Chemical composition of leaf volatiles in Macaranga species (Euphorbiaceae) and their potential role as olfactory cues in host-localization of foundress queens of specific ant partners

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Abstract

Host-plant finding by foundress queens is an important step in the establishment of ant–plant symbioses and olfactory cues may play a crucial role in the MacarangaCrematogaster ant–plant system for attracting foundresses over longer distances. MicroSPE was used to investigate leaf volatiles of 11 myrmecophytic and non-myrmecophytic Macaranga species. Chemical analysis (GC–MS) yielded a total of 114 compounds comprising a great diversity, including aliphatic compounds, aromatics, mono- and sesquiterpenoids. An analysis of the volatile data using the CNESS distances of the chemical profiles, followed by visualization of the data with non-metric multidimensional scaling (NMDS) showed that even closely related species sharing the same ant partners have clearly different scent patterns. Comparison of spectra of volatile compounds between obligate myrmecophytic Macaranga species and myrmecophilous species that are only facultatively associated with unspecific arboreal ants did not reveal general differences. Choice experiments conducted with foundresses revealed that the ants have the capacity to distinguish between different host species. However, the behavior of the foundresses following surface contact with saplings indicates that other cues, like surface structure, may play a more important role in host-recognition over short distances than volatile compounds. We discuss alternative hypotheses for the possible role of leaf volatiles in the examined Macaranga species as chemical defense against herbivores.

Introduction

Mutualistic ant–plant associations are common in tropical ecosystems. Over 400 tropical plant species from more than 40 genera are known worldwide as myrmecophytes (ant–plants, Davidson and McKey, 1993). These plants are protected by specific ants, usually in exchange for housing and sometimes food (e.g. Janzen, 1969, Fiala et al., 1989, Gaume et al., 1997, Heil et al., 2001, Heil and McKey, 2003). The South East Asian CrematogasterMacaranga ant–plant symbiotic system is one of the most species rich ant–plant systems worldwide. The genus Macaranga includes about 250 dioecious shrub and tree species with a paleotropic distribution pattern and its center of diversity in New Guinea and Borneo (Whitmore, 1969). Most species within the genus Macaranga Thou. (Euphorbiaceae) in SE Asia are associated with ants, but the degree of interaction between plants and ants may vary from loosely facultative, non-specific myrmecophylic to obligate myrmecophytic associations (Fiala et al., 1994, Feldhaar et al., 2003a). In facultative myrmecophilous interactions plants are visited by unspecific arboreal ants foraging for food bodies or extrafloral nectar. In obligate myrmecophytic associations Macaranga host-plants provide food bodies as well as nesting-space in hollow internodes (“domatia”) for ants. In return, ants confer protection against herbivores as well as competitive climbers (Fiala et al., 1989, Fiala et al., 1994, Federle et al., 1997, Heil et al., 2001). Twenty-nine species of Macaranga are known to be obligately associated with to date nine only informally described ant species, mainly from the genus Crematogaster subgenus Decacrema (Fiala et al., 1999, Blattner et al., 2001, Davies et al., 2001, Feldhaar et al., 2003a). Thus, in obligate associations each Macaranga species is interacting with only one to four different ant species. From the ant's point of view the specificity of the association is slightly lower as each ant species is able to colonize between two to seven different host-plant species over its whole distributional range (Fiala et al., 1999, Feldhaar et al., 2003a,b). However, in spite of the usually sympatric occurrence of several myrmecophytic Macaranga species high levels of species-specificity are maintained in this ant–plant symbiotic system (Fiala et al., 1999). One key character that restricts host-usage of the specific ant partners is a waxy surface of stems and branches of some Macaranga host species. The specific Crematogaster ants can be separated into “wax runners” that are able to walk on these surfaces and “non-wax runners” that are not (or less) able to do so (Federle et al., 1997, Fiala et al., 1999, Feldhaar et al., 2003a).

The most crucial moment of these obligate associations is their beginning, as the two matching partners have to come together in each successive generation to establish the association anew. It is vital for foundress queens that host-localization and host-choice is performed as quickly as possible to avoid predation outside the safety of the host-plants, whereas rapid colonization at sapling stage is often crucial for the host-plants to survive this vulnerable stage without damage by herbivores and competitors. Generally, small host-plants from the height of 15–30 cm are colonized by individual foundresses. The host-plants are rarely found uninhabited (Fiala et al., 1999) thus proving that the foundresses were able to locate the saplings although these often grow hidden amidst the vegetation along forest edges or in the understorey. However, to date, the proximate mechanisms involved in host-plant finding are not known from any ant–plant system. Because most foundresses were found to colonize saplings at night (Fiala and Maschwitz, 1990), we hypothesize that chemical cues (e.g. volatiles emitted by vegetative tissues) prevail over visual cues.

The aim of the present study is to characterize the chemistry of leaf volatile compounds of 11 Macaranga species in order to identify the components in the bouquet and to learn if the leaf volatiles show sufficient variation among Macaranga species to allow for specific host-plant recognition. Subsequent questions are, if volatile composition is related to the phylogeny of the plants or other traits such as wax-coating or specific ant partners. Additionally, to study host-choice behavior of foundresses and their specialization in host-finding, we conducted choice experiments with alate queens and sympatrically occurring Macaranga species. We discuss the potential of leaf volatiles as chemical cues for host-plant recognition in mutualistic ants and other possible functions, e.g. as chemical defense against herbivores.

