The alternative hypotheses we present in figure 2 could be addressed with herbarium specimens for plant species with long-term herbarium records and which vary in their phenological sensitivities to climate change. While collections may not always allow us to differentiate between alternative scenarios, they could reveal how herbivory changes with warming for plants across a range of phenological sensitivities, and inform field experiments to tease apart mechanisms. In some cases, it may be possible to test for herbivory by novel herbivores by quantifying types of damage that can be traced back to particular insect genera or species, such as galls and leaf mines , or chewing damage that is characteristic of certain insect orders, e.g. margin feeding, circular hole feeding, and skeletonization. Butterfly collections might also help in resolving alternative scenarios, although we suspect that larvae, responsible for most herbivore damage, may be under-represented in collections compared to adult Lepidoptera, and flight phenology may not be correlated with larval phenology . The mismatch between adult and larval butterfly life histories is a challenge for using butterfly collections to explore phenological asynchronies. However, there are also scenarios in which phenological change at the adult stage may affect herbivory, which may offer opportunities to use the extensive collections of butterflies and moths that are available. For example, some Lepidoptera species may develop ‘lost generations’, raspberry container growing in which warmer temperatures signal caterpillars to develop into adults rather than entering diapause. The adults of the last generation may suffer high mortality rates at the onset of winter; for a more thorough discussion of this topic, see.
Museum specimens of moths and butterflies could inform how common it is for Lepidoptera species to add another generation in response to climate change, and contrasting herbarium specimens of their host plants could reveal how herbivory is differentially impacted by species that have and have not added generations with climate change.One of the most supported predictions in global change biology is that species’ ranges will shift poleward and upward in elevation as the climate warms. For many insect species, poleward range expansion may be explained by increased over-winter survival and/or feeding owing to warmer winters. For multivoltine insects, longer growing seasons can also increase the number of generations completed per year, leading to population growth that might facilitate range expansion if host plants are available. Most predictions on plant species’ range shifts are predicated on the assumption that abiotic factors determine range edges; however, biotic factors can also contribute to range limits. There is also growing evidence that biotic factors, such as herbivores and disease can interact with abiotic factors to determine the trailing range edges of some plant species. However, the factors that drive range limits at leading and trailing edges remain unknown for most species. Biological collections typically have associated metadata describing when and where collections were made, and therefore provide rich data on species distributions and distributional shifts over time. Species distribution models are commonly used to map past and present distributions, but they are intrinsically limited by the number and representation of input records, and, in the case of global change research, the number of records available from before and after global change.
The extensive digitization efforts currently underway for insect and plant specimens will improve our predictions and ability to track changing distributions. For well sampled plant species, we might also be able to investigate changes in herbivory at poleward range edges to determine if it has declined over time as plant ranges expand into novel habitats—an extension of the enemy release hypothesis associated with species invasions, discussed below. Larger digital collections of insect herbivores will provide the opportunity to compare range shifts across insect clades and to identify traits that govern range expansion and contraction. For example, we might expect that warmer winters will disrupt winter diapause for many insect species, leading to range contraction and decline, while those that do not have diapause will benefit from higher rates of winter survival. However, it is also possible that insects with diapause are more likely to maintain phenological synchrony with on how herbivore damage will change over time. Species traits might also determine whether species shift over time or space, and how these two responses trade-off . The ability of insect herbivores to switch host plants may be another factor that constrains or facilitates herbivore range expansion, and thus plant –herbivore interaction strengths. Specialized insects that do not feed on newly encountered plant species may be limited in their geographical spread, whereas more generalist herbivores would be less constrained. Herbaria may capture such switches to novel hosts, showing up as new types of herbivore damage on specimens as host plants and their insect herbivores shift their distributions and provide the opportunity for novel plant –herbivore interactions. For example, leaf mines and galls—which are preserved on herbarium specimens—are made by a wide variety of insect herbivore taxa, including some of the most diverse groups of insects—Lepidoptera, Coleoptera , and Diptera —and are often specific to insect genera or species .
