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      Premature Attraction of Pollinators to Inaccessible Figs of Ficus altissima: A Search for Ecological and Evolutionary Consequences

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          Abstract

          Adult life spans of only one or two days characterise life cycles of the fig wasps (Agaonidae) that pollinate fig trees ( Ficus spp., Moraceae). Selection is expected to favour traits that maximise the value of the timing of encounters between such mutualistic partners, and fig wasps are usually only attracted to their hosts by species- and developmental-stage specific volatiles released from figs at the time when they are ready to be entered, oviposited in and pollinated. We found that Ficus altissima is exceptional, because it has persistent tight-fitting bud covers that prevent its Eupristina altissima pollinator (and a second species of ‘cheater’ agaonid) from entering its figs for several days after they start to be attracted. We examined the consequences of delayed entry for the figs and fig wasps and tested whether delayed entry has been selected to increase adult longevity. We found that older pollinators produced fewer and smaller offspring, but seed production was more efficient. Pollinator offspring ratios also varied depending on the age of figs they entered. The two agaonids from F. altissima lived slightly longer than six congeners associated with typical figs, but this was explainable by their larger body sizes. Delayed entry generates reproductive costs, especially for the pollinator. This opens an interesting perspective on the coevolution of figs and their pollinators and on the nature of mutualistic interactions in general.

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          Plasticity in life-history traits.

          We describe the impact of recent life-history plasticity theory on insect studies, particularly on the interface between genetics and plasticity. We focus on the three-dimensional relationship between three key life-history traits: adult size (or mass), development time and growth rate, and the connections to life cycle regulation, host plant choice, and sexual selection in seasonal environments. The review covers fitness consequences of variation in size, development time and growth rate, and effects of sex, photoperiod, temperature, diet, and perceived mortality risk on these traits. We give special attention to evidence for adaptive plasticity in growth rates because of the important effects of such plasticity on the expected relationships between development time and adult size and, hence, on the use of life-history, fitness, and optimality approaches in ecology, as well as in genetics.
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            Fig-eating by vertebrate frugivores: a global review.

            The consumption of figs (the fruit of Ficus spp.: Moraceae) by vertebrates is reviewed using data from the literature, unpublished accounts and new field data from Borneo and Hong Kong. Records of frugivory from over 75 countries are presented for 260 Ficus species (approximately 30% of described species). Explanations are presented for geographical and taxonomic gaps in the otherwise extensive literature. In addition to a small number of reptiles and fishes, 1274 bird and mammal species in 523 genera and 92 families are known to eat figs. In terms of the number of species and genera of fig-eaters and the number of fig species eaten we identify the avian families interacting most with Ficus to be Columbidae, Psittacidae, Pycnonotidae, Bucerotidae, Sturnidae and Lybiidae. Among mammals, the major fig-eating families are Pteropodidae, Cercopithecidae, Sciuridae, Phyllostomidae and Cebidae. We assess the role these and other frugivores play in Ficus seed dispersal and identify fig-specialists. In most, but not all, cases fig specialists provide effective seed dispersal services to the Ficus species on which they feed. The diversity of fig-eaters is explained with respect to fig design and nutrient content, phenology of fig ripening and the diversity of fig presentation. Whilst at a gross level there exists considerable overlap between birds, arboreal mammals and fruit bats with regard to the fig species they consume, closer analysis, based on evidence from across the tropics, suggests that discrete guilds of Ficus species differentially attract subsets of sympatric frugivore communities. This dispersal guild structure is determined by interspecific differences in fig design and presentation. Throughout our examination of the fig-frugivore interaction we consider phylogenetic factors and make comparisons between large-scale biogeographical regions. Our dataset supports previous claims that Ficus is the most important plant genus for tropical frugivores. We explore the concept of figs as keystone resources and suggest criteria for future investigations of their dietary importance. Finally, fully referenced lists of frugivores recorded at each Ficus species and of Ficus species in the diet of each frugivore are presented as online appendices. In situations where ecological information is incomplete or its retrieval is impractical, this valuable resource will assist conservationists in evaluating the role of figs or their frugivores in tropical forest sites.
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              Specific attraction of fig-pollinating wasps: role of volatile compounds released by tropical figs.

              Floral scents often act as pollinator attractants. In the case of obligate and specific plant-pollinator relationships, the role of floral signals may be crucial in allowing the encounter of the partners. About 750 Ficus species (Moraceae) are involved in such interactions, each with a distinct species of pollinating wasp (Chalcidoidea, Agaonidae). Several species have been shown to release volatile compounds, but their role in pollinator attraction has rarely been simultaneously tested. We investigated the floral scents of four tropical fig species and combined chemical analysis with biological tests of stimulation of insects. Pollinators of three species were stimulated by the odor of their associated fig species and generally not by the odor of another species. The fourth actually comprised two distinct varieties. The main compound was often a different one in each species. Floral blends of different species always shared compounds, but ratios of these compounds varied among species.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2014
                22 January 2014
                : 9
                : 1
                : e86735
                Affiliations
                [1 ]Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Kunming, China
                [2 ]Yunnan Academy of Biodiversity, Southwest Forestry University, Kunming China
                [3 ]School of Biology, University of Leeds, Leeds, United Kingdom
                [4 ]Department of Zoology and Entomology, Rhodes University, Grahamstown, South Africa
                Ghent University, Belgium
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: YZ YQP DRY. Performed the experiments: YZ YQP DRY. Analyzed the data: YZ. Contributed reagents/materials/analysis tools: YQP DRY. Wrote the paper: YZ YQP SGC.

                Article
                PONE-D-13-38595
                10.1371/journal.pone.0086735
                3899289
                24466217
                5b6948bb-e6e8-4566-a23c-2600d34a1f73
                Copyright @ 2014

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 19 September 2013
                : 17 December 2013
                Page count
                Pages: 8
                Funding
                This study was funded by Candidates of the Young and Middle Aged Academic Leaders of Yunnan Province (2011HB041), and the Chinese Natural Science Foundation (31372253, 31120002). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology
                Ecology
                Community Ecology
                Species Interactions
                Behavioral Ecology
                Evolutionary Biology
                Animal Behavior
                Behavioral Ecology
                Evolutionary Ecology
                Zoology
                Animal Behavior
                Entomology
                Veterinary Science
                Animal Management
                Animal Behavior
                Sexual Behavior

                Uncategorized
                Uncategorized

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