An official website of the United States government
Abstract Over 125 million years of ant-plant interactions have culminated in one of the most intriguing evolutionary outcomes in life history. The myrmecophyteDuroia hirsuta(Rubiaceae) is known for its mutualistic association with the antMyrmelachista schumanniand several other species, mainlyAzteca, in the north-western Amazon. While both ants provide indirect defences to plants, onlyM. schumanninests in plant domatia and has the unique behaviour of clearing the surroundings of its host tree from heterospecific plants, potentially increasing resource availability to its host. Using a 12-year survey, we asked how the continuous presence of either onlyM. schumannior onlyAztecaspp. benefits the growth and defence traits of host trees. We found that the continuous presence ofM. schumanniimproved relative growth rates and leaf shearing resistance ofDuroiabetter than trees withAzteca. However, leaf herbivory, dry matter content, trichome density, and secondary metabolite production were the same in all trees. Survival depended directly on ant association (> 94% of trees died when ants were absent). This study extends our understanding of the long-term effects of strict ant-plant mutualism on host plant traits in the field and reinforces the use ofD. hirsuta–M. schumannias a model system suitable for eco-co-evolutionary research on plant–animal interactions.
more »
« less
Symbiotic ant traits produce differential host‐plant carbon and water dynamics in a multi‐species mutualism
Abstract 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.
more »
« less
- PAR ID:
- 10383246
- Publisher / Repository:
- Wiley Blackwell (John Wiley & Sons)
- Date Published:
- Journal Name:
- Ecology
- Volume:
- 104
- Issue:
- 1
- ISSN:
- 0012-9658
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract Ant‐hemipteran mutualisms are keystone interactions that can be variously affected by warming: these mutualisms can be strengthened or weakened, or the species can transition to new mutualist partners. We examined the effects of elevated temperatures on an ant‐aphid mutualism in the subalpine zone of the Rocky Mountains in Colorado, USA. In this system, inflorescences of the host plant,Ligusticum porteriCoult. & Rose (Apiaceae), are colonized by the ant‐tended aphidAphis asclepiadisFitch or less frequently by the non‐ant tended aphidCavariella aegopodii(Scopoli) (both Hemiptera: Aphididae). Using an 8‐year observational study, we tested for two key mechanisms by which ant‐hemipteran mutualisms may be altered by climate change: shifts in species identity and phenological mismatch. Whereas the aphid species colonizing the host plant is not changing in response to year‐to‐year variation in temperature, we found evidence that a phenological mismatch between ants and aphids could occur. In warmer years, colonization of host plant inflorescences by ants is decreased, whereas forA. asclepiadisaphids, host plant colonization is mostly responsive to date of snowmelt. We also experimentally establishedA. asclepiadiscolonies on replicate host plants at ambient and elevated temperatures. Ant abundance did not differ between aphid colonies at ambient vs. elevated temperatures, but ants were less likely to engage in tending behaviors on aphid colonies at elevated temperatures. Sugar composition of aphid honeydew was also altered by experimental warming. Despite reduced tending by ants, aphid colonies at elevated temperatures had fewer intraguild predators. Altogether, our results suggest that higher temperatures may disrupt this ant‐aphid mutualism through both phenological mismatch and by altering benefits exchanged in the interaction.more » « less
-
Abstract 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.more » « less
-
Abstract Mutualism benefits partner species, and theory predicts these partnerships can affect the abundance, diversity, and composition of partner and non‐partner species. We used 16 years of monitoring data to determine the ant partner species of tree cholla cacti (Cylindropuntia imbricata), which reward ants with extrafloral nectar in exchange for anti‐herbivore defense. These long‐term data revealed one dominant ant partner (Liometopum apiculatum) and two less common partners (Crematogaster opuntiaeandForelius pruinosus). We then used short‐term characterization of the terrestrial ant community by pitfall trapping to sample partner and non‐partner ant species across ten plots of varying cactus density. We found that the dominant ant partner tended a higher proportion cacti in plots of higher cactus density, and was also found at higher occurrence within the pitfall traps in higher density plots, suggesting a strong positive feedback that promotes ant partner occurrence where plant partners are available. Despite the strong association and increased partner occurrence, ant community‐wide effects from this mutualism appear limited. Of the common ant species, the occurrence of a single non‐partner ant species was negatively associated with cactus density and with the increased presence ofL. apiculatum. Additionally, the composition and diversity of the ant community in our plots were insensitive to cactus density variation, indicating that positive effects of the mutualism on the dominant ant partner did not have cascading impacts on the ant community. This study provides novel evidence that exclusive mutualisms, even those with a strong positive feedback, may be limited in the scope of their community‐level effects.more » « less
-
Tree carbon allocation is a dynamic process that depends on the tree’s environment, but we know relatively little about how biotic interactions influence these dynamics. In central Kenya, the loss of vertebrate herbivores and the savanna’s invasion by the ant Pheidole megacephala are disrupting mutualisms between the foundational tree Acacia (Vachellia) drepanolobium and its native ant defenders. Here, we piloted a 13Carbon (C) pulse-labeling method to investigate the influence of these biotic interactions on C allocation to ant partners by adult trees in situ. Trees withstood experimental conditions and took up sufficient labeled 13CO2 for 13C to be detected in various C sinks, including ant mutualists. The δ13C in ants collected shortly after labeling suggested that trees exposed to herbivores allocated relatively more newly assimilated C to native ant defenders. Our results demonstrate the viability of the pulse-labeling method and suggest that C allocation to ant partners depends on the biotic context of the tree, but further investigation with replication is needed to characterize such differences in relation to invasion and herbivore loss.more » « less
