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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. 

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. 

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.