Dataset Information

Diversity and evolution of a trait mediating ant-plant interactions: insights from extrafloral nectaries in Senna (Leguminosae).

ABSTRACT:

Background and aims

Plants display a wide range of traits that allow them to use animals for vital tasks. To attract and reward aggressive ants that protect developing leaves and flowers from consumers, many plants bear extrafloral nectaries (EFNs). EFNs are exceptionally diverse in morphology and locations on a plant. In this study the evolution of EFN diversity is explored by focusing on the legume genus Senna, in which EFNs underwent remarkable morphological diversification and occur in over 80 % of the approx. 350 species.

Methods

EFN diversity in location, morphology and plant ontogeny was characterized in wild and cultivated plants, using scanning electron microscopy and microtome sectioning. From these data EFN evolution was reconstructed in a phylogenetic framework comprising 83 Senna species.

Key results

Two distinct kinds of EFNs exist in two unrelated clades within Senna. 'Individualized' EFNs (iEFNs), located on the compound leaves and sometimes at the base of pedicels, display a conspicuous, gland-like nectary structure, are highly diverse in shape and characterize the species-rich EFN clade. Previously overlooked 'non-individualized' EFNs (non-iEFNs) embedded within stipules, bracts, and sepals are cryptic and may represent a new synapomorphy for clade II. Leaves bear EFNs consistently throughout plant ontogeny. In one species, however, early seedlings develop iEFNs between the first pair of leaflets, but later leaves produce them at the leaf base. This ontogenetic shift reflects our inferred diversification history of iEFN location: ancestral leaves bore EFNs between the first pair of leaflets, while leaves derived from them bore EFNs either between multiple pairs of leaflets or at the leaf base.

Conclusions

EFNs are more diverse than previously thought. EFN-bearing plant parts provide different opportunities for EFN presentation (i.e. location) and individualization (i.e. morphology), with implications for EFN morphological evolution, EFN-ant protective mutualisms and the evolutionary role of EFNs in plant diversification.

SUBMITTER: Marazzi B

PROVIDER: S-EPMC3662506 | biostudies-literature | 2013 Jun

REPOSITORIES: biostudies-literature

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Publications

Diversity and evolution of a trait mediating ant-plant interactions: insights from extrafloral nectaries in Senna (Leguminosae).

Marazzi Brigitte B Conti Elena E Sanderson Michael J MJ McMahon Michelle M MM Bronstein Judith L JL

Annals of botany 20121026 6

<h4>Background and aims</h4>Plants display a wide range of traits that allow them to use animals for vital tasks. To attract and reward aggressive ants that protect developing leaves and flowers from consumers, many plants bear extrafloral nectaries (EFNs). EFNs are exceptionally diverse in morphology and locations on a plant. In this study the evolution of EFN diversity is explored by focusing on the legume genus Senna, in which EFNs underwent remarkable morphological diversification and occur ...[more]

PMID: 23104672

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Project description:Ant guards protect plants from herbivores, but can also hinder pollination by damaging reproductive structures and/or repelling pollinators. Natural selection should favour the evolution of plant traits that deter ants from visiting flowers during anthesis, without waiving their defensive services. The Distraction Hypothesis posits that rewarding ants with extrafloral nectar could reduce their visitation of flowers, reducing ant-pollinator conflict while retaining protection of other structures.We characterised the proportion of flowers occupied by ants and the number of ants per flower in a Mexican ant-plant, Turnera velutina. We clogged extrafloral nectaries on field plants and observed the effects on patrolling ants, pollinators and ants inside flowers, and quantified the effects on plant fitness. Based on the Distraction Hypothesis, we predicted that preventing extrafloral nectar secretion should result in fewer ants active at extrafloral nectaries, more ants inside flowers and a higher proportion of flowers occupied by ants, leading to ant-pollinator conflict, with reduced pollinator visitation and reduced plant fitness.Overall ant activity inside flowers was low. Preventing extrafloral nectar secretion through clogging reduced the number of ants patrolling extrafloral nectaries, significantly increased the proportion of flowers occupied by ants from 6.1% to 9.7%, and reduced plant reproductive output through a 12% increase in the probability of fruit abortion. No change in the numbers of ants or pollinators inside flowers was observed. This is the first support for the Distraction Hypothesis obtained under field conditions, showing ecological and plant fitness benefits of the distracting function of extrafloral nectar during anthesis. Synthesis. Our study provides the first field experimental support for the Distraction Hypothesis, suggesting that extrafloral nectaries located close to flowers may bribe ants away from reproductive structures during the crucial pollination period, reducing the probability of ant occupation of flowers, reducing ant-pollinator conflict and increasing plant reproductive success.

