Only Attract Ants? The Versatility of Petiolar Extrafloral Nectaries in <i>Passiflora</i>

Abstract

Passiflora species presents a coevolutive relationship with Heliconiini butterflies, their primary herbivores. The Heliconiini caterpillars are able to detoxify toxic compounds produced by Passiflora, thus morphological defense strategies stand out over chemical innovations. In this framework, we highlight the presence of mimetic structures and extrafloral nectaries (EFN) as morphological strategies. Heliconian butterflies oviposit only on leaves that do not possess previous eggs, so the presence of egg mimics could prevent the oviposition. EFN are glands that offer nectar to territorial and aggressive ants, establishing mutualistic relationships. Here, we present a structural and chemical analysis of petiolar EFN and nectar from Passiflora alata and P. edulis in order to have insights about the implications of these features in deterring heliconian caterpillars. P. alata have one to four stipitate-crateriform EFN while P. edulis possess a pair of convex glands. Butterflies lay their eggs isolatedly or in up to three on leaves of both species. Our morphological results suggest that EFN from P. alata may act as egg mimics. Ontogenetic data suggest that the variation in the number of glands observed in this species is a serial homology, wherein the selection pressure for this variation is possibly the oviposition pattern. P. alata retain alkaloids, flavonoids and terpenoids inside nectariferous cells; sugars and flavonoids are found in the nectar of both species, while alkaloids are also detected in P. edulis. There is a selective retention/release of secondary metabolites from the EFN tissues to nectar. Knowing that these compounds can be dissuasive to some herbivores and inoffensive to others, we plotted this relationship in a consumer growth versus secondary metabolite concentration diagram. Our results suggest a more active role in the modulation of the gland defense from plants besides the establishment of a mutualistic relationship with ants, an important response in a coevolutive scenario.

A light in the shadow: the use of Lucifer Yellow technique to demonstrate nectar reabsorption

“…Since nectar of Passiflora edulis possesses glucose, fructose and sucrose [19], we associate the non-occurrence of reabsorption in EFN of Passiflora to the presence of a relative thick cuticle and cuticular flanges. The abundance of wax can vary widely and is an important factor for permeability: a cuticle rich in wax favors the passage of fat soluble substances but is a significant barrier for water soluble compounds [24].…”

“…These glands exude profuse nectar available during daytime (Figure 3F). The nectar of P. edulis is composed by sucrose, glucose and fructose [19]. Some relevant anatomical details are pertinent [19]: the multiple epidermis is covered by a cuticle and cuticular flanges extend up to the inner periclinal wall of the first cell layer.…”

“…The nectar of P. edulis is composed by sucrose, glucose and fructose [19]. Some relevant anatomical details are pertinent [19]: the multiple epidermis is covered by a cuticle and cuticular flanges extend up to the inner periclinal wall of the first cell layer. The nectar rising out of the epidermis promotes the cuticle detachment, although cuticle disruption is observed only when ants have access to the EFN.…”

“…For that, we performed tests with LYCH dye, adapting its already known use in studies of nectar secretion and nectary structure [11,12], on the floral nectaries of Cucurbita pepo L. (Cucurbitaceae), a species recognized by its ability for nectar reabsorption [2,16,17], and extrafloral nectaries of Passiflora edulis Sims (Passifloraceae), where structural characteristics indicates that nectar reabsorption does not occur [18,19]. …”

New perspectives in nectar evolution and ecology: simple alimentary reward or a complex multiorganism interaction?

“…There has been almost no research into this class of substances in extra-floral nectar. Cardoso-Gustavson et al [47] recently reported trace amounts of alkaloids in the extrafloral nectar of Passiflora. The amounts of alkaloids were not sufficient to induce deleterious effects on ant metabolism and growth and may therefore have functions other than deterrence.…”