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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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Mutualism strength increases as water availability decreases.(A) Relationship between annual precipitation of a site and the density of scale insects for all 26 sites (R2 = 0.31, F1,24 = 12.15, p<0.002). (B) Relationship between annual precipitation of a site and ant colony size (density of worker ants) for all 26 sites (R2 = 0.32, F1,24 = 12.95, p<0.002). (C) Relationship between annual precipitation of a site and the latency of ant response to a standardized disturbance (R2 = 0.40, F1,24 = 17.87, p<0.0003). Error bars represent the square root of the total variance across sites divided by the sample size at each site. (D) Difference in percent leaf area eaten between when ants were present and when ants were experimentally excluded at three dry-forest sites along the annual-precipitation gradient from driest (Chamela) to wettest (Santa Rosa). Bars represent mean differences from matched-pair experiments within trees ± SE. Asterisks (*) indicate bars are significantly different from zero by one-sample matched-pair Wilcoxon tests (p<0.04); Chamela, N = 39; Huatulco, N = 27; Santa Rosa, N = 40.
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pbio-1001705-g003: Mutualism strength increases as water availability decreases.(A) Relationship between annual precipitation of a site and the density of scale insects for all 26 sites (R2 = 0.31, F1,24 = 12.15, p<0.002). (B) Relationship between annual precipitation of a site and ant colony size (density of worker ants) for all 26 sites (R2 = 0.32, F1,24 = 12.95, p<0.002). (C) Relationship between annual precipitation of a site and the latency of ant response to a standardized disturbance (R2 = 0.40, F1,24 = 17.87, p<0.0003). Error bars represent the square root of the total variance across sites divided by the sample size at each site. (D) Difference in percent leaf area eaten between when ants were present and when ants were experimentally excluded at three dry-forest sites along the annual-precipitation gradient from driest (Chamela) to wettest (Santa Rosa). Bars represent mean differences from matched-pair experiments within trees ± SE. Asterisks (*) indicate bars are significantly different from zero by one-sample matched-pair Wilcoxon tests (p<0.04); Chamela, N = 39; Huatulco, N = 27; Santa Rosa, N = 40.

Mentions: (A) Map showing the 26 study sites and (B) their annual precipitation. Additional work was conducted at three of the sites, Chamela (white circle), Huatulco (gray diamond), and Santa Rosa (black triangle), that spanned the Mesoamerican dry-forest precipitation gradient.


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

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

Mutualism strength increases as water availability decreases.(A) Relationship between annual precipitation of a site and the density of scale insects for all 26 sites (R2 = 0.31, F1,24 = 12.15, p<0.002). (B) Relationship between annual precipitation of a site and ant colony size (density of worker ants) for all 26 sites (R2 = 0.32, F1,24 = 12.95, p<0.002). (C) Relationship between annual precipitation of a site and the latency of ant response to a standardized disturbance (R2 = 0.40, F1,24 = 17.87, p<0.0003). Error bars represent the square root of the total variance across sites divided by the sample size at each site. (D) Difference in percent leaf area eaten between when ants were present and when ants were experimentally excluded at three dry-forest sites along the annual-precipitation gradient from driest (Chamela) to wettest (Santa Rosa). Bars represent mean differences from matched-pair experiments within trees ± SE. Asterisks (*) indicate bars are significantly different from zero by one-sample matched-pair Wilcoxon tests (p<0.04); Chamela, N = 39; Huatulco, N = 27; Santa Rosa, N = 40.
© Copyright Policy
Related In: Results  -  Collection

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

pbio-1001705-g003: Mutualism strength increases as water availability decreases.(A) Relationship between annual precipitation of a site and the density of scale insects for all 26 sites (R2 = 0.31, F1,24 = 12.15, p<0.002). (B) Relationship between annual precipitation of a site and ant colony size (density of worker ants) for all 26 sites (R2 = 0.32, F1,24 = 12.95, p<0.002). (C) Relationship between annual precipitation of a site and the latency of ant response to a standardized disturbance (R2 = 0.40, F1,24 = 17.87, p<0.0003). Error bars represent the square root of the total variance across sites divided by the sample size at each site. (D) Difference in percent leaf area eaten between when ants were present and when ants were experimentally excluded at three dry-forest sites along the annual-precipitation gradient from driest (Chamela) to wettest (Santa Rosa). Bars represent mean differences from matched-pair experiments within trees ± SE. Asterisks (*) indicate bars are significantly different from zero by one-sample matched-pair Wilcoxon tests (p<0.04); Chamela, N = 39; Huatulco, N = 27; Santa Rosa, N = 40.
Mentions: (A) Map showing the 26 study sites and (B) their annual precipitation. Additional work was conducted at three of the sites, Chamela (white circle), Huatulco (gray diamond), and Santa Rosa (black triangle), that spanned the Mesoamerican dry-forest precipitation gradient.

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