skip to main content
Explore Scholarly Publications and Datasets in the NSF-PAR

This content will become publicly available on October 17, 2023

Title: Host plant phenology shapes aphid abundance and interactions with ants
Phenological mismatch can occur when plants and herbivores differentially respond to changing phenological cues, such as temperature or snow melt date. This often shifts herbivore feeding to plant stages of lower quality. How herbivores respond to plant quality may be also mediated by temperature, which could lead to temperature-by-phenology interactions. We examined how aphid abundance and mutualism with ants were impacted by temperature and host plant phenology. In this study system, aphids Aphis asclepiadis colonize flowering stalks of the host plant, Ligusticum porteri. Like other aphids, abundance of this species is dependent on ant protection. To understand how host plant phenology and temperature affect aphid abundance, we used a multiyear observational study and a field experiment. We observed 20 host plant populations over five years (2017–2021), tracking temperature and snow melt date as well as host plant phenology and insect abundance. We found host plant and aphid phenology to differentially respond to temperature and snow melt timing. Early snow melt accelerated host plant phenology to a greater extent than aphid phenology, which was more responsive to temperature. Both the likelihood of aphid colony establishment and ant recruitment were reduced when aphids colonized host plants at post-flowering stages. In 2019, we more » experimentally accelerated host plant phenology by advancing snow melt date by two weeks. We factorially combined this treatment with open top warming chambers surrounding aphid colonies. Greatest growth occurred for colonies under ambient temperatures when they occurred on host plants at the flowering stage. Altogether, our results suggest that phenological mismatch with host plants can decrease aphid abundance, and this effect is exacerbated by temperature increases and changes to the ant–aphid mutualism. « less
Authors:
; ; ; ; ;
Award ID(s):
1655914
Publication Date:
NSF-PAR ID:
10379663
Journal Name:
Oikos
ISSN:
0030-1299
Sponsoring Org:
National Science Foundation
More Like this
  1. ; ; ; ; ; ; ( , Entomologia Experimentalis et Applicata)
    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 tendingmore »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.

    « less
  2. ; ; ; ; ; ; ; ( , Arthropod-Plant Interactions)
    Abstract Declining snow cover is reshaping ecological communities. Early loss of snow cover initiates changes in key interactions that mediate herbivore abundance, i.e., top-down and bottom-up effects. In this study, we used a field experiment to test the effects of host plant water stress and phenology on the multitrophic interactions that determine aphid abundance. The aphid, Aphis asclepiadis , in our study system colonizes the flowering stalks of the host plant Ligusticum porteri and relies on a protection mutualism with ants. We added snow and water to replicate host plants and tested for a variety of phenological and physiological responses to these treatments. Relative to host plants in ambient conditions, both water and snow addition reduced key signals of water stress (senescence and abscisic acid levels) and increased seed set. While aphid colonies were generally larger with reduced host plant water stress, the ant–aphid mutualism interacted with plant quality in complex ways. Without ant tending, we did not detect differences in aphid colony growth with host plant treatment. When tended by ants, aphid colony growth was greatest on host plants with snow addition. Host plant quality also altered the benefits exchanged in this mutualism. Ant-tended colonies hosted by plants withmore »snow addition produced honeydew enriched in trehalose, which may have decreased both ant and natural enemy abundance. Our results suggest that early loss of snow reduces aphid abundance by creating low-quality, water-stressed host plants, and this effect may be exacerbated by natural enemies and the costs of ant attendance.« less
  3. ; ; ; ; ( , Journal of Animal Ecology)
    Abstract

    The abiotic environment drives species abundances and distributions both directly and indirectly through effects on multi‐trophic species interactions. However, few studies have documented the individual and combined consequences of these direct and indirect effects.

    We studied an ant‐tended aphid along an elevational gradient, where lower elevations were more arid. Hypotheses of stronger species interactions at lower elevations and a greater sensitivity of higher trophic levels to climate led us to predict increased top‐down control of aphids by natural enemies (third trophic level) but even stronger protection from mutualist ants (fourth trophic level) with increasing aridity. As a result, we predicted that mutualism strength and aphid abundance would increase with aridity.

