Leaf out and flowering occur earlier now than historically, and plants are moving upwards in elevation or polewards in latitude as the climate warms . These shifts in space and time could have important community and ecosystem consequences, particularly if the species closely associated with plants are not responding synchronously . However, interactions between plants and their associates, and species interactions more generally, are understudied in the context of long‐term anthropogenic environmental change because long‐term data on these interactions are relatively rare . Here, we used pressed plant specimens from the northeastern US to determine how herbivory has changed over the last 112 years. While herbarium specimens have been used to quantify long‐term changes in plant phenology and morphology , they are used much less often to investigate changing interactions between plants and their antagonists. Changes in these antagonistic relationships could have consequences for ecosystem structure and function. For example, insect herbivory is a major driver of plant coexistence , biomass production , nutrient turnover and retention , animal composition , and ecosystem trajectories . Additionally, long‐term herbivory data from herbarium specimens could inform pest management by revealing trends over time, thus allowing us to determine if monitoring of certain crop or forest plants should become more frequent as global change progresses and whether new pest control strategies might be needed. Predictions for how climate warming across seasons and years may affect herbivory are complex , square pots and empirical assessment of herbivory change is limited because there are few existing long‐term observational or experimental datasets .
In experimental settings, insect survival and fecundity increase with warmer temperatures . We might thus predict that herbivory should increase with climate warming unless temperatures exceed thermal optima of the herbivores . However, warming in winter could increase insect mortality by reducing snow pack, which exposes insects to very low temperatures, and/or by disrupting winter diapause . Total herbivore damage may be further complicated by a number of additional interacting factors, including changes in insect predation , plant and insect phenology , and community composition . As a result of these or other mechanisms, patterns of herbivory across latitude and elevation are highly variable . As a consequence, spatial variation in herbivory might not reliably capture how herbivory has changed over time and with recent anthropogenic transformation of habitats and climate. Over the past few decades, it has become clear that, alongside climate change, urbanization may have profound effects on interactions between plants and their insect herbivores. Urbanization is increasing at unprecedented rates , and its effects on herbivore damage to plants remain poorly described. A number of studies show that certain leaf‐feeding insects are excluded from urban habitats, which may reduce herbivory . However, some herbivores may benefit from urbanization if they are able to escape their natural enemies or if the urban heat island effect increases population sizes . There remains, therefore, large uncertainty about whether the relationship between herbivory and urbanization can be generalized, and how climate change and urbanization may interact to influence the effects of insect herbivores on their plant hosts. In the northeastern US, mean yearly temperatures have risen 0.8°C from the early to the late 20th century. Winter temperature, a key determinant of insect herbivore survival , has increased by 0.9°C, more than other seasons .
Some urban areas within the region, such as in the Boston metropolitan area, have expanded rapidly , whereas other parts of the region remain largely rural. Here, we examine trends in herbivore damage over this time span across four plant species with varied life histories and broad geographical distributions. First, we tested whether insect herbivory was associated with warmer temperatures and urbanization. Second, we explored a proximate, biotic driver of changing herbivory over time—insect herbivore presence—with occupancy models constructed from the present‐day insect herbivore observations collected by citizen scientists. Although we do not have matching temporal data on the insect herbivores, if shifts in insect herbivore populations are driving changes in herbivory, we would predict that insect herbivore occupancy should be positively associated with the same suite of climate variables driving herbivory change through time. Effects of urbanization are more difficult to predict and might add to or counteract effects of climate change on herbivory.New England encompasses much of the northeastern USA and includes the states of Maine, Vermont, New Hampshire, Massachusetts, Connecticut, and Rhode Island. The climate isvariable and characterized by a strong latitudinal gradient in temperature and varied geography, including mountains in Maine, Vermont, and New Hampshire. Detailed information on the climatic history of this region is included in Appendix S1 and Figure S1. We sampled herbivore damage on four focal taxa in this region: shagbark hickory [Carya ovata], swamp white oak [Quercus bicolor], showy tick trefoil [Desmodium canadense], and wild lowbush blueberry [Vaccinium angustifolium]. These species are native to the northeastern United States and are subject to natural herbivory in the wild but were identified by local experts as only rarely subject to herbivory within herbaria.
