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
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 Crematogaster–Macaranga 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)
- et al.
Molecular analysis of phylogenetic relationships among myrmecophytic Macaranga species (Euphorbiaceae)
Molecular Phylogenetics and Evolution
(2001) - et al.
Leaf volatile compounds and the distribution of ant patrolling in an ant–plant protection mutualism: preliminary results on Leonardoxa (Fabaceae: Caesalpinioideae) and Petalomyrmex (Formicidae: Formicinae)
Acta Oecologia
(2000) - et al.
Innate attraction supplants experience during host plant selection in an obligate plant–ant
Behavioural Processes
(1999) Chemical ecology of host-plant selection by herbivorous arthropods: a multitrophic perspective
Biochemical Systematics and Ecology
(2000)- et al.
Induced plant defences: from molecular biology to evolutionary ecology
Basic and Applied Ecology
(2003) - et al.
Molecular phylogeny of Crematogaster subgenus Decacrema ants (Hymenoptera: Formicidae) and the colonization of Macaranga (Euphorbiaceae) trees
Molecular Phylogenetics and Evolution
(2003) - et al.
Diversity, evolutionary specialization and geographic distribution of a mutualistic ant–plant complex: Macaranga and Crematogaster in South East Asia
Biological Journal of the Linnean Society
(1999) - et al.
Terpenoids
- et al.
SnifProbe: new method and device for vapor and gas sampling
Journal of Chromatography A
(2000) - et al.
Floral scents – a checklist of volatile compounds isolated by head-space techniques
Phytochemistry
(1993)
The formation and function of plant volatiles: perfumes for pollinator attraction and defense
Current Opinion in Plant Biology
Behavioral responses of insects to plant secondary compounds
Identification of Essential Oil Components by Gas Chromatography/Mass Spectrometry
A direct sample introduction device for mass spectrometry studies and GC–MS analysis
European Journal of Mass Spectrometry
Molecular phylogeny of Magnolia (Magnoliaceae) inferred from cpDNA sequences and evolutionary divergence of the floral scents
Journal of Plant Research
Volatile signalling in plant–plant-herbivore interactions: what is real?
Current Opinion in Plant Biology
AFLP analysis of phylogenetic relationships among myrmecophytic species of Macaranga (Euphorbiaceae) and their allies
Plant Systematics and Evolution
Do Lecythidaceae specialists (Coleoptera, Cerambycidae) shun fetid tree species?
Biotropica
Host-Plant Selection by Phytophagous Insects
Multidimensional Similarity Structure Analysis
Systematics of Macaranga Sects. Pachystemon and Pruinosae (Euphorbiaceae)
Harvard Papers in Botany
Evolution of myrmecophytism in western malesian Macaranga (Euphorbiaceae)
Evolution
The evolutionary ecology of symbiotic ant–plant relationships
Journal of Hymenoptera Research
Multitrophic effects of herbivore-induced plant volatiles in an evolutionary context
Entomologia Experimentalis et Applicata
Trade-off between chemical and biotic antiherbivore defense in the South East Asian plant genus Macaranga
Journal of Chemical Ecology
Slippery ant–plants and skilful climbers: selection and protection of specific ant partners by epicuticular wax blooms in Macaranga (Euphorbiaceae)
Oecologia
Dynamics of the Crematogaster–Macaranga association: the ant partner makes the difference
Insectes Sociaux
Diversity of ant–plant interactions: Protective efficacy in Macaranga species with different degrees of ant-association
Oecologia
Cited by (44)
Leaf epicuticular wax content changes under different rainfall regimes, and its removal affects the leaf chlorophyll content and gas exchanges of Aspidosperma pyrifolium in a seasonally dry tropical forest
2017, South African Journal of BotanyCitation Excerpt :EW content (or quantity) is not the only factor determining the properties and function of the waxy layer; knowledge on composition (or quality) is also imperative. Compounds as β-amyrins, lupeol, triterpenes, taraxerol, alkanes and other classes were found in the EW of other plant genera, as Macaranga and Manihot (Markstädter et al., 2000; Jürgens et al., 2006). These compounds, however, were related to plant-insect interactions, and research that addresses the importance of EW composition in response to abiotic stressors, such as water deficit, is still scarce.
Eulemur, me lemur: The evolution of scent-signal complexity in a primate clade
2012, Philosophical Transactions of the Royal Society B: Biological SciencesComparative pollination ecology of five european euphorbia species
2021, International Journal of Plant Sciences