Interactive Effects of Temperature, Aridity, and Plant Stoichiometry on Insect Herbivory: Past and Present.

AbstractThe influence of climate on deep-time plant-insect interactions is becoming increasingly well known, with temperature, CO2 increases (and associated stoichiometric changes in plants), and aridity likely playing a critical role. In our modern climate, all three factors are shifting at an unprecedented rate, with uncertain consequences for biodiversity. To investigate effects of temperature, stoichiometry (specifically that of nitrogen), and aridity on insect herbivory, we explored insect herbivory in three modern floral assemblages and in 39 fossil floras, especially focusing on eight floras around a past hyperthermal event (the Paleocene-Eocene Thermal Maximum) from Bighorn Basin (BB). We find that higher temperatures were associated with increased herbivory in the past, especially among BB sites. In these BB sites, non-N2-fixing plants experienced a lower richness but higher frequency of herbivory damage than N2-fixing plants. Herbivory frequency but not richness was greater in BB sites compared with contemporaneous, nearby, but less arid sites from Hanna Basin. Compared with deep-time environments, herbivory frequency and richness are higher in modern sites, suggesting that current accelerated warming uniquely impacts plant-insect interactions. Overall, our work addresses multiple aspects of climate change using fossil data while also contextualizing the impact of modern anthropogenic change on Earth's most diverse interactions.

Insect herbivory within modern forests is greater than fossil localities.

Fossilized leaves provide the longest running record of hyperdiverse plant-insect herbivore associations. Reconstructions of these relationships over deep time indicate strong links between environmental conditions, herbivore diversity, and feeding damage on leaves. However, herbivory has not been compared between the past and the modern era, which is characterized by intense anthropogenic environmental change. Here, we present estimates for damage frequencies and diversities on fossil leaves from the Late Cretaceous (66.8 Ma) through the Pleistocene (2.06 Ma) and compare these estimates with Recent (post-1955) leaves collected via paleobotanical methods from modern ecosystems: Harvard Forest, United States; the Smithsonian Environmental Research Center, United States; and La Selva, Costa Rica. Total damage frequency, measured as the percentage of leaves with any herbivore damage, within modern ecosystems is greater than any fossil locality within this record. This pattern is driven by increased frequencies across nearly all functional feeding groups within the Recent. Diversities of total, specialized, and mining damage types are elevated within the Recent compared with fossil floras. Our results demonstrate that plants in the modern era are experiencing unprecedented levels of insect damage, despite widespread insect declines. Human influence, such as the rate of global climate warming, influencing insect feeding and timing of life cycle processes along with urbanization and the introduction of invasive plant and insect species may drive elevated herbivory. This research suggests that the strength of human influence on plant-insect interactions is not controlled by climate change alone but rather, the way in which humans interact with terrestrial landscape.

Widespread homogenization of plant communities in the Anthropocene.

Native biodiversity decline and non-native species spread are major features of the Anthropocene. Both processes can drive biotic homogenization by reducing trait and phylogenetic differences in species assemblages between regions, thus diminishing the regional distinctiveness of biotas and likely have negative impacts on key ecosystem functions. However, a global assessment of this phenomenon is lacking. Here, using a dataset of >200,000 plant species, we demonstrate widespread and temporal decreases in species and phylogenetic turnover across grain sizes and spatial extents. The extent of homogenization within major biomes is pronounced and is overwhelmingly explained by non-native species naturalizations. Asia and North America are major sources of non-native species; however, the species they export tend to be phylogenetically close to recipient floras. Australia, the Pacific and Europe, in contrast, contribute fewer species to the global pool of non-natives, but represent a disproportionate amount of phylogenetic diversity. The timeline of most naturalisations coincides with widespread human migration within the last ~500 years, and demonstrates the profound influence humans exert on regional biotas beyond changes in species richness.

Bias assessments to expand research harnessing biological collections.

Biological collections are arguably the most important resources for investigations into the impacts of human activities on biodiversity. However, the apparent opportunities presented by museum-derived datasets have not resulted in consistent or widespread use of specimens in ecology outside phenological research and species distribution modeling. We attribute this gap between opportunity and application to biases introduced by collectors, curators, and preservation practices and an imperfect understanding of these biases and how to mitigate them. To facilitate broader use of specimen-based data, we characterize collection biases across key axes and explore interactions among them. We then present a framework for determining the bias assessments needed when extracting data from biological collections. We show that bias assessments required by particular ecological studies will depend on the response variables being measured and the predictor axes of interest. We argue that quantification of biases in specimen-derived datasets is needed to facilitate the widespread application of these data.