Section snippets

Plant material

Macaranga plants were collected from Peninsular Malaysia or Borneo and then cultivated in greenhouses at the Biocenter of the University of Würzburg. Because we collected all volatile samples from greenhouse plants of which we kept only one or a few individuals, no herbarium specimens were collected from our sampled trees. Nevertheless, voucher specimens of the investigated Macaranga species are in the collection of the senior author and have also been deposited in the herbaria of the

Leaf volatiles of Macaranga species

Chemical composition of leaf volatiles from 11 Macaranga species is shown in Table 2. Compounds listed in Table 2 are ordered in classes, which to some degree reflect their biosynthetic origin (see Knudsen et al., 1993). Using the MicroSPE technique, we detected a total of 114 volatiles, from which 89 could be identified by mass spectra and retention times. Number of components ranged from 29 in M. hosei to 69 in Macaranga bancana. For a summary of volatile spectra based on dominant compound

Leaf volatiles in Macaranga species and their potential role as cues in host-plant finding and host-plant choice: relations to phylogeny, wax-coating and ant-inhabitation

One objective of this study was to gain insight into the composition of leaf volatiles that might be important for host-choice and/or host-recognition of foundress queens. Attraction from a distance may involve olfaction, vision, or both. As nuptial flights of specific partner-ants are usually nocturnal (Fiala and Maschwitz, 1990; H. Feldhaar, personal observations) volatile compounds of potential host-plants may play a crucial role as olfactory cues in host-localization over longer distances.

Acknowledgements

The authors thank Karl Eduard Linsenmair, Zoology III for financial support for maintenance of the greenhouse facilities, and Andrea Hilpert for careful help in cultivation of the plants. We are thankful to Taina Witt and Stefan Dötterl for their valuable comments on the manuscript, and help with the statistical analyses of the chemical scent profiles. We are grateful for financial support by the Deutsche Forschungsgemeinschaft (DFG). Andreas Jürgens (Grant JU418/3-1), Heike Feldhaar and

References (61)

  • E. Pichersky et al.

    The formation and function of plant volatiles: perfumes for pollinator attraction and defense

    Current Opinion in Plant Biology

    (2002)
  • E. Städler

    Behavioral responses of insects to plant secondary compounds

  • R.P. Adams

    Identification of Essential Oil Components by Gas Chromatography/Mass Spectrometry

    (1995)
  • A. Amirav et al.

    A direct sample introduction device for mass spectrometry studies and GC–MS analysis

    European Journal of Mass Spectrometry

    (1997)
  • H. Azuma et al.

    Molecular phylogeny of Magnolia (Magnoliaceae) inferred from cpDNA sequences and evolutionary divergence of the floral scents

    Journal of Plant Research

    (1999)
  • I.T. Baldwin et al.

    Volatile signalling in plant–plant-herbivore interactions: what is real?

    Current Opinion in Plant Biology

    (2002)
  • G. Bänfer et al.

    AFLP analysis of phylogenetic relationships among myrmecophytic species of Macaranga (Euphorbiaceae) and their allies

    Plant Systematics and Evolution

    (2004)
  • A. Berkov et al.

    Do Lecythidaceae specialists (Coleoptera, Cerambycidae) shun fetid tree species?

    Biotropica

    (2000)
  • E.A. Bernays et al.

    Host-Plant Selection by Phytophagous Insects

    (1994)
  • Boesch, D.F., 1977. Application of numerical classification in ecological investigations of water pollution. Report...
  • I. Borg et al.

    Multidimensional Similarity Structure Analysis

    (1987)
  • S.J. Davies

    Systematics of Macaranga Sects. Pachystemon and Pruinosae (Euphorbiaceae)

    Harvard Papers in Botany

    (2001)
  • S.J. Davies et al.

    Evolution of myrmecophytism in western malesian Macaranga (Euphorbiaceae)

    Evolution

    (2001)
  • D.W. Davidson et al.

    The evolutionary ecology of symbiotic ant–plant relationships

    Journal of Hymenoptera Research

    (1993)
  • M. Dicke et al.

    Multitrophic effects of herbivore-induced plant volatiles in an evolutionary context

    Entomologia Experimentalis et Applicata

    (2000)
  • Dötterl, S., 2004. Importance of floral scent compounds for the interaction between Silene latifolia (Caryophyllaceae)...
  • G. Eck et al.

    Trade-off between chemical and biotic antiherbivore defense in the South East Asian plant genus Macaranga

    Journal of Chemical Ecology

    (2001)
  • W. Federle et al.

    Slippery ant–plants and skilful climbers: selection and protection of specific ant partners by epicuticular wax blooms in Macaranga (Euphorbiaceae)

    Oecologia

    (1997)
  • H. Feldhaar et al.

    Dynamics of the CrematogasterMacaranga association: the ant partner makes the difference

    Insectes Sociaux

    (2003)
  • B. Fiala et al.

    Diversity of ant–plant interactions: Protective efficacy in Macaranga species with different degrees of ant-association

    Oecologia

    (1994)
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