Limits...
Water stress strengthens mutualism among ants, trees, and scale insects.

Pringle EG, Akçay E, Raab TK, Dirzo R, Gordon DM - PLoS Biol. (2013)

Bottom Line: Abiotic environmental variables strongly affect the outcomes of species interactions.A model of the carbon trade-offs for the mutualistic partners shows that the observed strategies can arise from the carbon costs of rare but extreme events of herbivory in the rainy season.Thus, water limitation, together with the risk of herbivory, increases the strength of a carbon-based mutualism.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Stanford University, Stanford, California, United States of America ; Michigan Society of Fellows, University of Michigan, Ann Arbor, Michigan, United States of America ; Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, Michigan, United States of America ; School of Natural Resources and Environment, University of Michigan, Ann Arbor, Michigan, United States of America.

ABSTRACT
Abiotic environmental variables strongly affect the outcomes of species interactions. For example, mutualistic interactions between species are often stronger when resources are limited. The effect might be indirect: water stress on plants can lead to carbon stress, which could alter carbon-mediated plant mutualisms. In mutualistic ant-plant symbioses, plants host ant colonies that defend them against herbivores. Here we show that the partners' investments in a widespread ant-plant symbiosis increase with water stress across 26 sites along a Mesoamerican precipitation gradient. At lower precipitation levels, Cordia alliodora trees invest more carbon in Azteca ants via phloem-feeding scale insects that provide the ants with sugars, and the ants provide better defense of the carbon-producing leaves. Under water stress, the trees have smaller carbon pools. A model of the carbon trade-offs for the mutualistic partners shows that the observed strategies can arise from the carbon costs of rare but extreme events of herbivory in the rainy season. Thus, water limitation, together with the risk of herbivory, increases the strength of a carbon-based mutualism.

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Schematic of relationships among water, carbon, and mutualistic carbohydrate allocation strategies.Trees and protective ants engage in an indirect exchange of carbon. Trees produce carbohydrates by photosynthesis and use them for growth, reproduction, and to support the scale insects that feed the defending ant colony. Water is necessary for trees to produce leaves and affects the efficiency with which leaves produce carbohydrates. Ants use carbohydrates to make sterile workers and reproductives. Workers defend the tree leaves from herbivory, and thereby protect the carbon source. Arrows denote positive effects; lines that end in Ts denote negative effects. In this study, we examine these relationships to test whether water stress leads to carbon stress and thereby increases the strength of the ant–plant mutualism.
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pbio-1001705-g001: Schematic of relationships among water, carbon, and mutualistic carbohydrate allocation strategies.Trees and protective ants engage in an indirect exchange of carbon. Trees produce carbohydrates by photosynthesis and use them for growth, reproduction, and to support the scale insects that feed the defending ant colony. Water is necessary for trees to produce leaves and affects the efficiency with which leaves produce carbohydrates. Ants use carbohydrates to make sterile workers and reproductives. Workers defend the tree leaves from herbivory, and thereby protect the carbon source. Arrows denote positive effects; lines that end in Ts denote negative effects. In this study, we examine these relationships to test whether water stress leads to carbon stress and thereby increases the strength of the ant–plant mutualism.

Mentions: Plant carbon limitation may be an important physiological mechanism mediating plant response to water stress [12],[13], but it is not clear how carbon limitation affects plant–animal mutualisms [14],[15]. Sustained water limitation causes plants to close stomata and reduce leaf area, which should increase the risk of carbon starvation [16],[17]. Such carbon stress would be exacerbated by leaf-area loss from herbivory (Figure 1). Because ants defend the leaves but represent a carbon cost to plants, plants under water stress should invest more in ant defenders if (1) water stress indeed leads to reduced carbon availability and (2) the carbon cost of maintaining ant colonies is lower than the cost of leaf herbivory.


Water stress strengthens mutualism among ants, trees, and scale insects.

Pringle EG, Akçay E, Raab TK, Dirzo R, Gordon DM - PLoS Biol. (2013)

Schematic of relationships among water, carbon, and mutualistic carbohydrate allocation strategies.Trees and protective ants engage in an indirect exchange of carbon. Trees produce carbohydrates by photosynthesis and use them for growth, reproduction, and to support the scale insects that feed the defending ant colony. Water is necessary for trees to produce leaves and affects the efficiency with which leaves produce carbohydrates. Ants use carbohydrates to make sterile workers and reproductives. Workers defend the tree leaves from herbivory, and thereby protect the carbon source. Arrows denote positive effects; lines that end in Ts denote negative effects. In this study, we examine these relationships to test whether water stress leads to carbon stress and thereby increases the strength of the ant–plant mutualism.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3818173&req=5

pbio-1001705-g001: Schematic of relationships among water, carbon, and mutualistic carbohydrate allocation strategies.Trees and protective ants engage in an indirect exchange of carbon. Trees produce carbohydrates by photosynthesis and use them for growth, reproduction, and to support the scale insects that feed the defending ant colony. Water is necessary for trees to produce leaves and affects the efficiency with which leaves produce carbohydrates. Ants use carbohydrates to make sterile workers and reproductives. Workers defend the tree leaves from herbivory, and thereby protect the carbon source. Arrows denote positive effects; lines that end in Ts denote negative effects. In this study, we examine these relationships to test whether water stress leads to carbon stress and thereby increases the strength of the ant–plant mutualism.
Mentions: Plant carbon limitation may be an important physiological mechanism mediating plant response to water stress [12],[13], but it is not clear how carbon limitation affects plant–animal mutualisms [14],[15]. Sustained water limitation causes plants to close stomata and reduce leaf area, which should increase the risk of carbon starvation [16],[17]. Such carbon stress would be exacerbated by leaf-area loss from herbivory (Figure 1). Because ants defend the leaves but represent a carbon cost to plants, plants under water stress should invest more in ant defenders if (1) water stress indeed leads to reduced carbon availability and (2) the carbon cost of maintaining ant colonies is lower than the cost of leaf herbivory.

Bottom Line: Abiotic environmental variables strongly affect the outcomes of species interactions.A model of the carbon trade-offs for the mutualistic partners shows that the observed strategies can arise from the carbon costs of rare but extreme events of herbivory in the rainy season.Thus, water limitation, together with the risk of herbivory, increases the strength of a carbon-based mutualism.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Stanford University, Stanford, California, United States of America ; Michigan Society of Fellows, University of Michigan, Ann Arbor, Michigan, United States of America ; Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, Michigan, United States of America ; School of Natural Resources and Environment, University of Michigan, Ann Arbor, Michigan, United States of America.

ABSTRACT
Abiotic environmental variables strongly affect the outcomes of species interactions. For example, mutualistic interactions between species are often stronger when resources are limited. The effect might be indirect: water stress on plants can lead to carbon stress, which could alter carbon-mediated plant mutualisms. In mutualistic ant-plant symbioses, plants host ant colonies that defend them against herbivores. Here we show that the partners' investments in a widespread ant-plant symbiosis increase with water stress across 26 sites along a Mesoamerican precipitation gradient. At lower precipitation levels, Cordia alliodora trees invest more carbon in Azteca ants via phloem-feeding scale insects that provide the ants with sugars, and the ants provide better defense of the carbon-producing leaves. Under water stress, the trees have smaller carbon pools. A model of the carbon trade-offs for the mutualistic partners shows that the observed strategies can arise from the carbon costs of rare but extreme events of herbivory in the rainy season. Thus, water limitation, together with the risk of herbivory, increases the strength of a carbon-based mutualism.

Show MeSH
Related in: MedlinePlus