Phenological sensitivity to temperature mediates herbivory.

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.

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

PREMISE: Despite 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. METHODS: We 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 bicolor and Onoclea 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. RESULTS: Damage 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. DISCUSSION: These 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.

Using computer vision on herbarium specimen images to discriminate among closely related horsetails (Equisetum).

PREMISE: Equisetum is a distinctive vascular plant genus with 15 extant species worldwide. Species identification is complicated by morphological plasticity and frequent hybridization events, leading to a disproportionately high number of misidentified specimens. These may be correctly identified by applying appropriate computer vision tools. METHODS: We hypothesize that aerial stem nodes can provide enough information to distinguish among Equisetum hyemale, E. laevigatum, and E . ×ferrissii, the latter being a hybrid between the other two. An object detector was trained to find nodes on a given image and to distinguish E. hyemale nodes from those of E. laevigatum. A classifier then took statistics from the detection results and classified the given image into one of the three taxa. Both detector and classifier were trained and tested on expert manually annotated images. RESULTS: In our exploratory test set of 30 images, our detector/classifier combination identified all 10 E. laevigatum images correctly, as well as nine out of 10 E. hyemale images, and eight out of 10 E. ×ferrissii images, for a 90% classification accuracy. DISCUSSION: Our results support the notion that computer vision may help with the identification of herbarium specimens once enough manual annotations become available.

Machine Learning Using Digitized Herbarium Specimens to Advance Phenological Research.

Machine learning (ML) has great potential to drive scientific discovery by harvesting data from images of herbarium specimens-preserved plant material curated in natural history collections-but ML techniques have only recently been applied to this rich resource. ML has particularly strong prospects for the study of plant phenological events such as growth and reproduction. As a major indicator of climate change, driver of ecological processes, and critical determinant of plant fitness, plant phenology is an important frontier for the application of ML techniques for science and society. In the present article, we describe a generalized, modular ML workflow for extracting phenological data from images of herbarium specimens, and we discuss the advantages, limitations, and potential future improvements of this workflow. Strategic research and investment in specimen-based ML methods, along with the aggregation of herbarium specimen data, may give rise to a better understanding of life on Earth.

Local- and landscape-scale variables shape insect diversity in an urban biodiversity hot spot.

Local community structure is shaped by processes acting at local and landscape scales. The relative importance of drivers operating across different spatial scales is difficult to test without observations across regional or latitudinal gradients. Cities exhibit strong but predictable environmental gradients overlaying a mosaic of highly variable but repeated habitat types within a constrained area. Thus, cities present a unique opportunity to explore how both local and landscape factors influence local biotic communities. We used insect communities to examine the interactions among local environmental variables (such as temperature and relative humidity), local habitat characteristics (such as plant community composition), and broad-scale patterns of urbanization (including biophysical, human-built, and socioeconomic variables) on local insect abundance, species richness, and species composition in Los Angeles, a hot, dry, near-desert city. After accounting for seasonal trends, insect species richness and abundance were highest in drier and hotter sites, but the magnitude of local environmental effects varied with the degree of urbanization. In contrast, insect species composition was best predicted by broad-scale urbanization trends, with the more native communities occurring in less urbanized sites and more cosmopolitan insects occurring in highly urbanized sites. However, insect species richness and abundance were >30% higher and insect composition was similar across sites that hosted either native or drought-tolerant plants, regardless of the degree of urbanization. These results demonstrate that urban insect biodiversity is a product of interacting mechanisms working at both local and landscape scales. However, local-scale changes to urban habitats, such as cultivating plants that are adapted to the natural environment nearest the city, can positively impact urban biodiversity regardless of location.

Temperature accounts for the biodiversity of a hyperdiverse group of insects in urban Los Angeles.

