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 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.
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Elevated temperatures alter an ant‐aphid mutualism
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,
- Award ID(s):
- 1655914
- NSF-PAR ID:
- 10457064
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Entomologia Experimentalis et Applicata
- Volume:
- 167
- Issue:
- 10
- ISSN:
- 0013-8703
- Page Range / eLocation ID:
- p. 891-905
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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null (Ed.)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 with 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.more » « less
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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 environment 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.
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