An Endophyte-Rich Diet Increases Ant Predation on a Specialist Herbivorous Insect

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An Endophyte-Rich Diet Increases Ant Predation on a Specialist Herbivorous Insect Ecological Entomology (2015), DOI: 10.1111/een.12186 SHORT COMMUNICATION An endophyte-rich diet increases ant predation on a specialist herbivorous insect , , TOBIN J. HAMMER1 2 andSUNSHINE A. VANBAEL2 3 1Department of Ecology and Evolutionary Biology, Cooperative Institute for Research in Environmental Sciences, University of Colorado at Boulder, Boulder, Colorado, U.S.A., 2Smithsonian Tropical Research Institute, Apartado, Republic of Panama and 3Department of Ecology and Evolutionary Biology, Tulane University, New Orleans, Louisiana, U.S.A. Abstract. 1. All plants form symbioses with microfungi, known as endophytes, which live within plant tissues. Numerous studies have documented endophyte–herbivore antagonism in grass systems, but plant–endophyte–insect interactions are highly variable for forbs and woody plants. 2. The net effect of endophytes on insect herbivory may be modified by their interactions with higher trophic levels, such as predators. Including these multitrophic dynamics may explain some of the variability among endophyte studies of non-grass plants, which are currently based exclusively on bitrophic studies. 3. The abundance of natural foliar endophytes in a Neotropical vine was manipulated and beetles were fed high or low endophyte diets. Experimental assays assessed whether dietary endophyte load affected beetle growth, leaf consumption, and susceptibility to ant predation. 4. Beetles feeding on high- versus low-endophyte plants had almost identical growth and leaf consumption rates. 5. In a field bioassay, however, it was discovered that feeding on an endophyte-rich diet increased a beetle’s odds of capture by predatory ants nine-fold. 6. Endophytes could thus provide an indirect, enemy-mediated form of plant defence that operates even against specialist herbivores. We argue that a multitrophic approach is necessary to untangle the potentially diverse types of endophyte defence among plants. Key words. Acromis sparsa, Azteca lacrymosa, endophytic fungi, insect herbivory, Merremia umbellata, multitrophic interactions. Introduction Gange, 2009). While several studies have addressed the poten- tial multitrophic effects of mycorrhizal fungi (e.g. Gange et al., The aboveground tissues of all plants are infected by 2003; Laird & Addicott, 2009; Schausberger et al., 2012; Moon non-pathogenic, microscopic fungi known as endophytes et al., 2013), foliar endophytes may present different ecological (sensu Wilson, 1995). Similar to mycorrhizal fungi, foliar dynamics because of their potential to interact directly with endophytes can improve plant nutrient acquisition, confer aboveground herbivores and their natural enemies. protection from abiotic stress (Rodriguez et al., 2009), and can A number of studies have demonstrated that some grasses also mediate their hosts’ interactions with insect herbivores engage in defensive mutualisms with vertically transmitted (Hartley & Gange, 2009). Plant–endophyte–insect interactions endophytes that directly protect their hosts from insect attack could be further modulated by feedbacks with higher trophic by producing toxic secondary metabolites (Schardl et al., 2004; levels, but the impacts of foliar endophytes on the predators Müller & Krauss, 2005), but these mutualisms may be weak- and parasitoids of their host plant’s herbivores have not yet ened by negative effects on the herbivores’ natural enemies. been investigated outside of a few model grasses (Hartley & For example, grass endophyte-produced toxins retained by Correspondence: Sunshine A. Van Bael, Tulane University, 6823 St. the herbivore can limit the performance of its predators (de Charles Avenue, Boggs Suite 400, New Orleans, LA 70118, U.S.A. Sassi et al., 2006), pathogens (Richmond et al., 2004), and E-mail: [email protected] parasitoids (Bultman et al., 1997; Härri et al., 2008). For forbs © 2015 The Royal Entomological Society 1 2 Tobin J. Hammer and Sunshine A. Van Bael and woody plants, however, the effects of endophytes and nat- by the faecal shield. We hypothesised that high endophyte con- ural enemies on insect herbivory have only been investigated in sumption would lower ant predation on larvae when faecal isolation. In these systems, where endophytes are horizontally shields were present. Irrespective of the role of faecal shields, transmitted from spore fall in the environment (Herre et al., if endophytes do not directly limit beetle herbivory, but release 2007), direct endophyte effects on insect herbivory are highly beetles from top-down control by ant predators, the net outcome variable across studies, and it has been questioned whether the of endophyte infection could be to increase herbivory on host