Water Stress Strengthens Mutualism Among Ants, Trees, and Scale Insects

Pringle, Elizabeth G.; Akçay, Erol; Raab, Theodore K.; Dirzo, Rodolfo; Gordon, Deborah M.

doi:10.1371/journal.pbio.1001705

Cited by 52 publications

(59 citation statements)

References 49 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…, Pringle et al. ). Because plant neighbors have the potential to influence myrmecophytes both directly (e.g., through competition) or indirectly (e.g., facilitation via modifications of environmental conditions), they may play important roles in both the evolutionary (e.g., see Janzen ) and ecological dynamics of these widespread associations.…”

Section: Introductionmentioning

confidence: 99%

Influence of neighboring plants on the dynamics of an ant–acacia protection mutualism

Palmer

Riginos

Damiani

et al. 2017

Ecology

View full text Add to dashboard Cite

Ant-plant protection symbioses, in which plants provide food and/or shelter for ants in exchange for protection from herbivory, are model systems for understanding the ecology of mutualism. While interactions between ants, host plants, and herbivores have been intensively studied, we know little about how plant-plant interactions influence the dynamics of these mutualisms, despite strong evidence that plants compete for resources, that hosting ants can be costly, and that host-plant provisioning to ants can therefore be constrained by resource availability. We used field experiments in a semiarid Kenyan savanna to examine interactions between the ant-plant Acacia drepanolobium, neighboring grasses, and two species of symbiotic acacia-ants with divergent behaviors: Crematogaster mimosae, an aggressive symbiont that imposes high costs to host trees via consumption of extrafloral nectar, and Tetraponera penzigi, a less-protective symbiont that imposes lower costs because it does not consume nectar. We hypothesized that by competing with acacias for resources, neighboring grasses (1) reduce hosts' ability to support costly C. mimosae, while having little or no effect on the ability of hosts to support low-cost T. penzigi, and (2) reduce sapling growth rates irrespective of ant occupant. We factorially manipulated the presence/absence of grasses and the identity of ant occupants on saplings and evaluated effects on colony survivorship and sapling growth rates over 40 weeks. Contrary to prediction, the high-cost/high-reward nectar-dependent mutualist C. mimosae had higher colony-survival rates on saplings with grass neighbors present. Grasses appear to have indirectly facilitated the survival of C. mimosae by reducing water stress on host plants; soils under saplings shaded by grasses had higher moisture content, and these saplings produced more active nectaries than grass-removal saplings. Consistent with prediction, survival of low-cost/low-reward T. penzigi did not differ significantly between grass-removal treatments. Saplings occupied by low-cost/low-reward T. penzigi grew 100% more on average than saplings occupied by high-cost/high-reward C. mimosae, demonstrating that mutualist-partner identity strongly and differentially influences demographic rates of young plants. In contrast, contrary to prediction, grass neighbors had no significant net impact on sapling growth rates. Our results suggest that neighboring plants can exert strong and counterintuitive effects on ant-plant protection symbioses, highlighting the need to integrate plant-plant interactions into our understanding of these mutualisms.

show abstract

Section: Introductionmentioning

confidence: 99%

Influence of neighboring plants on the dynamics of an ant–acacia protection mutualism

Palmer

Riginos

Damiani

et al. 2017

Ecology

View full text Add to dashboard Cite

show abstract

“…), which may impact these interactions via weather perturbations (e.g., Piovia‐Scott ), resource limitation (e.g., Pringle et al. ), and herbivory (e.g., Pringle et al. ).…”

Section: Introductionmentioning

confidence: 99%

Fire disturbance disrupts an acacia ant–plant mutualism in favor of a subordinate ant species

