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

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.

[1]  M. Pizo,et al.  Size and lipid content of nonmyrmecochorous diaspores: effects on the interaction with litter-foraging ants in the Atlantic rain forest of Brazil , 2001, Plant Ecology.

[2]  M. Westoby,et al.  Convergence of elaiosomes and insect prey: evidence from ant foraging behaviour and fatty acid composition , 1994 .

[3]  B. Hölldobler,et al.  A trail pheromone component of the ant Mayriella overbecki Viehmeyer (Formicidae: Myrmicinae) , 2000, Naturwissenschaften.

[4]  B. Smith,et al.  Intensity and the ratios of compounds in the scent of snapdragon flowers affect scent discrimination by honeybees (Apis mellifera) , 2005, Journal of Comparative Physiology A.

[5]  O. Pellmyr,et al.  Plant-animal interactions : an evolutionary approach , 2002 .

[6]  A. Bertsch,et al.  Analysis of the Labial Gland Secretions of the Male Bumblebee Bombus griseocollis (Hymenoptera: Apidae) , 2004, Zeitschrift fur Naturforschung. C, Journal of biosciences.

[7]  Susannah Andersson Antennal responses to floral scents in the butterflies Inachis io, Aglais urticae (Nymphalidae), and Gonepteryx rhamni (Pieridae) , 2003, CHEMOECOLOGY.

[8]  D. Davidson Ecological Studies of Neotropical Ant Gardens , 1988 .

[9]  Michael Fenner Seeds: The Ecology of Regeneration in Plant Communities , 1992 .

[10]  W. M. Whitten,et al.  Fragrance Collection, Storage, and Accumulation by Individual Male Orchid Bees , 2004, Journal of Chemical Ecology.

[11]  P. Moore Seeds. The ecology of regeneration in plant communities . Edited by M. Fenner. x + 373 pp. C.A.B International, 1992. ISBN 085198 726 5 £49.50 (US $94.00), H/b , 1992, Seed Science Research.

[12]  I. Valterová,et al.  The first synthesis of geranyllinalool enantiomers , 2002 .

[13]  W. Barthlott,et al.  Ants as epiphyte gardeners: comparing the nutrient quality of ant and termite canopy substrates in a Venezuelan lowland rain forest , 2001, Journal of Tropical Ecology.

[14]  Stacey L. Sheridan,et al.  THE ROLE OF CHEMICAL SENSES IN SEED-CARRYING BEHAVIOR BY ANTS : A BEHAVIORAL, PHYSIOLOGICAL, AND MORPHOLOGICAL STUDY , 1996 .

[15]  D. Levey,et al.  COMPLEX ANT-PLANT INTERACTIONS: RAIN FOREST ANTS AS SECONDARY DISPERSERS AND POST-DISPERSAL SEED PREDATORS' , 1993 .

[16]  Donat Agosti,et al.  Ants : standard methods for measuring and monitoring biodiversity , 2000 .

[17]  J. Clément,et al.  Geranyllinalool (Diterpene Alcohol) , 1990, Journal of Chemical Ecology.

[18]  D. Davidson,et al.  Neotropical ant gardens II. Bioassays of seed compounds , 1990, Journal of Chemical Ecology.

[19]  D. Plepys Odour-mediated nectar foraging in the silver Y moth, Autographa gamma , 2002 .

[20]  J. Orivel,et al.  Selection of epiphyte seeds by ant-garden ants , 1999 .

[21]  E. Morgan,et al.  Trail pheromone of the antTetramorium impurum and model compounds: Structure-activity comparisons , 1990, Journal of Chemical Ecology.

[22]  Wesley Rodrigues Silva,et al.  Seed dispersal and frugivory : ecology, evolution, and conservation , 2002 .

[23]  Wilhelm Barthlott,et al.  Spatial Distribution of Vascular Epiphytes (including Hemiepiphytes) in a Lowland Amazonian Rain Forest (Surumoni Crane Plot) of Southern Venezuela 1 , 2000 .

[24]  C. Christian Consequences of a biological invasion reveal the importance of mutualism for plant communities , 2001, Nature.

[25]  H. Topoff,et al.  Queen Sex Pheromone of the Slave-making Ant, Polyergus breviceps , 2007, Journal of Chemical Ecology.

[26]  W. Roelofs,et al.  Identification of Host Fruit Volatiles from Hawthorn (Crataegus spp.) Attractive to Hawthorn-Origin Rhagoletis pomonella Flies , 2003, Journal of Chemical Ecology.

[27]  R. Menzel,et al.  Optical Imaging of Odor-Evoked Glomerular Activity Patterns in the Antennal Lobes of the Ant Camponotus rufipes , 1999, Naturwissenschaften.

[28]  T. Akino,et al.  Seed cleaning behavior by tropical ants and its anti-fungal effect , 2005, Journal of Ethology.

[29]  E. Wilson The arboreal ant fauna of Peruvian Amazon forests : a first assessment , 1987 .

[30]  N. Vereecken,et al.  Cuticular Hydrocarbons as Sex Pheromone of the Bee Colletes cunicularius and the Key to its Mimicry by the Sexually Deceptive Orchid, Ophrys exaltata , 2005, Journal of Chemical Ecology.

[31]  D. Davidson,et al.  Neotropical ant gardens , 1990, Journal of Chemical Ecology.

[32]  C. Brew,et al.  Seed dispersal by ants: behaviour-releasing compounds in elaiosomes , 1989, Oecologia.

[33]  A. Borg-Karlson,et al.  Structure–Activity Relationships of Benzoic Acid Derivatives as Antifeedants for the Pine Weevil, Hylobius abietis , 2006, Journal of Chemical Ecology.