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1. Mutualism disruption by an invasive ant reduces carbon fixation for a foundational East African ant‐plant

   https://doi.org/10.1111/ele.13725  

   Milligan, Patrick D. ; Martin, Timothy A. ; John, Grace P. ; Riginos, Corinna ; Goheen, Jacob R. ; Carpenter, Scott M. ; Palmer, Todd M. ; Irwin, ed., Rebecca ( March 2021 , Ecology Letters)

   Invasive ants shape assemblages and interactions of native species, but their effect on fundamental ecological processes is poorly understood. In East Africa,Pheidole megacephalaants have invaded monodominant stands of the ant‐treeAcacia drepanolobium, extirpating native ant defenders and rendering trees vulnerable to canopy damage by vertebrate herbivores. We used experiments and observations to quantify direct and interactive effects of invasive ants and large herbivores onA. drepanolobiumphotosynthesis over a 2‐year period. Trees that had been invaded for ≥ 5 years exhibited 69% lower whole‐tree photosynthesis during key growing seasons, resulting from interaction between invasive ants and vertebrate herbivores that caused leaf‐ and canopy‐level photosynthesis declines. We also surveyed trees shortly before and after invasion, finding that recent invasion induced only minor changes in leaf physiology. Our results from individual trees likely scale up, highlighting the potential of invasive species to alter ecosystem‐level carbon fixation and other biogeochemical cycles.

    

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2. Symbiotic ant traits produce differential host‐plant carbon and water dynamics in a multi‐species mutualism

   https://doi.org/10.1002/ecy.3880  

   Milligan, Patrick D. ; Martin, Timothy A. ; Pringle, Elizabeth G. ; Prior, Kirsten M. ; Palmer, Todd M. ( November 2022 , Ecology)

   Cooperative interactions may frequently be reinforced by “partner fidelity feedback,” in which high‐ or low‐quality partners drive positive feedbacks with high or low benefits for the host, respectively. Benefits of plant–animal mutualisms for plants have been quantified almost universally in terms of growth or reproduction, but these are only two of many sinks to which a host‐plant allocates its resources. By investigating how partners to host‐plants impact two fundamental plant resources, carbon and water, we can better characterize plant–partner fidelity and understand how plant–partner mutualisms may be modulated by resource dynamics. In Laikipia, Kenya, four ant species compete forAcacia drepanolobiumhost‐plants. These ants differ in multiple traits, from nectar consumption to host‐plant protection. Using a 5‐year ant removal experiment, we compared carbon fixation, leaf water status, and stem non‐structural carbohydrate concentrations for adult ant–plants with and without ant partners. Removal treatments showed that the ants differentially mediate tree carbon and/or water resources. All three ant species known to be aggressive against herbivores were linked to benefits for host‐plant resources, but only the two species that defend but do not prune the host,Crematogaster mimosaeandTetraponera penzigi, increased tree carbon fixation. Of these two species, only the nectivoreC. mimosaeincreased tree simple sugars.Crematogaster nigriceps, which defends the tree but also castrates flowers and prunes meristems, was linked only to lower tree water stress approximated by pre‐dawn leaf water potential. In contrast to those defensive ants,Crematogaster sjostedti, a poor defender that displaces other ants, was linked to lower tree carbon fixation. Comparing the effects of the four ant species across control trees suggests that differential ant occupancy drives substantial differences in carbon and water supply among host trees. Our results highlight that ant partners can positively or negatively impact carbon and/or water relations for their host‐plant, and we discuss the likelihood that carbon‐ and water‐related partner fidelity feedback loops occur across ant–plant mutualisms.

    

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3. Drought impairs herbivore-induced volatile terpene emissions by ponderosa pine but not through constraints on newly assimilated carbon

   https://doi.org/10.1093/treephys/tpad016  

   Malone, Shealyn C. ; Simonpietri, Austin ; Knighton, Walter B. ; Trowbridge, Amy M. ; Schnitzler, ed., Jörg-Peter ( February 2023 , Tree Physiology)

