Functional Ecology 2010 doi: 10.1111/j.1365-2435.2010.01696.x A hitchhiker’s guide to a crowded syconium: how do fig nematodes find the right ride?
Anusha Krishnan, Subhashini Muralidharan, Likhesh Sharma and Renee M. Borges*
Centre for Ecological Sciences, Indian Institute of Science, Bangalore 560 012, India
Summary 1. Organisms with low mobility, living within ephemeral environments, need to find vehicles that can disperse them reliably to new environments. The requirement for specificity in this pas- senger–vehicle relationship is enhanced within a tritrophic interaction when the environment of passenger and vehicle is provided by a third organism. Such relationships pose many interesting questions about specificity within a tritrophic framework. 2. Central to understanding how these tritrophic systems have evolved, is knowing how they function now. Determining the proximal cues and sensory modalities used by passengers to find vehicles and to discriminate between reliable and non-reliable vehicles is, therefore, essential to this investigation. 3. The ancient, co-evolved and highly species-specific nursery pollination mutualism between figs and fig wasps is host to species-specific plant-parasitic nematodes which use fig wasps to tra- vel between figs. Since individual globular fig inflorescences, i.e. syconia, serve as incubators for hundreds of developing pollinating and parasitic wasps, a dispersal-stage nematode within such a chemically complex and physically crowded environment is faced with the dilemma of choos- ing the right vehicle for dispersal into a new fig. Such a system therefore affords excellent oppor- tunities to investigate mechanisms that contribute to the evolution of specificity between the passenger and the vehicle. 4. In this study of fig–wasp–nematode tritrophic interactions in Ficus racemosa within which seven wasp species can breed, we demonstrate using two-choice as well as cafeteria assays that plant- parasitic nematodes (Schistonchus racemosa) do not hitch rides randomly on available eclosing wasps within the fig syconium, but are specifically attracted, at close range, i.e. 3 mm distance, to only that vehicle which can quickly, within a few hours, reliably transfer it to another fig. This vehi- cle is the female pollinating wasp. Male wasps and female parasitic wasps are inappropriate vehicles since the former are wingless and die within the fig, while the latter never enter another fig. Nema- todes distinguished between female pollinating wasps and other female parasitic wasps using volatiles and cuticular hydrocarbons. Nematodes could not distinguish between cuticular hydro- carbons of male and female pollinators but used other cues, such as volatiles, at close range, to find female pollinating wasps with which they have probably had a long history of chemical adaptation. 5. This study opens up new questions and hypotheses about the evolution and maintenance of specificity in fig–wasp–nematode tritrophic interactions. Key-words: cuticular hydrocarbons, host specificity, plant–animal interactions, phoresy, plant–insect interactions, tritrophic interactions, volatiles
of the passenger or its progeny either due to crowding, Introduction habitat deterioration, sibling rivalry or for mate finding Phoresy is a phenomenon in which the phoretic organism (Farish & Axtell 1971; Binns 1982; Colwell 1986; Kruitbos, (the passenger) actively seeks out its vehicle for dispersal or Heritage & Wilson 2009). Therefore, ephemeral, patchy or migration out of areas unsuitable for further development unpredictable habitats coupled with low vagility of the passenger select for the evolution of a passenger–vehicle *Correspondence author. E-mail: [email protected] relationship (Houck & OConnor 1991; Zeh & Zeh 1992)