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Pyrrolizidine Alkaloids Negatively Affect a Generalist Herbivore Feeding on the Chemically Protected Legume Crotalaria Pallida

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Pyrrolizidine Alkaloids Negatively Affect a Generalist Herbivore Feeding on the Chemically Protected Legume Crotalaria Pallida Pyrrolizidine Alkaloids Negatively Affect a Generalist Herbivore Feeding on the Chemically Protected Legume Crotalaria pallida R Cogni & J R Trigo Neotropical Entomology ISSN 1519-566X Volume 45 Number 3 Neotrop Entomol (2016) 45:252-257 DOI 10.1007/s13744-016-0361-6 1 23 Your article is protected by copyright and all rights are held exclusively by Sociedade Entomológica do Brasil. This e-offprint is for personal use only and shall not be self- archived in electronic repositories. If you wish to self-archive your article, please use the accepted manuscript version for posting on your own website. You may further deposit the accepted manuscript version in any repository, provided it is only made publicly available 12 months after official publication or later and provided acknowledgement is given to the original source of publication and a link is inserted to the published article on Springer's website. The link must be accompanied by the following text: "The final publication is available at link.springer.com”. 1 23 Author's personal copy Neotrop Entomol (2016) 45:252–257 DOI 10.1007/s13744-016-0361-6 ECOLOGY, BEHAVIOR AND BIONOMICS Pyrrolizidine Alkaloids Negatively Affect a Generalist Herbivore Feeding on the Chemically Protected Legume Crotalaria pallida 1 2 RCOGNI ,JRTRIGO 1Departamento de Ecologia, Instituto de Biociências, Univ de São Paulo, São Paulo, Brasil 2Depto de Biologia Animal, Instituto de Biologia, Univ Estadual de Campinas, Campinas, SP, Brasil Keywords Abstract Chemical defense, herbivory, sequester, Plant secondary metabolites can have opposing effects on adapted specialization specialist and non-adapted, generalist herbivores. In this study, we Correspondence used Heliothis virescens (Fabricius) (Lepidoptera: Noctuidae) as a R Cogni, Departamento de Ecologia, generalist, non-adapted model herbivore to test the possible effects Instituto de Biociências, Univ de São Paulo, São Paulo, Brasil; [email protected] of Crotalaria pallida (Fabaceae: Papilionoideae) defenses on herbi- vore performance. Neonate H. virescens larvae were able to con- Edited by Raúl A Laumann – Embrapa sume C. pallida leaves and fruits and grow for a few instars, but Received 25 February 2015 and accepted 3 none of them survived to pupation. We added isolated pyrrolizidine January 2016 alkaloids (PAs) to an artificial diet at different concentrations, and Published online: 29 January 2016 PA concentration significantly affected the number of larvae that achieved pupation. Larval survival was not reduced at a PA concen- * Sociedade Entomológica do Brasil 2016 tration similar to the concentration on green seeds of C. pallida,but it was significantly reduced at PA concentration 5 and 100 times higher. These results suggest that PAs in isolation are not the de- fense responsible for the mortality in fresh C. pallida plants, indicat- ing the importance of other possible defenses. The negative effect of PAs on fitness of the non-adapted, generalist herbivore is in agreement with few previous studies, but it is in clear contrast to a previous study on the effects of PAs on the adapted specialist herbivore Utetheisa ornatrix (L.) that were able to sequester PAs with no fitness costs. Introduction of mates (Bowers 1992, Nishida 2002, Macel 2011, Trigo 2011). For example, the moth Utetheisa ornatrix (L.) Secondary metabolites are one of the most pervasive de- (Lepidoptera: Erebidae) is able to sequester specific defen- fense mechanisms against herbivores in plants sive chemicals, pyrrolizidine alkaloids (PAs), from its host (Schoonhoven et al 2005). Many studies have shown the plant and use it for defense and as a male mating phero- negative effects of these substances on survival and fecun- mone (Eisner & Meinwald 1995). In a series of experiments dity of herbivores (Awmack & Leather 2002). However, in which PAs were added to an artificial diet at different herbivorous insects have evolved mechanisms to tolerate concentrations, fitness components of this moth were af- specific plant defense chemicals. Moreover, in some cases, fected only slightly or not at all by PAs, suggesting that plant defenses can be used as a cue by specialist herbivores sequestration in this species does not incur in fitness cost to find their host plants or be used as phagostimulants (Cogni et al 2012). In addition, larvae showed preference (Bernays & Chapman 1994). Many specialist herbivorous for feeding on diets with higher concentrations of PAs in insects can also sequester these defensive chemicals and choice experiments (Hoina et al 2012). These results indi- use them as protection against predators or