Insect mutualisms buffer warming effects on multiple trophic levels

Marquis, Michael; Toro, Israel Del; Pelini, Shannon L.

doi:10.1890/13-0760.1

Cited by 30 publications

(31 citation statements)

References 25 publications

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“…In open-top warming experiments, populations of the aphid, Chaitophorus populicola, were higher when tended by mutualistic ants, regardless of temperature [139]. In their study, plant stress decreased with warming only when both ants and C. populicola aphids were associated in mutualistic Other guilds Temperate S. Korea Beetles Effect of temperature on communities [143] interactions, suggesting that such interspecific interactions could buffer the effects of warming on herbivore communities.…”

Section: Other Guildsmentioning

confidence: 90%

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Forest Insects and Climate Change

Roques²,

2018

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Purpose of Review Climate change affects populations of forest insect pests in a number of ways. We reviewed the most recent literature (2013-2017) on this subject including previous reviews on the topic. We provide a comprehensive discussion of the subject, with special attention to insect range expansion, insect abundance, impacts on forest ecosystems, and effects on forest insect communities. We considered forest insects according to their major guilds and biomes. Recent Findings Effects of climate change on forest insects are demonstrated for a number of species and guilds, although generalizations of results available so far are difficult because of species-specific responses to climate change. In addition, disentangling direct and indirect effects of climate change is complex due to the large number of variables affected. Modeling based on climate projections is useful when combined with mechanistic explanations. Summary Expansion of either the true range or the outbreak range is observed in several model species/groups of major insect guilds in boreal and temperate biomes. Mechanistic explanations are provided for a few species and are mainly based on increase in winter temperatures. In relation to insect abundance, climate change can either promote outbreaks or disrupt trophic interactions and decrease the severity of outbreaks. There is good evidence that some recent outbreaks of bark beetles and defoliating insects are influenced by climate change and are having a large impact on ecosystems as well as on communities of forest insects.

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Section: Other Guildsmentioning

confidence: 90%

“…Even though populations increased over this period, per capita rates of change were negatively associated with climate change variables in time series models. It appears that negative effects of climate change on population growth can be buffered by other ecological factors [135,139].…”

Section: Defoliatorsmentioning

confidence: 99%

Forest Insects and Climate Change

Roques²,

2018

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“…In other work along the same elevational gradient, we found that natural enemy abundance and top‐down control of aphids ( A. varians feeding on C. angustifolium ) were greater at low elevations (Nelson, Pratt, et al, ). Predation and parasitism by invertebrates are often stronger at lower elevations (Roslin et al, ; Sam et al, ; Straw et al, ), and experimental warming has been found to directly affect the abundance of predators of other aphids ( Chaitophorus populicola ) feeding on aspen (Marquis, Del Toro, & Pelini, ). It is possible that natural enemy abundance also increased with aridity in our system, but we may not have detected such patterns because many flying natural enemies (e.g., parasitoid wasps) spend only brief amounts of time at aphid colonies.…”

Section: Discussionmentioning

confidence: 99%

Elevational cline in herbivore abundance driven by a monotonic increase in trophic‐level sensitivity to aridity

Nelson

Symanski

Hecking

et al. 2019

Journal of Animal Ecology

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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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“…Usually, elevated temperature increases insect overwintering, damage magnitude and range expansion 10 . Besides, climate change may significantly modify the dynamic interactions between plants and insects 11 . Temperature increase may facilitate the growth of herbivores through restraining the concentrations of several phenolic compounds in plant leaves 12 .…”

Section: Introductionmentioning

confidence: 99%

Temperature warming strengthens the mutualism between ghost ants and invasive mealybugs

Zhou

Shan

et al. 2017

Sci Rep

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Although the exogenous forces that directly affect the mutualisms between ants and honeydew-producing hemipterans have been well documented, few studies have been focused on the impacts of environmental warming on ant-hemipteran interactions. Here, we investigated how temperature warming affects the mutualism between ghost ant Tapinoma melanocephalum and invasive mealybug Phenacoccus solenopsis by experimental manipulation of temperature. We found that higher temperatures have significant direct effects on the growth rate of mealybug colony, and the positive effect of ant tending on mealybug colony growth is temperature-dependent. Honeydew excretion by mealybugs was affected by ant tending and temperature warming, and was significantly increased under higher temperature. The effect of ant tending on percentage parasitism was also influenced by temperature warming. Ant performance including tending level, aggression, activity, and honeydew consumption was enhanced by temperature warming, which may provide superior protection to the mealybugs. Our results show that ghost ant-mealybug mutualism is strengthened in a warmer environment. These findings may facilitate the prediction of how each partner in the ant-hemipteran-enemy interactions responds to increasing temperature.

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Insect mutualisms buffer warming effects on multiple trophic levels

Cited by 30 publications

References 25 publications

Forest Insects and Climate Change

Forest Insects and Climate Change

Elevational cline in herbivore abundance driven by a monotonic increase in trophic‐level sensitivity to aridity

Temperature warming strengthens the mutualism between ghost ants and invasive mealybugs

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