    We documented patterns of aphid abundance and tested for both the direct and multi‐trophic indirect effects of aridity on aphid performance. To do so, we used both observational and manipulative methods across two years in replicate high‐ and low‐elevation valleys, where summer temperatures decreased by 3.7°C and precipitation increased by 27 mm/mo from low to high elevations.

    Aphid colonies were 75% larger in the most (vs. least) arid sites, and this was best explained by changes in interactions with predators and ants. Aphids were unaffected by the direct effects of the abiotic environmentmore »or its indirect effects via host plant quality. In contrast, natural enemy effects increased with aridity; under ant exclusion, natural enemies had no effect on aphids in the least arid sites but depressed colony growth by 252% in the most arid sites. Ant activity also increased with aridity, with ants discovering more aphid colonies and experimental baits and allocating more foragers per aphid, although there was no effect of aridity on ant abundance or community composition. Correspondingly, the mutualist services provided by ants increased with aridity; ants provided no benefits to aphids in the least arid sites but doubled colony growth in the most arid sites.

    In summary, an elevational cline in herbivore abundance was driven by a monotonic increase in trophic‐level sensitivity to aridity. These findings illustrate that predicting species responses to climate change will require a multi‐trophic perspective.

    « less
  4. ; ; ; ( , Scientific Reports)
    Abstract

    A holistic understanding of superorganism biology requires study of colony sociometry, or the quantitative relationships among growth, nest architecture, morphology, and behavior. For ant colonies that obligately nest within plant hosts, their sociometry is likely intertwined with the plant, which has implications for the evolution, strength, and stability of the mutualism. In theAzteca-Cecropiamutualism, plants provide ants with food rewards and hollow stems for nesting in return for protection from herbivores. Several interesting questions arise when considering ant-plant sociometry: are colony growth and plant growth synchronized? How do colonies distribute themselves within the stem of their host plant? How do plant traits influence worker morphology? How is collective personality related to tree structure, nest organization, and worker morphology? To address these questions, we investigated patterns within and relationships among five major sociometric categories of colonies in the field – plant traits, colony size, nest organization, worker morphology, and collective personality. We found that colony sociometry was intimately intertwined with host plant traits. Colony and plant growth rates were synchronized, suggesting that positive feedback between plant and colony growth stabilizes the mutualism. The colony’s distribution inside the host tree tended to follow leaf growth, with most workers, brood, and the queenmore »in the top half of the tree. Worker morphology correlated with plant size instead of colony size or age, which suggests that plant traits influence worker development. Colony personality was independent of colony distribution and tree structure but may correlate with worker size such that colonies with smaller, less variable workers had more aggressive personalities. This study provides insights into how ant-plant structural relationships may contribute to plant protection and the strength of mutualisms.

    « less
  5. ; ; ; ; ; ; ( , Ecology and Evolution)
    Abstract

    Several studies have demonstrated the ecological consequences of genetic variation within a single plant species. For example, these studies show that individual plant genotypes support unique composition of the plants' associated arthropod community. By contrast, fewer studies have explored how plant genetic variation may influence evolutionary dynamics in the plant's associated species. Here, we examine how aphids respond evolutionarily to genetic variation in their host plant. We conducted two experiments to examine local adaptation and rapid evolution of the free‐feeding aphidChaitophorus populicolaacross genetic variants of its host plant,Populus angustifolia. To test for local adaptation, we collected tree cuttings and aphid colonies from three sites along an elevation/climate gradient and conducted a reciprocal transplant experiment. In general, home aphids (aphids transplanted onto trees from the same site) produced 1.7–3.4 times as many offspring as foreign aphids (aphids transplanted onto trees from different sites). To test for rapid evolution, we used 4 clonally replicated aphid genotypes and transplanted each onto 5 clonally replicatedP. angustifoliagenotypes. Each tree genotype started with the same aphid genotype composition. After 21 days (~two aphid generations), aphid genotype composition changed (i.e., aphids evolved) and some tree genotypes supported unique evolutionary trajectories of aphids. These results suggest that plant evolutionmore »in response to human perturbation, such as climate change and invasive species, will also result in evolutionary responses in strongly interacting species that could cascade to affect whole communities.

    « less
  • Citation Formats
  • MLA
  • APA
  • Chicago
  • BibTeX
  • Save / Share this Record
  • Send to Email