Seed odor mediates an obligate ant–plant mutualism in Amazonian rainforests

Abstract

Seed dispersal mutualisms are essential for the survival of diverse plant species and communities worldwide. Among invertebrates, only ants have a major role in seed dispersal, and thousands of plant species produce seeds specialized for ant dispersal in ''diffuse'' multispecies interactions. An outstanding but poorly understood ant-seed mutualism occurs in the Amazonian rainforest, where arboreal ants collect seeds of several epiphyte species and cultivate them in nutrient-rich nests, forming abundant and conspicuous hanging gardens known as ant-gardens (AGs). AG ants and plants are dominant members of lowland Amazonian ecosystems, and their interaction is both specific and obligate, but the means by which ants locate, recognize, and accept their mutualist seeds while rejecting other seeds is unknown. Here we address the chemical and behavioral basis of the AG interaction. We show that workers of the AG ant Camponotus femoratus are attracted to odorants emanating from seeds of the AG plant Peperomia macrostachya, and that chemical cues also elicit seed-carrying behavior. We identify five compounds from P. macrostachya seeds that, as a blend, attract C. femoratus workers. This report of attractive odorants from ant-dispersed seeds illustrates the intimacy and complexity of the AG mutualism and begins to illuminate the chemical basis of this important and enigmatic interaction.seed dispersal ͉ ant-garden ͉ myrmecochory ͉ Camponotus femoratus ͉ Peperomia macrostachya S eed dispersal mutualisms play an essential role in community regeneration and species survival (1-3). Myrmecochory, or seed dispersal by ants, occurs in some 3,000 plant species in over 80 families worldwide, and it is generally a diffuse multispecies interaction mediated by seed-borne nutritional rewards called elaiosomes that are rich in proteins and lipids (4). Ants carry these seeds to their nests, consume the elaiosomes, and abandon the seeds with enhanced prospects for survival and germination (4). Behavioral assays and chemical analyses indicate that ant preference for elaiosomes is mediated by characteristic nonvolatile lipids, especially 1,2-diolein, that are more typical of insect prey than of seeds (5, 6). Myrmecochory is best described in temperate mesic forests and fire-dominated ecosystems, where it can be vital to community organization (1, 4).Tropical ant-seed interactions, on the other hand, are poorly understood, despite the fact that ants are the most common animals in tropical moist forests (7,8), where they play important roles in seed dispersal and viability (9-11). In the tropics, ant-dispersed seeds may lack discrete nutritional rewards, or be collected independently of them (11-13). Such seeds are best known from the Neotropical ant-gardens (AGs), an ant-plant mutualism that occurs throughout lowland Amazonia. At least two ant species are obligate gardeners that retrieve seeds of AG epiphytes (but not other seeds), embed them in arboreal carton nests, and depend on the resulting plants for nest integrity (Fig. 1) (11-13). T...

Defining Habitat Use by the Parabiotic Ants Camponotus femoratus (Fabricius, 1804) and Crematogaster levior Longino, 2003

“…This interaction includes nine species of ants (obligate AGs inhabitant) however, AGs with parabiotic association between C. femoratus and C. levior are among the most commonly found in the Amazon (Davidson, 1988;Orivel & Leroy, 2011). In exchange for support and humidity control for the nest and, in some cases, extrafloral nectar (Davidson, 1988;Schmit-Neuerburg & Blüthgen, 2007), the ants offer dispersion and protection to their mutualistic epiphyte (Vantaux et al, 2007;Youngsteadt et al, 2008Youngsteadt et al, , 2009Vicente et al, 2014). Although the complexity of this interaction and these ants occurring throughout the Neotropical region (Souza et al, 2007;Ryder-Wilkie et al, 2010;Emery & Tsutsui, 2013;Vicente et al, 2014Vicente et al, , 2016) the natural history of these species is virtually unknown.…”

Sequestration of prenylated benzoic acid and chromenes by Naupactus bipes (Coleoptera: Curculionidae) feeding on Piper gaudichaudianum (Piperaceae)

“…This is the first report of sequestration of benzoic acid chromenes from plants by a given insect species. Indeed, aromatic compounds such as salicylic acid derivatives were found to mediate mutualism between Peperomia macrostachya and ants Camponotus femoratus (Youngsteadt et al 2008). The possible roles of prenylated benzoic acids derivatives (1 and 2) and chromenes (3 and 4) in mediating a specific relationship between N. bipes and P. gaudichaudianum can be envisaged based on some evidences.…”

The assembly of ant-farmed gardens: mutualism specialization following host broadening

“…That dispersal by ants and rewards for ants (in the form of nectar) are correlated in the oldest domatium-bearing lineage here studied, the Rubiaceae clade Hydnophytinae (figure 4), suggests that food rewards may be a pre-adaptation for AG lineages, as they are more generally for farming mutualisms [1]. Other pre-adaptations for the convergent evolution of AG plants and ants may include chemical compounds in the seeds [25][26][27], making them attractive to ants, and polydomy [22], an ant species' ability to form several interlinked nests, which allows negotiating the lag-time between seed-planting and rewards (domatia or food), essential in any farming mutualism. The recurrent recruitment of new epiphyte lineages into the AGs probably promoted the evolution of domatia, which enhance uptake of ant-derived nutrients [44,64,65].…”