   Volatile terpenes serve multiple biological roles including tree resistance against herbivores. The increased frequency and severity of drought stress observed in forests across the globe may hinder trees from producing defense-related volatiles in response to biotic stress. To assess how drought-induced physiological stress alters volatile emissions alone and in combination with a biotic challenge, we monitored pre-dawn water potential, gas-exchange, needle terpene concentrations and terpene volatile emissions of ponderosa pine (Pinus ponderosa) saplings during three periods of drought and in response to simulated herbivory via methyl jasmonate application. Although 3-, 6- and 7-week drought treatments reduced net photosynthetic rates by 20, 89 and 105%, respectively, the magnitude of volatile fluxes remained generally resistant to drought. Herbivore-induced emissions, however, exhibited threshold-like behavior; saplings were unable to induce emissions above constitutive levels when pre-dawn water potentials were below the approximate zero-assimilation point. By comparing compositional shifts in emissions to needle terpene concentrations, we found evidence that drought effects on constitutive and herbivore-induced volatile flux and composition are primarily via constraints on the de novo fraction, suggesting that reduced photosynthesis during drought limits the carbon substrate available for de novo volatile synthesis. However, results from a subsequent 13CO2 pulse-chase labeling experiment then confirmed that both constitutive (<3% labeled) and herbivore-induced (<8% labeled) de novo emissions from ponderosa pine are synthesized predominantly from older carbon sources with little contribution from new photosynthates. Taken together, we provide evidence that in ponderosa pine, drought does not constrain herbivore-induced de novo emissions through substrate limitation via reduced photosynthesis, but rather through more sophisticated molecular and/or biophysical mechanisms that manifest as saplings reach the zero-assimilation point. These results highlight the importance of considering drought severity when assessing impacts on the herbivore-induced response and suggest that drought-altered volatile metabolism constrains induced emissions once a physiological threshold is surpassed.

    

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4. A soil‐nesting invasive ant disrupts carbon dynamics in saplings of a foundational ant–plant

   https://doi.org/10.1111/1365-2745.13803  

   Milligan, Patrick D. ; Martin, Timothy A. ; Pringle, Elizabeth G. ; Riginos, Corinna ; Mizell, Gabriella M. ; Palmer, Todd M. ( November 2021 , Journal of Ecology)

   Nearly every terrestrial ecosystem hosts invasive ant species, and many of those ant species construct underground nests near roots and/or tend phloem‐feeding hemipterans on plants. We have a limited understanding of how these invasive ant behaviours change photosynthesis, carbohydrate availability and growth of woody plants.

   We measured photosynthesis, water relations, carbohydrate concentrations and growth for screenhouse‐rearedAcacia drepanolobiumsaplings on which we had manipulated invasivePheidole megacephalaants and nativeCeroplastessp. hemipterans to determine whether and how soil nesting and hemipteran tending by ants affect plant carbon dynamics. In a field study, we also compared leaf counts of vertebrate herbivore‐excluded and ‐exposed saplings in invaded and non‐invaded savannas to examine how ant invasion and vertebrate herbivory are associated with differences in sapling photosynthetic crown size.

   Though hemipteran infestations are often linked to declines in plant performance, our screenhouse experiment did not find an association between hemipteran presence and differences in plant physiology. However, we did find that soil nesting byP. megacephalaaround screenhouse plants was associated with >58% lower whole‐crown photosynthesis, >31% lower pre‐dawn leaf water potential, >29% lower sucrose concentrations in woody tissues and >29% smaller leaf areas. In the field, sapling crowns were 29% smaller in invaded savannas than in non‐invaded savannas, mimicking screenhouse results.

   Synthesis. We demonstrate that soil nesting near roots, a common behaviour byPheidole megacephalaand other invasive ants, can directly reduce carbon fixation and storage ofAcacia drepanolobiumsaplings. This mechanism is distinct from the disruption of a native ant mutualism byP. megacephala, which causes similar large declines in carbon fixation for matureA. drepanolobiumtrees.Acacia drepanolobiumalready has extremely low natural rates of recruitment from the sapling to mature stage, and we infer that these negative effects of invasion on saplings potentially curtail recruitment and reduce population growth in invaded areas. Our results suggest that direct interactions between invasive ants and plant roots in other ecosystems may strongly influence plant carbon fixation and storage.

    

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5. Mutualisms in a warming world: How increased temperatures affect the outcomes of multi‐mutualist interactions

   https://doi.org/10.1002/ecy.3955  

   Magnoli, Susan M. ; Keller, Kane R. ; Lau, Jennifer A. ( January 2023 , Ecology)

   In nature, plant species simultaneously interact with many different mutualistic partners. These mutualists may influence one another through direct interference or indirectly by competing for shared reward resources or through alteration of plant traits. Together, these mutualists also may combine to affect plant hosts in ways that may not be predictable based on pairwise interactions. Given that the outcome of mutualistic interactions often depends on environmental conditions, multi‐mutualist effects on one another, and their plant hosts may be affected by global changes. Here, we grew focal plants under simulated global warming conditions and manipulated the presence of partner mutualists to test how warming affects the outcome of interactions between focal plants and their partners (nitrogen‐fixing rhizobia, ant defenders, and pollinators) and interactions among these partner mutualists. We find that warming alters the fitness benefits plants receive from rhizobium resource mutualists but not ant mutualists and that warming altered plant investment in all mutualists. We also find that mutualist partners interact, often by altering the availability of plant‐produced rewards that facilitate interactions with other partners. Our work illustrates that global changes may affect some but not all mutualisms, often asymmetrically (e.g., affecting investment in the mutualist partner but not plant host benefits) and also highlights the ubiquity of interactions between the multiple mutualists associating with a shared host.

    

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