The urban heat island effect is a worldwide phenomenon that has been linked to species distributions and abundances in cities. However, effects of urban heat on biotic communities are nearly impossible to disentangle from effects of land cover in most cases because hotter urban sites also have less vegetation and more impervious surfaces than cooler sites within cities. We sampled phorid flies, one of the largest, most biologically diverse families of true flies (Insecta: Diptera: Phoridae), at 30 sites distributed within the central Los Angeles Basin, where we found that temperature and the density of urban land cover are decoupled. Abundance, richness, and community composition of phorids inside urban Los Angeles were most parsimoniously accounted for by mean air temperature in the week preceding sampling. Sites with intermediate mean temperatures had more phorid fly individuals and higher richness. Communities were more even at urban sites with lower minimum temperatures and sites located further away from natural areas, suggesting that communities separated from natural source populations may be more homogenized. Species composition was best explained by minimum temperature. Inasmuch as warmer areas within cities can predict future effects of climate change, phorid fly communities are likely to shift nonlinearly under future climates in more natural areas. Exhaustive surveys of biotic communities within cities, such as the one we describe here, can provide baselines for determining the effects of urban and global climate warming as they intensify.

Azteca ants maintain unique microbiomes across functionally distinct nest chambers.

The microbiome of built structures has considerable influence over an inhabitant's well-being, yet the vast majority of research has focused on human-built structures. Ants are well-known architects, capable of constructing elaborate dwellings, the microbiome of which is underexplored. Here, we explore the bacterial and fungal microbiomes in functionally distinct chambers within and outside the nests of Azteca alfari ants in Cecropia peltata trees. We predicted that A. alfari colonies (1) maintain distinct microbiomes within their nests compared to the surrounding environment, (2) maintain distinct microbiomes among nest chambers used for different functions, and (3) limit both ant and plant pathogens inside their nests. In support of these predictions, we found that internal and external nest sampling locations had distinct microbial communities, and A. alfari maintained lower bacterial richness in their 'nurseries'. While putative animal pathogens were suppressed in chambers that ants actively inhabited, putative plant pathogens were not, which does not support our hypothesis that A. alfari defends its host trees against microbial antagonists. Our results show that ants influence microbial communities inside their nests similar to studies of human homes. Unlike humans, ants limit the bacteria in their nurseries and potentially prevent the build-up of insect-infecting pathogens. These results highlight the importance of documenting how indoor microbiomes differ among species, which might improve our understanding of how to promote indoor health in human dwellings.

Temperature controls phenology in continuously flowering Protea species of subtropical Africa.

PREMISE OF THE STUDY: Herbarium specimens are increasingly used as records of plant flowering phenology. However, most herbarium-based studies on plant phenology focus on taxa from temperate regions. Here, we explore flowering phenologic responses to climate in the subtropical plant genus Protea (Proteaceae), an iconic group of plants that flower year-round and are endemic to subtropical Africa. METHODS: We present a novel, circular sliding window approach to investigate phenological patterns developed for species with year-round flowering. We employ our method to evaluate the extent to which site-to-site and year-to-year variation in temperature and precipitation affect flowering dates using a database of 1727 herbarium records of 25 Protea species. We also explore phylogenetic conservatism in flowering phenology. RESULTS: We show that herbarium data combined with our sliding window approach successfully captured independently reported flowering phenology patterns (r = 0.93). Both warmer sites and warmer years were associated with earlier flowering of 3-5 days/°C, whereas precipitation variation had no significant effect on flowering phenology. Although species vary widely in phenological responsiveness, responses are phylogenetically conserved, with closely related species tending to shift flowering similarly with increasing temperature. DISCUSSION: Our results point to climate-responsive phenology for this important plant genus and indicate that the subtropical, aseasonally flowering genus Protea has temperature-driven flowering responses that are remarkably similar to those of better-studied northern temperate plant species, suggesting a generality across biomes that has not been described elsewhere.

Biological collections for understanding biodiversity in the Anthropocene.

Global change has become a central focus of modern biology. Yet, our knowledge of how anthropogenic drivers affect biodiversity and natural resources is limited by a lack of biological data spanning the Anthropocene. We propose that the hundreds of millions of plant, fungal and animal specimens deposited in natural history museums have the potential to transform the field of global change biology. We suggest that museum specimens are underused, particularly in ecological studies, given their capacity to reveal patterns that are not observable from other data sources. Increasingly, museum specimens are becoming mobilized online, providing unparalleled access to physiological, ecological and evolutionary data spanning decades and sometimes centuries. Here, we describe the diversity of collections data archived in museums and provide an overview of the diverse uses and applications of these data as discussed in the accompanying collection of papers within this theme issue. As these unparalleled resources are under threat owing to budget cuts and other institutional pressures, we aim to shed light on the unique discoveries that are possible in museums and, thus, the singular value of natural history collections in a period of rapid change.This article is part of the theme issue 'Biological collections for understanding biodiversity in the Anthropocene'.

