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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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Neutrality in plant–herbivore interactions
Understanding the distribution of herbivore damage among leaves and individual plants is a central goal of plant–herbivore biology. Commonly observed unequal patterns of herbivore damage have conventionally been attributed to the heterogeneity in plant quality or herbivore behaviour or distribution. Meanwhile, the potential role of stochastic processes in structuring plant–herbivore interactions has been overlooked. Here, we show that based on simple first principle expectations from metabolic theory, random sampling of different sizes of herbivores from a regional pool is sufficient to explain patterns of variation in herbivore damage. This is despite making the neutral assumption that herbivory is caused by randomly feeding herbivores on identical and passive plants. We then compared its predictions against 765 datasets of herbivory on 496 species across 116° of latitude from the Herbivory Variability Network. Using only one free parameter, the estimated attack rate, our neutral model approximates the observed frequency distribution of herbivore damage among plants and especially among leaves very well. Our results suggest that neutral stochastic processes play a large and underappreciated role in natural variation in herbivory and may explain the low predictability of herbivory patterns. We argue that such prominence warrants its consideration as a powerful force in plant–herbivore interactions.
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- Award ID(s):
- 2409605
- PAR ID:
- 10554614
- Publisher / Repository:
- The Royal Society
- Date Published:
- Journal Name:
- Proceedings of the Royal Society B: Biological Sciences
- Volume:
- 291
- Issue:
- 2017
- ISSN:
- 0962-8452
- Page Range / eLocation ID:
- 20232687
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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PREMISE Quantifying how closely related plant species differ in susceptibility to insect herbivory is important for our understanding of variation in plant-insect ecological interactions and evolutionary pressures on plant functional traits. However, empirically measuring in situ variation in herbivory over the entire geographic range where a plant-insect complex occurs is logistically difficult. Recently, new methods have been developed to use herbarium specimens to investigate patterns in plant-insect interactions across geographic areas, and during periods of accelerating anthropogenic change. Such investigations can provide insights into changes in herbivory intensity and phenology in plants that are of ecological and agricultural importance. METHODS Here, we analyze 274 pressed herbarium samples from all 14 species in the economically important plant genus Cucurbita (Cucurbitaceae) to investigate variation in herbivory damage. This collection is comprised of specimens of wild, undomesticated Cucurbita that were collected from across their native range in the Neotropics and subtropics, and Cucurbita cultivars that were collected from both within their native range and from locations where they have been introduced for agriculture in temperate Eastern North America. RESULTS We find that herbivory is common on individuals of all Cucurbita species collected from throughout their geographic ranges; however, estimates of herbivory varied considerably among individuals, with greater damage observed in specimens collected from unmanaged habitat. We also find evidence that mesophytic species accrue more insect damage than xerophytic species. CONCLUSIONS Our study demonstrates that herbarium specimens are a useful resource for understanding ecological interactions between domesticated crop plants and co-evolved insect herbivores.more » « less
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PREMISE Quantifying how closely related plant species differ in susceptibility to insect herbivory is important for our understanding of variation in plant-insect ecological interactions and evolutionary pressures on plant functional traits. However, empirically measuring in situ variation in herbivory over the entire geographic range where a plant-insect complex occurs is logistically difficult. Recently, new methods have been developed to use herbarium specimens to investigate patterns in plant-insect interactions across geographic areas, and during periods of accelerating anthropogenic change. Such investigations can provide insights into changes in herbivory intensity and phenology in plants that are of ecological and agricultural importance. METHODS Here, we analyze 274 pressed herbarium samples from all 14 species in the economically important plant genus Cucurbita (Cucurbitaceae) to investigate variation in herbivory damage. This collection is comprised of specimens of wild, undomesticated Cucurbita that were collected from across their native range in the Neotropics and subtropics, and Cucurbita cultivars that were collected from both within their native range and from locations where they have been introduced for agriculture in temperate Eastern North America. RESULTS We find that herbivory is common on individuals of all Cucurbita species collected from throughout their geographic ranges; however, estimates of herbivory varied considerably among individuals, with greater damage observed in specimens collected from unmanaged habitat. We also find evidence that mesophytic species accrue more insect damage than xerophytic species. CONCLUSIONS Our study demonstrates that herbarium specimens are a useful resource for understanding ecological interactions between domesticated crop plants and co-evolved insect herbivores.more » « less
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1098/rspb.2023.2687