Our focal plant species span a broad range of life histories and are eaten by different insect herbivores, some of which are specialized. Desmodium canadense is an understorey herb that is a host plant for many butterflies and moths. Carya ovata is a common canopy tree that provides food for a variety of wildlife. Vaccinium angustifo‐ lium is a low‐lying shrub used for commercial blueberry production. Quercus bicolor is a canopy tree used as a timber species. These species are located on distant branches of the angiosperm phylogeny, including Fagales , Ericales , and Fabales , and thus represent highly divergent evolutionary histories. The primary insect herbivore species associated with these plants in our study region are listed in Table S1. We quantified herbivory on all specimens collected in New England and preserved within the Harvard University Herbaria, excluding duplicate specimens—those collected on the same day and in the same location as a specimen already sampled—and those without county‐ level location data or full collection dates . In total, we quantified herbivory on 123 C. ovata, 89 Q. bicolor, 149 D. canadense, and 215 V. angustifolium specimens , spanning the years from 1896 to 2008. None of the specimens we examined were type specimens, and the species we included in our study were selected to be common and thus well‐represented in herbaria. We scored herbivory by overlaying a grid of 5 cm by 5 cm cells, and scoring presence or absence of damage in five randomly selected grid cells, ensuring that selected cells had at least one‐ fourth leaf cover . We focused on “chewing”—leaf removal by herbivores with mandibles, likely including Lepidoptera , Coleoptera , and Orthoptera —because it was the most common type of herbivory on specimens and is the subject of most ecological studies on herbivory . When leaves overlapped within a grid cell, we carefully lifted upper leaves to check for herbivory on the leaves below. However, such approaches do not cross over well to herbarium specimens. For example, herbarium specimens frequently have overlapping leaves that are fixed to specimen sheets. These vouchers can be carefully manipulated and inspected for the presence or absence of herbivory—as we did here—but do not allow us to accurately calculate leaf area. We scored herbivory by examining specimens under a microscope, allowing us to document evidence of herbivory even where the percentage of leaf removed was small, square plant pot and to better determine whether leaf damage occurred before the specimen was collected or subsequently in the herbarium . Digitized specimens that might be used for image processing to calculate leaf area are typically not high resolution enough to differentiate between these two types of damage. Our scoring of herbivory using a grid‐based system allows us to derive data on the intensity of herbivory while avoiding challenges posed by measuring leaf area. Achallenge in quantifying herbivory on herbarium specimens is that a suite of herbivores feed on pressed plants after they are collected. Thus, post collection damage must be distinguished from damage caused before a specimen was collected. We differentiated between damage by herbivores within herbaria and damage by herbivores on living specimens by the morphology of the damage. We found in this analysis and in a previous study that live plants generally form toughened, necrotic wounds around herbivore damage, but this is not present on specimens damaged indoors post collection. For examples of outdoor damage to live plants and indoor insect damage to specimens after collection, see Figure S2. Given that collectors aim to collect unblemished specimens, our analysis likely represents a down biased and therefore conservative estimate of total herbivory. Nonetheless, estimates are comparable among species and across years under the assumption that collector bias has remained relatively consistent across years. Shifting collection practices—for example, an increased tendency to include damaged specimens in more recent time periods— could give the appearance of changing herbivory through time.
We therefore consulted with curators at several herbaria, and although anecdotal, they reported no knowledge of systematic changes in collection methods that should affect herbivory on specimens. In addition, we note that these biases are not expected to apply to analyses of temperature and urbanization because collectors are not more likely to collect damaged specimens in warmer/cooler or more/less urbanized locations. To further explore potential for collection bias, we recorded the collector identity for each specimen, and then subset the data to collectors that collected five or more specimens. This yielded a total of 32 collectors. We then tested for an effect of collector on herbivory using a generalized linear model with a logit link function in the lme4 package in R with proportion of grid cells with chewing damage as the response and collector identity as the predictor. To examine relationships between climate and herbivory, we extracted various temperature predictors from the PRISM ClimateGroup, 2004 gridded data, all of which were county‐level means corresponding to each specimen collection date . To broadly represent temperatures during overwintering and spring development of insect herbivores, we extracted mean temperatures from January to March during the year when a specimen was collected. This climate predictor is designed to capture a range of mechanisms, including early season phenology and winter mortality. One potential benefit of higher early spring temperatures for insect fitness is faster development out of young, vulnerable stages wherein insects are more susceptible to natural enemies . To more directly capture effects of winter mortality on insects, we extracted mean temperatures in the three coldest months of the year . To represent the potential effects of summer temperature, including heat wave effects on insect mortality, we extracted mean temperatures of the three warmest months in the current and prior year . We included the prior year because many specimens were collected in spring or early summer, prior to the onset of high summer temperatures in the current year. Finally, to represent overall temperatures experienced by insects and plants throughout the year, we extracted mean annual temperatures. This suite of predictors matches the climatic data available for herbivore occurrences . As a proxy for urban development, we used human population density estimated by county and year with data from the most recent US Census . As census data are collected every 10 years, we matched each specimen to the nearest decadal population estimate.We used HOSTS, a database of Lepidoptera host plants collated from primary literature to identify insect herbivore species associated with our focal plants in the continental USA. We focus here on the order Lepidoptera as they are the most frequently collected and recorded insect taxa and have the most complete data on host associations and occurrence. We extracted occurrence data within New England from the Global Biodiversity Information Facility for each herbivore species. All records were collected between 1990 and 2015 and classified as research‐grade observations from iNaturalist, a crowd‐sourcing platform that sources natural history observations from the public. Species with fewer than 30 records were excluded from subsequent analyses because it is challenging to fit species distribution models with fewer than 30 records . The final dataset included 6,853 records for 69 herbivore species, 47 of which were herbivores of Q. bicolor, 16 of V. angustifolium, five of D. canadense, and one of C. ovata . These included one nonnative species, the gypsy moth, Lymantria dispar, which is invasive and was introduced from Europe to Massachusetts, US in 1868 or 1869 .