse evolved after enemy release in invaded regions. these species (e.g., as fodder). Common gorse, Ulex europaeus To address this issue, we first described the pattern and variation (Fabaceae), is a long-lived spiny shrub that can reach more than of QAs in gorse and their ecological relevance relative to its 4 m height. It is native to Western Europe but has been intro- natural enemies. Specifically, the following questions were duced by Europeans, mainly since the beginning of the studied: (1) do gorse individuals richer in QAs show lower nineteenth century, in several regions of the world where it attack rates by their main natural enemies? (2) Does QA con- often became invasive, including New Zealand, Australia, centration differ between native and invaded regions? To an- South and North America, and the islands of Hawaii and swer these questions, we used a common garden experiment Reunion (Holm et al. 1997). In Europe, gorse is attacked by with individuals from native and introduced gorse populations several pathogens and herbivores. However, adult gorse plants and measured the QA concentration in their shoots, their life are protected from large grazers by their thorns and are only history traits, and the level of infestation by herbivores. attacked by small specialists, of which the most common and harmful are the specific weevil Exapion ulicis (Coleoptera: Apionidae) and to a lesser extent the moth Cydia succedana Materials and methods (Lepidoptera: Tortricidae; Barat et al. 2007, 2008). Exapion ulicis spends its whole life cycle on gorse, feeding on gorse Experimental design shoots and flowers. Females lay their eggs inside young pods in spring, and larvae develop at the expense of seeds (Davies Studied gorse plants come from two native regions, Brittany 1928; Barat et al. 2007). Females of C. succedana lay eggs (France) and Scotland (UK), and from two invaded regions, outside the pods and the emerging larvae chew the pod wall to Reunion Island (Indian Ocean) and New Zealand (Pacific enter the pods and develop at the expense of the seed. Several Ocean). Population genetic analyses showed that gorse from other enemies attacking the vegetative parts of gorse were also these two invaded regions likely came from the northern described (e.g., aphids, spider mites, and fungi; Zwölfer 1962). part of Western Europe (France and UK; Hornoy 2011). In its native range, gorse
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