defensive mutualism paradigm is generalisable beyond grasses plants – a finding that would further call into question the role (Saikkonen et al., 2010). Natural enemies are known to be of endophytes as defensive mutualists of forbs and woody plants. critical in constraining insect herbivore populations (Strong et al., 1984; Cornell et al., 1998), but whether they interact with endophytes to synergistically regulate herbivory on non-grass Materials and methods plants has, to our knowledge, not been addressed. Our study was conducted at the Smithsonian Tropical Research Endophytes and enemies could interact in a variety of ways, Institute in Gamboa, Panama, during the summers of 2011 and resulting in a diversity of feedbacks on the intensity of herbi- 2012. We established potted M. umbellata plants in a greenhouse vore pressure on plants. Endophytes are most likely to influ- by taking cuttings of wild vines growing locally; each cutting ence enemies indirectly through their effects on plants and/or was separated into equal numbers of individually potted cuttings herbivores. For example, an herbivore’s body size, devel- or clones. All plants were kept in plastic tents in the greenhouse opmental rate, nutritional composition, or behaviour, which to reduce endophyte inoculum landing on the plants. We waited have been long recognised to modulate predation (Price et al., until our greenhouse plants flushed all new leaves in this envi- 1980), may also be affected by endophyte-produced toxins or ronment, to avoid using leaves that had been exposed in the field. through endophyte alteration of leaf metabolism and physical We assigned low- and high-endophyte treatments (hereafter, properties (Clay et al., 1985; Petrini et al., 1992; Mejía et al., ‘Elow’and‘Ehigh’, respectively) to equal numbers of each clone, 2014). Endophyte-infected plants can have different volatile to ensure an equal representation of genotypes in each treatment profiles from endophyte-free plants (Yue et al., 2001; Jallow group. Foliar endophyte abundance in leaves was manipulated et al., 2008); endophytes have also been shown to mediate according to established protocols (Bittleston et al., 2010). herbivore-induced plant volatile emission (Li et al., 2014), Briefly, we exposed Ehigh plants to naturally occurring commu- which in turn may influence enemy attraction (Takabayashi & nities of airborne fungi at night, while maintaining all plants in Dicke, 1996). Furthermore, retention of fungi or sequestration plastic tents in the greenhouse during the day to limit colonisa- of fungal toxins in or on the herbivore’s body could deter enemy tion and keep the light environment constant. Elow plants were attack. Unless these interactions are considered, it will not be maintained continually inside the plastic tents. All protocols known whether the net endophyte effect on plant defence is rein- were identical between 2011 and 2012 except that, in 2012, the forced or reversed by natural enemies. Studies including such plants were grown in indoor growth chambers during the day, information may help resolve the currently uncertain standing rather than a greenhouse. To verify the success of endophyte of foliar endophytes as defensive mutualists of non-grass plants. treatment, we plated 16 surface-sterilised 2 mm2 leaf fragments As a first step in characterising the sign and intensity of from Elow (n = 45) and Ehigh (n = 27) plants on 2% malt extract links between horizontally transmitted foliar endophytes, plants, agar (see Van Bael et al., 2009 for details). The proportion of herbivores, and their enemies, we experimentally manipulated leaf fragments giving rise to fungal colonies after 7 days was endophyte abundance in foliage of the tropical vine Merremia used as a measure of foliar endophyte abundance for each plant. umbellata L. (Convolvulaceae) and measured herbivore perfor- In 2011, 28 wild A. sparsa egg masses (containing c. 20–40 mance, feeding rates, and defence against an ant predator. We eggs) were collected from M. umbellata plants in the Gamboa first fed high- and low-endophyte leaves to the herbivorous bee- area, and separated from their mothers. As soon as the lar- tle Acromis sparsa Boheman (Chrysomelidae: Cassidinae), an vae hatched, broods were divided in half and immediately fed obligate specialist and important herbivore on M. umbellata either Elow or Ehigh cut leaves in plastic containers. We mea- (Windsor, 1987), and measured beetle growth and feeding rates. sured the total mass and number of individuals in each of the We hypothesised that, in the absence of enemies, endophyte 56 half-brood groups (containing 14 individuals, on average) treatment would affect neither herbivore performance nor leaf on days 4 and 9 of larval development and during the pupal consumption, as these monophagous beetles may be adapted to stage.
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