1. Predicting how ecological interactions will respond to global change is a major challenge. Plants and their associated insect herbivores compose much of macroscopic diversity, yet how their interactions have been altered by recent environmental change remains underexplored.
2. To address this gap, we quantified herbivory on herbarium specimens of four plant species with records extending back 112 years. Our study focused on the northeastern US, where temperatures have increased rapidly over the last few decades. This region also represents a range of urban development, a form of global change that has shown variable effects on herbivores in the past studies.
3. Herbarium specimens collected in the early 2000s were 23% more likely to be damaged by herbivores than those collected in the early 1900s. Herbivory was greater following warmer winters and at low latitudes, suggesting that climate warming may drive increasing insect damage over time. In contrast, human population densities were negatively associated with herbivore damage.
4. To explore whether changes in insect occurrence or abundance might explain shifts in herbivory, we used insect observational records to build climate occupancy models for lepidopteran herbivores (butterflies and moths) of our focal plant species.
5. These models show that higher winter temperatures were associated with higher probability of insect herbivore presence, while urbanization was associated with reduced probability of herbivore presence, supporting a link between insect herbivore occurrence and herbivory mediated through environment.
6. Synthesis. Using a temporal record of plant herbivory that spans over a century, we show that both temperature and urbanization influence insect damage to plants, but in very different ways. Our results indicate that damage to plants by insect herbivores will likely continue to increase through time in the northeastern US as global temperatures rise, but that urbanization may disrupt local effects of winter warming on herbivory by excluding certain herbivores. These changes may scale to shape ecosystem processes that are driven by herbivory, including plant productivity.
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Climate change alters plant–herbivore interactions
Plant–herbivore interactions have evolved in response to coevolutionary dynamics, along with selection driven by abiotic conditions. We examine how abiotic factors influence trait expression in both plants and herbivores to evaluate how climate change will alter this long‐standing interaction. The paleontological record documents increased herbivory during periods of global warming in the deep past. In phylogenetically corrected meta‐analyses, we find that elevated temperatures, CO2concentrations, drought stress and nutrient conditions directly and indirectly induce greater food consumption by herbivores. Additionally, elevated CO2delays herbivore development, but increased temperatures accelerate development. For annual plants, higher temperatures, CO2and drought stress increase foliar herbivory. Our meta‐analysis also suggests that greater temperatures and drought may heighten florivory in perennials. Human actions are causing concurrent shifts in CO2, temperature, precipitation regimes and nitrogen deposition, yet few studies evaluate interactions among these changing conditions. We call for additional multifactorial studies that simultaneously manipulate multiple climatic factors, which will enable us to generate more robust predictions of how climate change could disrupt plant–herbivore interactions. Finally, we consider how shifts in insect and plant phenology and distribution patterns could lead to ecological mismatches, and how these changes may drive future adaptation and coevolution between interacting species.
more » « less- Award ID(s):
- 1655732
- NSF-PAR ID:
- 10452581
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- New Phytologist
- Volume:
- 229
- Issue:
- 4
- ISSN:
- 0028-646X
- Page Range / eLocation ID:
- p. 1894-1910
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Global climate change and shifting land‐use are increasing plant stress due to abiotic factors such as drought, heat, salinity and cold, as well as via the intensification of biotic stressors such as herbivores and pathogens. The ability of plants to tolerate such stresses is modulated by the bacteria and fungi that live on or inside of plant tissues and comprise the plant microbiome. However, the impacts of diverse classes of beneficial members of the microbiome and the contrasting stresses that impact plants are most commonly studied independently of each other.
Our meta‐analysis of 288 experiments across 89 studies moves beyond previous studies in that we simultaneously compare the roles of bacterial versus fungal microbiome members that live within plant tissues and colonize plant surfaces in ameliorating biotic versus abiotic sources of plant stress.
The magnitude of microbial stress amelioration can be measured as the greater proportional impact of beneficial microbes on plant performance in more stressful environments. In the plant experiments we examine, the magnitude of microbial stress amelioration is substantial: it is 23% of the effect size of the typical impact of stress and 56% of the effect size of beneficial microbiome members in the absence of stress.