for attraction cate that for some specific plant defenses, specialist Author's personal copy Pyrrolizidine Alkaloids Impaired a Generalist Herbivore 253 herbivores can be positively affected by sequestration with- Material and Methods out any negative effect or fitness costs. On the other hand, these plant defensive chemicals Larval performance on fresh plants may have a negative effect on non-adapted, generalist herbivores; for example, the generalist arctiines Heliothis virescens were purchased from Bio-Serv Estigmene acrea (Drury) and Grammia geneura (Frenchtown, NJ). Crotalaria pallida seeds were collect- (Strecker) are adapted to PAs, sequestering them ed from two populations: Campinas, state of São (Harmtann et al 2004); however, PAs have deterrent Paulo, Southeastern Brazil, and Archbold Biological and toxic effects on a variety of non-adapted, general- Station in Central Florida, USA (Cogni & Futuyma istinsectherbivores(vanDamet al 1995,Macelet al 2009). The composition of PAs of plants from these 2005, Narberhaus et al 2005). These findings suggest two populations was quantitatively and qualitatively that adapted specialist herbivores can act as agents of similar (Cogni et al 2011). The quantitative analysis natural selection that lower the levels of defensive was performed by colorimetric method and the quali- chemicals in host plant populations, while non- tative analysis by GC/MS (Trigo et al 1993, 2003, Cogni adapted generalists may increase these levels (van der et al 2011). We grew plants from seeds in the green- Meijden 1996). For example, introduced populations of house at the Life Science Building at Stony Brook Senecio jacobaea (Asteraceae) that lacked a specialist University in Stony Brook, NY, under natural sunlight. herbivore evolved increased levels of PAs and, conse- Plantswerewatereddailyandfertilizedeveryother quently, increased resistance to generalist herbivores week as in Cogni et al (2011). We fed larvae on fresh (Joshi & Vrieling 2005). Similarly, generalist damage leaves for the first 4 days; afterthat,larvaewerefed was negatively correlated to glucosinolate sinigrin con- with unripe seeds. This was done to simulate the wild centrations in Brassica nigra (Brassicaceae), but special- condition for the most common herbivore of Crotalaria ist damage was positively correlated (Lankau 2007). plants, U. ornatrix.NeonatesofU. ornatrix first con- The increase in sinigrin concentration was favored sume leaf material for some days before getting inside when specialists were removed, disfavored when gen- the pod to prey on unripe seeds (Ferro et al 2006, eralists were removed, and neutral when both gener- Eisner 2003). We put neonate larvae individually in alists and specialists were present (Lankau 2007). 1.5-mL microcentrifuge tubes with a leaf disc for In this study, we tested the effects of Crotalaria 48 h. Leaf discs were made from fresh leaves and pallida (Fabaceae: Papilionoideae) defenses on the gener- were 1 cm in diameter. After 4 days of feeding on alist, non-specialized model herbivore Heliothis virescens leaves,larvaeweretransferred to individual petri (Fabricius) (Lepidoptera: Noctuidae). We used this herbi- dishes (5-cm diameter) with a moistened filter paper vore as a model generalist to contrast with our previous and green pods. Pods were opened with a razor blade results on the specialist U. ornatrix (Cogni & Futuyma to completely expose seeds to larvae. Every other day, 2009,Cogniet al 2012, Hoina et al 2012,Franco& larvae were transferred to a clean dish and new pods Cogni 2013). Heliothis virescens is an economically impor- were provided. The amount of pod given to each larva tant polyphagous pest that can develop in more than 100 was 1/3 pod on days 5 and 7, 1/2 on day 9, 1 on days plant species belonging to more than 36 families (Blanco 11 and 13, and 2 (every other day) after day 13. We et al 2008, Karpinski et al 2014). This species was chosen checked for larval survivorship on alternate days. All as a model because it can feed on many plant species experiments were carried out in an incubator at 29°C and can consume leaves and fruits. Crotalaria pallida is and 12:12 photoperiod. We used 117 individual neonate an annual plant with current pantropical distribution that larvae for the Brazilian plants and 98 for the plants obscures its native origin (Polhill 1982). The constitutive from USA. presence of pyrrolizidine alkaloids is considered the major In addition to the main experiment with H. virescens resistance trait in Crotalaria (Wink & Mohamed 2003, eating on C. pallida plants, we carried out two controls Hartmann 1999,Trigo2011). Here we tested if a model concurrently. First, as a control for the ability of our generalist herbivore is able to consume and survive on H. viscerens stocktogrowonfreshplantmaterialin the chemically protected C. pallida, and how the main the laboratory, we used green beans, a non-toxic
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