Sensenig

Kimuyu

Guajardo

et al. 2017

Ecology

View full text Add to dashboard Cite

Although disturbance theory has been recognized as a useful framework in examining the stability of ant-plant mutualisms, very few studies have examined the effects of fire disturbance on these mutualisms. In myrmecophyte-dominated savannas, fire and herbivory are key drivers that could influence ant-plant mutualisms by causing complete colony mortality and/or decreasing colony size, which potentially could alter dominance hierarchies if subordinate species are more fire resilient. We used a large-scale, replicated fire experiment to examine long-term effects of fire on acacia-ant community composition. To determine if fire shifted ant occupancy from a competitive dominant to a subordinate ant species, we surveyed the acacia-ant community in 6-7 yr old burn sites and examined how the spatial scale of these burns influenced ant community responses. We then used two short-term fire experiments to explore possible mechanisms for the shifts in community patterns observed. Because survival of ant colonies is largely dependent on their ability to detect and escape an approaching fire, we first tested the evacuation response of all four ant species when exposed to smoke (fire signal). Then to better understand how fire and its interaction with large mammal herbivory affect the density of ants per tree, we quantified ant worker density in small prescribed burns within herbivore exclusion plots. We found clear evidence suggesting that fire disturbance favored the subordinate ant Crematogaster nigriceps more than the dominant and strong mutualist ant C. mimosae, whereby C. nigriceps (1) was the only species to occupy a greater proportion of trees in 6-7 yr old burn sites compared to unburned sites, (2) had higher burn/unburn tree ratios with increasing burn size, and (3) evacuated significantly faster than C. mimosae in the presence of smoke. Fire and herbivory had opposite effects on ant density per meter of branch for both C. nigriceps and C. mimosae, with fire decreasing ant densities per meter of branch and the presence of large herbivores increasing ant density. Taken together, these experiments suggest that major ecosystem disturbances like fire can disrupt mutualistic associations and maintain diversity in partner quality and identity despite a clear dominance hierarchy.

show abstract

“…B 281: 20140474 reduced folivory, influenced the evolution of this mutualism. Cordia alliodora is found throughout the neotropics, from Mexico to Argentina, and the quality of ant defence varies throughout this range [52]. Ants are particularly good defenders at the Chamela site studied here [11].…”

Section: Discussionmentioning

confidence: 80%

“…A question for future research is what factors restrict the distributions of these specialist bruchid seed predators, given that the range of their C. alliodora host tree extends virtually uninterrupted through the neotropics [33]. One important factor could be ambient climate, particularly precipitation in the tropical dry forests where the tree is common [52]. The timing and amount of precipitation determine the tree's reproductive phenology, which could have important consequences for reproductive isolation among species that interact with C. alliodora flowers and fruits.…”

Section: Discussionmentioning

confidence: 99%

Harnessing ant defence at fruits reduces bruchid seed predation in a symbiotic ant–plant mutualism

Pringle

2014

Proc. R. Soc. B.

Self Cite

View full text Add to dashboard Cite

In horizontally transmitted mutualisms, mutualists disperse separately and reassemble in each generation with partners genetically unrelated to those in the previous generation. Because of this, there should be no selection on either partner to enhance the other's reproductive output directly. In symbiotic ant-plant mutualisms, myrmecophytic plants host defensive ant colonies, and ants defend the plants from herbivores. Plants and ants disperse separately, and, although ant defence can indirectly increase plant reproduction by reducing folivory, it is unclear whether ants can also directly increase plant reproduction by defending seeds. The neotropical tree Cordia alliodora hosts colonies of Azteca pittieri ants. The trees produce domatia where ants nest at stem nodes and also at the node between the peduncle and the rachides of the infloresence. Unlike the stem domatia, these reproductive domatia senesce after the tree fruits each year. In this study, I show that the tree's resident ant colony moves into these ephemeral reproductive domatia, where they tend honeydew-producing scale insects and patrol the nearby developing fruits. The presence of ants significantly reduced pre-dispersal seed predation by Amblycerus bruchid beetles, thereby directly increasing plant reproductive output.

show abstract

Water Stress Strengthens Mutualism Among Ants, Trees, and Scale Insects

Abstract: When water is scarce, trees invest in the moderate carbon cost of supporting defensive ants to avoid the potentially high carbon cost of extremities being eaten.

Cited by 52 publications

References 49 publications

Influence of neighboring plants on the dynamics of an ant–acacia protection mutualism

Influence of neighboring plants on the dynamics of an ant–acacia protection mutualism

Fire disturbance disrupts an acacia ant–plant mutualism in favor of a subordinate ant species

Harnessing ant defence at fruits reduces bruchid seed predation in a symbiotic ant–plant mutualism

Contact Info

Product

Resources

About