The amount of benefit microbiome members confer to plants differs among classes of microbes, depending on whether plants are grown in stressful or non‐stressful environments. In the absence of stress, beneficial bacteria tend to confer greater plant benefits than do fungi. However, symbiotic fungi, especially arbuscular mycorrhizal fungi, more strongly ameliorate plant stress than do bacteria. In particular, beneficial microbes ameliorate salinity, foliar herbivory and fungal pathogen stress.
These results highlight the fact that the impacts of beneficial and antagonistic components of the microbiome on plant performance depend on biotic and abiotic environmental contexts. Furthermore, beneficial microbes are especially critical for plant health in stressful environments and thus present opportunities to mitigate negative consequences of global change.
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BACKGROUND The availability of nitrogen (N) to plants and microbes has a major influence on the structure and function of ecosystems. Because N is an essential component of plant proteins, low N availability constrains the growth of plants and herbivores. To increase N availability, humans apply large amounts of fertilizer to agricultural systems. Losses from these systems, combined with atmospheric deposition of fossil fuel combustion products, introduce copious quantities of reactive N into ecosystems. The negative consequences of these anthropogenic N inputs—such as ecosystem eutrophication and reductions in terrestrial and aquatic biodiversity—are well documented. Yet although N availability is increasing in many locations, reactive N inputs are not evenly distributed globally. Furthermore, experiments and theory also suggest that global change factors such as elevated atmospheric CO 2 , rising temperatures, and altered precipitation and disturbance regimes can reduce the availability of N to plants and microbes in many terrestrial ecosystems. This can occur through increases in biotic demand for N or reductions in its supply to organisms. Reductions in N availability can be observed via several metrics, including lowered nitrogen concentrations ([N]) and isotope ratios (δ 15 N) in plant tissue, reduced rates of N mineralization, and reduced terrestrial N export to aquatic systems. However, a comprehensive synthesis of N availability metrics, outside of experimental settings and capable of revealing large-scale trends, has not yet been carried out. ADVANCES A growing body of observations confirms that N availability is declining in many nonagricultural ecosystems worldwide. Studies have demonstrated declining wood δ 15 N in forests across the continental US, declining foliar [N] in European forests, declining foliar [N] and δ 15 N in North American grasslands, and declining [N] in pollen from the US and southern Canada. This evidence is consistent with observed global-scale declines in foliar δ 15 N and [N] since 1980. Long-term monitoring of soil-based N availability indicators in unmanipulated systems is rare. However, forest studies in the northeast US have demonstrated decades-long decreases in soil N cycling and N exports to air and water, even in the face of elevated atmospheric N deposition. Collectively, these studies suggest a sustained decline in N availability across a range of terrestrial ecosystems, dating at least as far back as the early 20th century. Elevated atmospheric CO 2 levels are likely a main driver of declines in N availability. Terrestrial plants are now uniformly exposed to ~50% more of this essential resource than they were just 150 years ago, and experimentally exposing plants to elevated CO 2 often reduces foliar [N] as well as plant-available soil N. In addition, globally-rising temperatures may raise soil N supply in some systems but may also increase N losses and lead to lower foliar [N]. Changes in other ecosystem drivers—such as local climate patterns, N deposition rates, and disturbance regimes—individually affect smaller areas but may have important cumulative effects on global N availability. OUTLOOK Given the importance of N to ecosystem functioning, a decline in available N is likely to have far-reaching consequences. Reduced N availability likely constrains the response of plants to elevated CO 2 and the ability of ecosystems to sequester carbon. Because herbivore growth and reproduction scale with protein intake, declining foliar [N] may be contributing to widely reported declines in insect populations and may be negatively affecting the growth of grazing livestock and herbivorous wild mammals. Spatial and temporal patterns in N availability are not yet fully understood, particularly outside of Europe and North America. Developments in remote sensing, accompanied by additional historical reconstructions of N availability from tree rings, herbarium specimens, and sediments, will show how N availability trajectories vary among ecosystems. Such assessment and monitoring efforts need to be complemented by further experimental and theoretical investigations into the causes of declining N availability, its implications for global carbon sequestration, and how its effects propagate through food webs. Responses will