Extrafloral nectar production of the ant-associated plant,Macaranga tanarius,is an induced, indirect, defensive response elicited by jasmonic acid

Abstract

Plant species in at least 66 families produce extrafloral nectar (EFN) on their leaves or shoots and therewith attract predators and parasitoids, such as ants and wasps, which in turn defend them against herbivores. We investigated whether EFN secretion is induced by herbivory and͞or artificial damage, and thus can be regarded as an induced defensive response. In addition, we studied the underlying signaling pathway. EFN secretion by field-grown Macaranga tanarius increased after herbivory, artificial leaf damage, and exogenous jasmonic acid (JA) application. Artificial damage strongly enhanced endogenous JA concentrations. The response in EFN production to artificial damage was much less pronounced in those leaves that were treated with phenidone to inhibit endogenous JA synthesis. Quantitative dose-response relations were found between the increase in nectar production and both the intensity of leaf damage and the amounts of exogenously applied JA. The amount of endogenously produced JA was positively correlated with the intensity of leaf damage. Increased numbers of defending insects and decreased numbers of herbivores were observed on leaves after inducing EFN production by exogenous JA treatment. Over 6 weeks, repeatedly applied JA or artificial damage resulted in a ten-fold reduction in herbivory. These results demonstrate that EFN production represents an alternative mechanism for induced, indirect defensive plant responses that are mediated via the octadecanoid signal transduction cascade. E xtrafloral nectaries are nectar-secreting glands that are not involved in pollination (1). They are known in at least 66 plant families (2). Many studies have shown that extrafloral nectar (EFN) can play an important role in a plant's defense against herbivores (for reviews, see ref. 3 and 4). Given a choice, ants forage preferentially on plants with extrafloral nectaries (5-7), and several ant and wasp species directly defend the nectary-bearing plant parts against other insects (8). Both insect groups reduce numbers of herbivorous insects on plants possessing extrafloral nectaries and thus lessen damage by herbivores (5,6,(8)(9)(10)(11)(12).Several studies have already indicated that EFN secretion or amino acid concentrations in EFN may increase in response to herbivory (10,(13)(14)(15) and that this reaction does not require herbivore-specific elicitors (16,17). However, most of these studies have suffered from methodological problems (discussed in ref. 17). Because of the lack of specific elicitors, it has been discussed whether EFN can actually be considered as an induced defense (18). Moreover, nothing is known about the underlying signaling pathway, and no study has focused on the effects of induced EFN production on nectary-visiting insects and herbivores.In this study, we used saplings of the southeast Asian pioneer tree Macaranga tanarius (L.) Muell. Arg. (Euphorbiaceae) to address the questions of (i) whether EFN production can be induced by natural or artificial damage; (ii) whether the plant hormone jasm...

Within-plant signaling by volatiles leads to induction and priming of an indirect plant defense in nature

“…4], a result consistent with earlier observations on lima bean plants exposed to artificial VOCs (31). It is therefore most likely that at least a part of this defensive effect was due to an EFN-mediated increase in ant numbers (27,29,32). …”

Temporal variation in extrafloral nectar secretion in different ontogenic stages of the fruits ofAlibertia verrucosaS. Moore (Rubiaceae) in a Neotropical savanna

“…Some studies show that in certain cases, the EFN secretion can be induced by jasmonic acid (Heil et al 2001), a phytohormone which often increases during fruit development (Lopez et al 1987;Czapski & Saniewski 1992;Creelman & Mullet 1997). In this context, such studies could support our initial hypothesis in which the EFN secretion can be higher in bigger and riper fruits of A. verrucosa.…”

The Direct and Ecological Costs of an Ant-Plant Symbiosis

“…Numerous studies have found that ant rewards are produced sparingly, which certainly suggests that they are costly to make. For example, Heil et al (2001) and Palmer et al (2008) showed that both domatia and extrafloral nectar production can be induced by herbivory, and plants often produce extrafloral nectar and food bodies on only young, expanding leaves, which are the most vulnerable to folivory (Coley and Barone 1996). However, other previous tests of the costs of ants to plants have been inconclusive (i.e., Rudgers 2004; Rudgers and Strauss 2004;Rutter and Rausher 2004).…”