Museum specimens provide novel insights into changing plant-herbivore interactions.

Mounting evidence shows that species interactions may mediate how individual species respond to climate change. However, long-term anthropogenic effects on species interactions are poorly characterized owing to a lack of data. Insect herbivory is a major ecological process that represents the interaction between insect herbivores and their host plants, but historical data on insect damage to plants is particularly sparse. Here, we suggest that museum collections of insects and plants can fill key gaps in our knowledge on changing trophic interactions, including proximate mechanisms and the net outcomes of multiple global change drivers across diverse insect herbivore-plant associations. We outline theory on how global change may affect herbivores and their host plants and highlight the unique data that could be extracted from museum specimens to explore their shifting interactions. We aim to provide a framework for using museum specimens to explore how some of the most diverse co-evolved relationships are responding to climate and land use change.This article is part of the theme issue 'Biological collections for understanding biodiversity in the Anthropocene'.

Ad hoc instrumentation methods in ecological studies produce highly biased temperature measurements.

In light of global climate change, ecological studies increasingly address effects of temperature on organisms and ecosystems. To measure air temperature at biologically relevant scales in the field, ecologists often use small, portable temperature sensors. Sensors must be shielded from solar radiation to provide accurate temperature measurements, but our review of 18 years of ecological literature indicates that shielding practices vary across studies (when reported at all), and that ecologists often invent and construct ad hoc radiation shields without testing their efficacy. We performed two field experiments to examine the accuracy of temperature observations from three commonly used portable data loggers (HOBO Pro, HOBO Pendant, and iButton hygrochron) housed in manufactured Gill shields or ad hoc, custom-fabricated shields constructed from everyday materials such as plastic cups. We installed this sensor array (five replicates of 11 sensor-shield combinations) at weather stations located in open and forested sites. HOBO Pro sensors with Gill shields were the most accurate devices, with a mean absolute error of 0.2°C relative to weather stations at each site. Error in ad hoc shield treatments ranged from 0.8 to 3.0°C, with the largest errors at the open site. We then deployed one replicate of each sensor-shield combination at five sites that varied in the amount of urban impervious surface cover, which presents a further shielding challenge. Bias in sensors paired with ad hoc shields increased by up to 0.7°C for every 10% increase in impervious surface. Our results indicate that, due to variable shielding practices, the ecological literature likely includes highly biased temperature data that cannot be compared directly across studies. If left unaddressed, these errors will hinder efforts to predict biological responses to climate change. We call for greater standardization in how temperature data are recorded in the field, handled in analyses, and reported in publications.

Early pest development and loss of biological control are associated with urban warming.

Climate warming is predicted to cause many changes in ectotherm communities, one of which is phenological mismatch, wherein one species' development advances relative to an associated species or community. Phenological mismatches already lead to loss of pollination services, and we predict that they also cause loss of biological control. Here, we provide evidence that a pest develops earlier due to urban warming but that phenology of its parasitoid community does not similarly advance. This mismatch is associated with greater egg production that likely leads to more pests on trees.

Urban warming drives insect pest abundance on street trees.

Cities profoundly alter biological communities, favoring some species over others, though the mechanisms that govern these changes are largely unknown. Herbivorous arthropod pests are often more abundant in urban than in rural areas, and urban outbreaks have been attributed to reduced control by predators and parasitoids and to increased susceptibility of stressed urban plants. These hypotheses, however, leave many outbreaks unexplained and fail to predict variation in pest abundance within cities. Here we show that the abundance of a common insect pest is positively related to temperature even when controlling for other habitat characteristics. The scale insect Parthenolecanium quercifex was 13 times more abundant on willow oak trees in the hottest parts of Raleigh, NC, in the southeastern United States, than in cooler areas, though parasitism rates were similar. We further separated the effects of heat from those of natural enemies and plant quality in a greenhouse reciprocal transplant experiment. P. quercifex collected from hot urban trees became more abundant in hot greenhouses than in cool greenhouses, whereas the abundance of P. quercifex collected from cooler urban trees remained low in hot and cool greenhouses. Parthenolecanium quercifex living in urban hot spots succeed with warming, and they do so because some demes have either acclimatized or adapted to high temperatures. Our results provide the first evidence that heat can be a key driver of insect pest outbreaks on urban trees. Since urban warming is similar in magnitude to global warming predicted in the next 50 years, pest abundance on city trees may foreshadow widespread outbreaks as natural forests also grow warmer.