need to involve reducing N demand via lowering atmospheric CO 2 concentrations, and/or increasing N supply. Successfully mitigating and adapting to declining N availability will require a broader understanding that this phenomenon is occurring alongside the more widely recognized issue of anthropogenic eutrophication. Intercalibration of isotopic records from leaves, tree rings, and lake sediments suggests that N availability in many terrestrial ecosystems has steadily declined since the beginning of the industrial era. Reductions in N availability may affect many aspects of ecosystem functioning, including carbon sequestration and herbivore nutrition. Shaded areas indicate 80% prediction intervals; marker size is proportional to the number of measurements in each annual mean. Isotope data: (tree ring) K. K. McLauchlan et al. , Sci. Rep. 7 , 7856 (2017); (lake sediment) G. W. Holtgrieve et al. , Science 334 , 1545–1548 (2011); (foliar) J. M. Craine et al. , Nat. Ecol. Evol. 2 , 1735–1744 (2018)more » « less
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Abstract The effects of climate change on plants and ecosystems are mediated by plant hydraulic traits, including interspecific and intraspecific variability of trait phenotypes. Yet, integrative and realistic studies of hydraulic traits and climate change are rare. In a semiarid grassland, we assessed the response of several plant hydraulic traits to elevated CO2(+200 ppm) and warming (+1.5 to 3°C; day to night). For leaves of five dominant species (three graminoids and two forbs), and in replicated plots exposed to 7 years of elevated CO2, warming, or ambient climate, we measured: stomatal density and size, xylem vessel size, turgor loss point, and water potential (pre‐dawn). Interspecific differences in hydraulic traits were larger than intraspecific shifts induced by elevated CO2and/or warming. Effects of elevated CO2were greater than effects of warming, and interactions between treatments were weak or not detected. The forbs showed little phenotypic plasticity. The graminoids had leaf water potentials and turgor loss points that were 10% to 50% less negative under elevated CO2; thus, climate change might cause these species to adjust their drought resistance strategy away from tolerance and toward avoidance. The C4 grass also reduced allocation of leaf area to stomata under elevated CO2, which helps explain observations of higher soil moisture. The shifts in hydraulic traits under elevated CO2were not, however, simply due to higher soil moisture. Integration of our results with others' indicates that common species in this grassland are more likely to adjust stomatal aperture in response to near‐term climate change, rather than anatomical traits; this contrasts with apparent effects of changing CO2on plant anatomy over evolutionary time. Future studies should assess how plant responses to drought may be constrained by the apparent shift from tolerance (via low turgor loss point) to avoidance (via stomatal regulation and/or access to deeper soil moisture).
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ABSTRACT Background Echium plantagineum , a native of Europe and Africa, is a noxious invasive weed in Australia forming monocultural stands in pastures and rangelands. It produces a complex mixture of bioactive secondary metabolites, including toxic pyrrolizidine alkaloids (PAs), that protect the plant from insect and livestock herbivory and naphthoquinones (NQs), which suppress competition from weeds, insects and pathogens, and also influence invasion success. However, the extent to which allelochemical production is impacted by environmental factors, thereby influencing plant defense against pests, remains unclear.Results Following plant stress induced by drought, herbivory and high temperature, extracts of
E. plantagineum shoots and roots were subjected to metabolic profiling by UPLC‐MS‐DAD‐ QToF mass spectrometry. Abundance of NQs, especially deoxyshikonin, shikonin and dimethylacrylshikonin, rapidly increased in roots exposed to elevated temperatures. Water withholding initially increased NQ abundance, but prolonged drought resulted in reduced total PAs and NQs. Intraspecific competition elevated the production of NQs, whereas simulated herbivory had no initial effect on NQs. Following herbivory, the abundance of the PA 3′‐O ‐acetylechimidine‐N ‐oxide in seedling shoots was increased.Conclusions Differential accumulation of defense metabolites by
E. plantagineum following exposure to various stressors suggested stress‐dependent biosynthetic regulation, particularly with respect to NQ production, which was rapidly induced following drought, intraspecific competition and high temperature treatment, thereby positively impacting resistance or defense against herbivores, weeds and pathogens. We propose that trade‐offs between above‐ and below‐ground metabolism inE. plantagineum may facilitate allelochemical production in response to stress, rendering plants with an enhanced ability to defend against other neighboring plants, insects and microbes, with allelochemical production further facilitated by catabolic recycling following lengthier exposure to stress. © 2019 Society of Chemical Industry