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Project description:Background and aimsIn complex communities, organisms often form mutualisms with multiple different partners simultaneously. Non-additive effects may emerge among species linked by these positive interactions. Ants commonly participate in mutualisms with both honeydew-producing insects (HPI) and their extrafloral nectary (EFN)-bearing host plants. Consequently, HPI and EFN-bearing plants may experience non-additive benefits or costs when these groups co-occur. The outcomes of these interactions are likely to be influenced by variation in preferences among ants for honeydew vs. nectar. In this study, a test was made for non-additive effects on HPI and EFN-bearing plants resulting from sharing exotic ant guards. Preferences of the dominant exotic ant species for nectar vs. honeydew resources were also examined.MethodsAnt access, HPI and nectar availability were manipulated on the EFN-bearing shrub, Morinda citrifolia, and ant and HPI abundances, herbivory and plant growth were assessed. Ant-tending behaviours toward HPI across an experimental gradient of nectar availability were also tracked in order to investigate mechanisms underlying ant responses.Key resultsThe dominant ant species, Anoplolepis gracilipes, differed from less invasive ants in response to multiple mutualists, with reductions in plot-wide abundances when nectar was reduced, but no response to HPI reduction. Conversely, at sites where A. gracilipes was absent or rare, abundances of less invasive ants increased when nectar was reduced, but declined when HPI were reduced. Non-additive benefits were found at sites dominated by A. gracilipes, but only for M. citrifolia plants. Responses of HPI at these sites supported predictions of the non-additive cost model. Interestingly, the opposite non-additive patterns emerged at sites dominated by other ants.ConclusionsIt was demonstrated that strong non-additive benefits and costs can both occur when a plant and herbivore share mutualist partners. These findings suggest that broadening the community context of mutualism studies can reveal important non-additive effects and increase understanding of the dynamics of species interactions.

Project description:Herbivory is an ecological process that is known to generate different patterns of selection on defensive plant traits across populations. Studies on this topic could greatly benefit from the general framework of the Geographic Mosaic Theory of Coevolution (GMT). Here, we hypothesize that herbivory represents a strong pressure for extrafloral nectary (EFN) bearing plants, with differences in herbivore and ant visitor assemblages leading to different evolutionary pressures among localities and ultimately to differences in EFN abundance and function. In this study, we investigate this hypothesis by analyzing 10 populations of Anemopaegma album (30 individuals per population) distributed through ca. 600 km of Neotropical savanna and covering most of the geographic range of this plant species. A common garden experiment revealed a phenotypic differentiation in EFN abundance, in which field and experimental plants showed a similar pattern of EFN variation among populations. We also did not find significant correlations between EFN traits and ant abundance, herbivory and plant performance across localities. Instead, a more complex pattern of ant-EFN variation, a geographic mosaic, emerged throughout the geographical range of A. album. We modeled the functional relationship between EFNs and ant traits across ant species and extended this phenotypic interface to characterize local situations of phenotypic matching and mismatching at the population level. Two distinct types of phenotypic matching emerged throughout populations: (1) a population with smaller ants (Crematogaster crinosa) matched with low abundance of EFNs; and (2) seven populations with bigger ants (Camponotus species) matched with higher EFN abundances. Three matched populations showed the highest plant performance and narrower variance of EFN abundance, representing potential plant evolutionary hotspots. Cases of mismatched and matched populations with the lowest performance were associated with abundant and highly detrimental herbivores. Our findings provide insights on the ecology and evolution of plant-ant guarding systems, and suggest new directions to research on facultative mutualistic interactions at wide geographic scales.

Dataset Information

Diversity and evolution of a trait mediating ant-plant interactions: insights from extrafloral nectaries in Senna (Leguminosae).

Background and aims

Methods

Key results

Conclusions

Publications

Diversity and evolution of a trait mediating ant-plant interactions: insights from extrafloral nectaries in Senna (Leguminosae).

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