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1. Herbarium specimens reveal herbivory patterns across the genus Cucurbita

   https://doi.org/2021.2007.2021.452357  

   Jenny, L.A.; Shapiro, L.R.; Davis, C.C.; Davies, T.J.; Pierce, N.E.; Meineke, E. (July 2021, bioRxiv)

   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. 

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2. Herbarium specimens reveal increasing herbivory over the past century

   https://doi.org/10.1111/1365-2745.13057  

   Meineke, Emily K.; Classen, Aimée T.; Sanders, Nathan J.; Jonathan Davies, T. (September 2018, Journal of Ecology)

   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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3. Phenological sensitivity to temperature mediates herbivory

   https://doi.org/10.1101/2020.09.01.278606  

   Meineke, E. K.; Davis, C. C.; Davies, T. J. (January 2021, Global change biology)

   null (Ed.)

   Species interactions drive ecosystem processes and are a major focus of global change research. Among the most consequential interactions expected to shift with climate change are those between insect herbivores and plants, both of which are highly sensitive to temperature. Insect herbivores and their host plants display varying levels of synchrony that could be disrupted or enhanced by climate change, yet empirical data on changes in synchrony are lacking. Using evidence of herbivory on herbarium specimens collected from the northeastern United States and France from 1900 to 2015, we provide evidence that plant species with temperature-sensitive phenologies experience higher levels of insect damage in warmer years, while less temperature-sensitive, co-occurring species do not. While herbivory might be mediated by interactions between warming and phenology through multiple pathways, we suggest that warming might lengthen growing seasons for phenologically sensitive plant species, exposing their leaves to herbivores for longer periods of time in warm years. We propose that elevated herbivory in warm years may represent a previously underappreciated cost to phenological tracking of climate change over longer timescales. 

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4. Phenological sensitivity to temperature mediates herbivory

   https://doi.org/10.1111/gcb.15600  

   Meineke, Emily K.; Davis, Charles C.; Davies, T. Jonathan (April 2021, Global Change Biology)

   Abstract Species interactions drive ecosystem processes and are a major focus of global change research. Among the most consequential interactions expected to shift with climate change are those between insect herbivores and plants, both of which are highly sensitive to temperature. Insect herbivores and their host plants display varying levels of synchrony that could be disrupted or enhanced by climate change, yet empirical data on changes in synchrony are lacking. Using evidence of herbivory on herbarium specimens collected from the northeastern United States and France from 1900 to 2015, we provide evidence that plant species with temperature‐sensitive phenologies experience higher levels of insect damage in warmer years, while less temperature‐sensitive, co‐occurring species do not. While herbivory might be mediated by interactions between warming and phenology through multiple pathways, we suggest that warming might lengthen growing seasons for phenologically sensitive plant species, exposing their leaves to herbivores for longer periods of time in warm years. We propose that elevated herbivory in warm years may represent a previously underappreciated cost to phenological tracking of climate change over longer timescales. 

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5. Applying machine learning to investigate long‐term insect–plant interactions preserved on digitized herbarium specimens

   https://doi.org/10.1002/aps3.11369  

   Meineke, Emily_K; Tomasi, Carlo; Yuan, Song; Pryer, Kathleen_M (June 2020, Applications in Plant Sciences)

   PremiseDespite the economic significance of insect damage to plants (i.e., herbivory), long‐term data documenting changes in herbivory are limited. Millions of pressed plant specimens are now available online and can be used to collect big data on plant–insect interactions during the Anthropocene. MethodsWe initiated development of machine learning methods to automate extraction of herbivory data from herbarium specimens by training an insect damage detector and a damage type classifier on two distantly related plant species (Quercus bicolorandOnoclea sensibilis). We experimented with (1) classifying six types of herbivory and two control categories of undamaged leaf, and (2) detecting two of the damage categories for which several hundred annotations were available. ResultsDamage detection results were mixed, with a mean average precision of 45% in the simultaneous detection and classification of two types of damage. However, damage classification on hand‐drawn boxes identified the correct type of herbivory 81.5% of the time in eight categories. The damage classifier was accurate for categories with 100 or more test samples. DiscussionThese tools are a promising first step for the automation of herbivory data collection. We describe ongoing efforts to increase the accuracy of these models, allowing researchers to extract similar data and apply them to biological hypotheses. 

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