The Lepidoptera that make leaf mines are not well represented in long-term citizen science data because leaf miners are typically micromoths, which are not the focus of long-term observations, and leaf mining and galling damage are only rarely included in herbivory studies, which tend to focus on chewing damage. Thus, herbarium specimens provide a record of a unique insect herbivore fauna not represented in long-term herbivore monitoring or herbivory studies. Herbarium specimens may also provide data on a key hypothesis in global change biology that is based on theory which dates back to Darwin: the role of natural enemy release in species invasions. The enemy release hypothesis describes the escape from native predators and parasites when species are introduced into novel habitats. While there is evidence that introduced plants escape their native herbivores, it is unclear how long this ‘release’ persists. Herbarium specimens can provide rare long-term data on herbivory and disease pressure that allows us to resolve this question. In a well-documented example, Schilthuizen et al. used herbarium specimens to show that the non-native cherry tree, Prunus serotina, acquired higher rates of herbivory over time after its introduction to Europe, while its native congener, Prunus padus, had stable herbivory levels over the same time period. This led to field investigations into the contemporary herbivore communities for these congeners, which revealed that, surprisingly, P. serotina had a richer herbivore community than the native P. padus, and that P. serotina had acquired specialized herbivores from other native host genera. This supports the hypothesis that non-native plants accumulate herbivore taxa over time in their novel habitats, which might have significant implications for plants that shift in their geographical distributions.Urbanization affects insect herbivores via a variety of mechanisms, including habitat fragmentation, habitat and host plant loss, and introduction of novel host plants that attract and support non-native herbivore communities. Given these concurrent pressures, the effects of urbanization on plant – herbivore relationships are complex and varied . However, in recent years, it has become increasingly clear that a key aspect of urbanization, the urban heat island effect, can drive relationships between plants and herbivores and may uniquely inform climate change predictions. The urban heat-island effect—the local warming of urban areas relative to surrounding countryside—increases urban temperatures 1– 128C higher than rural temperatures. Thus, local warming caused by urban development is similar in magnitude to warming expected globally over the next 100þ years, and it has therefore been suggested that cities may provide insights into the future effects of climate change. Like global warming, urban warming drives phenological advance in plants and insect herbivores. For example, plants leaf out and flower earlier in cities than in nearby rural areas, and urban heat is associated with earlier egg production for certain insect herbivore species. While the effects of warming global temperatures on the synchrony of plant –herbivore interactions is still generally unresolved owing to a lack of data, these relationships can be studied across urban temperature gradients, blueberry plant pot and there is some evidence for reduced synchrony between insect herbivores and their natural enemies as a result of urban warming. Because of the parallels between the abiotic and biotic effects of urban and global warming, natural history collections from urban areas may allow us to more broadly predict how global climate warming will affect interactions between plants and their insect herbivores. Phenology data from specimens—e.g. flowering, leaf-out, insect flight— paired with data on urbanization intensity in the areas where specimens were collected could inform predictionson phenological change and synchrony for a broad range of plant and herbivore species. Specimen data from urban areas are, perhaps surprisingly, plentiful. A recent study shows that across three areas with large digitized herbarium collections—the US, South Africa and Australia—plant specimens are often collected close to natural history museums or roads. Thus, specimens could be used to explore urban natural gradients.
Like temperature, urbanization can be easily assigned to historical specimens via contemporary measurements or existing data. As a proxy for urbanization, we can use human population density data from censuses, which many countries have been collecting since the early 1900s, and in some places urbanization can be translated from historical maps or as impervious surface derived from satellite imagery. One novel approach might be to derive markers of urbanization from the herbarium specimens themselves, for example, signature pollutants, although disentangling the contributions of different drivers would then present additional challenges. In recent years, growing evidence shows that urban warming may increase abundance of certain herbivores, notably sapfeeders, potentially leading to more insect damage on urban than on rural plants, a pattern that has been documented by entomologists for over a century. Sapfeeding herbivores, such as scale insects and aphids, are often preserved on leaves and branches and thus may provide insights into changing herbivore pressure in response to urbanization. In a recent study, Youngsteadt et al. counted armoured scale insects on branches of herbarium specimens of red maple Acer rubrum and on branches of live trees across an urban warming gradient. Using these data, they showed that interannual warming and urban warming may have surprisingly congruent effects on scale insect prevalence. In box 2, we discuss how herbarium specimens might be used to investigate more complicated interactions between multiple trophic levels, relationships that could inform biological control efforts and management of urban plants. While the urban heat island effect benefits certain herbivores that survive within the urban matrix by advancing their phenolog and increasing their abundance, urbanization also excludes some insect species—a pattern which has been documented with insect museum specimens—making the effects of urbanization on herbivore damage to plants difficult to predict. Long-term records of butterfly flight from Britain showed that habitat loss is associated with butterfly decline, especially for species that are less mobile and are habitat specialists. Relatedly, a recent study across 16 European cities showed that leaf chewing damage was lower in cities relative to nearby rural areas, perhaps driven in part by higher rates of bird and ant predation on insect herbivores in cities than in rural areas. Thus, a pattern that might be emerging from the literature is that certain sap-feeding insects benefit from urban heat , while leaf chewing and the insects that cause this type of damage, notably Lepidoptera, decline in response to loss of habitat and host plants caused by urbanization. This finding suggests that the effects of bottom-up versus top-down forces driving insect herbivore fitness might differ among feeding guilds . Measurements of broad-scale chewing herbivory , presence of sap-feeders, and incidence of sooty mould as a proxy from herbarium specimens, along with insect herbivore occurrence data, could be used to test this hypothesis . In addition to describing the effects of urbanization at the local scale, museum specimens may also reveal how urbanization affects species distributions at broader spatial scales. For example, while urbanization may disrupt poleward range expansion for some species, it is possible that cities serve as warm habitat stepping stones for species with long-distance dispersal mechanisms, facilitating their poleward expansion. The insects that create leaf mines have been described as ‘aerial plankton’ because they tend to disperse long distances. Herbarium specimens might capture this rapid northern expansion of leaf mining insects and provide a record of shifting interactions with native plants that may be more likely to respond in time than space —see box 1.