Getting ahead of the curve: cities as surrogates for global change.

Urbanization represents an unintentional global experiment that can provide insights into how species will respond and interact under future global change scenarios. Cities produce many conditions that are predicted to occur widely in the future, such as warmer temperatures, higher carbon dioxide (CO2) concentrations and exacerbated droughts. In using cities as surrogates for global change, it is challenging to disentangle climate variables-such as temperature-from co-occurring or confounding urban variables-such as impervious surface-and then to understand the interactive effects of multiple climate variables on both individual species and species interactions. However, such interactions are also difficult to replicate experimentally, and thus the challenges of cities are also their unique advantage. Here, we review insights gained from cities, with a focus on plants and arthropods, and how urban findings agree or disagree with experimental predictions and historical data. We discuss the types of hypotheses that can be best tested in cities, caveats to urban research and how to further validate cities as surrogates for global change. Lastly, we summarize how to achieve the goal of using urban species responses to predict broader regional- and ecosystem-level patterns in the future.

Homogenizing an urban habitat mosaic: arthropod diversity declines in New York City parks after Super Storm Sandy.

The frequency and intensity of hurricanes are increasing globally, and anthropogenic modifications in cities have created systems that may be particularly vulnerable to their negative effects. Organisms living in cities are exposed to variable levels of chronic environmental stress. However, whether chronic stress ameliorates or exacerbates the negative effects of hurricanes remains an open question. Here, we consider two hypotheses about the simultaneous consequences of acute disturbances from hurricanes and chronic stress from urbanization for the structure of urban arthropod communities. The tipping point hypothesis posits that organisms living in high stress habitats are less resilient than those in low stress habitats because they are living near the limits of their environmental tolerances; while the disturbance tolerance hypothesis posits that high stress habitats host organisms pre-adapted for coping with disturbance, making them more resilient to the effects of storms. We used a before-after-control-impact design in the street medians and city parks of Manhattan (New York City, New York, USA) to compare arthropod communities before and after Super Storm Sandy in sites that were flooded and unflooded during the storm. Our evidence supported the disturbance tolerance hypothesis. Significant compositional differences between street medians and city parks before the storm disappeared after the storm; similarly, unflooded city parks had significantly different arthropod composition while flooded sites were indistinguishable. These differences were driven by reduced occurrences and abundances of arthropods in city parks. Finally, those arthropod groups that were most tolerant to urban stress were also the most tolerant to flooding. Our results suggest that the species that survive in high stress environments are likely to be the ones that thrive in response to acute disturbance. As storms become increasingly common and extreme, this juxtaposition in responses to storm-associated disturbance may lead to diversity loss in cities, potentially leading entire urban landscapes to mirror the reduced diversity of street medians.

Responses of arthropod populations to warming depend on latitude: evidence from urban heat islands.

Biological effects of climate change are expected to vary geographically, with a strong signature of latitude. For ectothermic animals, there is systematic latitudinal variation in the relationship between climate and thermal performance curves, which describe the relationship between temperature and an organism's fitness. Here, we ask whether these documented latitudinal patterns can be generalized to predict arthropod responses to warming across mid- and high temperate latitudes, for taxa whose thermal physiology has not been measured. To address this question, we used a novel natural experiment consisting of a series of urban warming gradients at different latitudes. Specifically, we sampled arthropods from a single common street tree species across temperature gradients in four US cities, located from 35.8 to 42.4° latitude. We captured 6746 arthropods in 34 families from 111 sites that varied in summer average temperature by 1.7-3.4 °C within each city. Arthropod responses to warming within each city were characterized as Poisson regression coefficients describing change in abundance per °C for each family. Family responses in the two midlatitude cities were heterogeneous, including significantly negative and positive effects, while those in high-latitude cities varied no more than expected by chance within each city. We expected high-latitude taxa to increase in abundance with warming, and they did so in one of the two high-latitude cities; in the other, Queens (New York City), most taxa declined with warming, perhaps due to habitat loss that was correlated with warming in this city. With the exception of Queens, patterns of family responses to warming were consistent with predictions based on known latitudinal patterns in arthropod physiology relative to regional climate. Heterogeneous responses in midlatitudes may be ecologically disruptive if interacting taxa respond oppositely to warming.

Physiological thermal limits predict differential responses of bees to urban heat-island effects.

Changes in community composition are an important, but hard to predict, effect of climate change. Here, we use a wild-bee study system to test the ability of critical thermal maxima (CTmax, a measure of heat tolerance) to predict community responses to urban heat-island effects in Raleigh, NC, USA. Among 15 focal species, CTmax ranged from 44.6 to 51.3°C, and was strongly predictive of population responses to urban warming across 18 study sites (r2 = 0.44). Species with low CTmax declined the most. After phylogenetic correction, solitary species and cavity-nesting species (bumblebees) had the lowest CTmax, suggesting that these groups may be most sensitive to climate change. Community responses to urban and global warming will likely retain strong physiological signal, even after decades of warming during which time lags and interspecific interactions could modulate direct effects of temperature.

Urban warming reduces aboveground carbon storage.

A substantial amount of global carbon is stored in mature trees. However, no experiments to date test how warming affects mature tree carbon storage. Using a unique, citywide, factorial experiment, we investigated how warming and insect herbivory affected physiological function and carbon sequestration (carbon stored per year) of mature trees. Urban warming increased herbivorous arthropod abundance on trees, but these herbivores had negligible effects on tree carbon sequestration. Instead, urban warming was associated with an estimated 12% loss of carbon sequestration, in part because photosynthesis was reduced at hotter sites. Ecosystem service assessments that do not consider urban conditions may overestimate urban tree carbon storage. Because urban and global warming are becoming more intense, our results suggest that urban trees will sequester even less carbon in the future.

Reduced cellular immune response in social insect lineages.

Social living poses challenges for individual fitness because of the increased risk of disease transmission among conspecifics. Despite this challenge, sociality is an evolutionarily successful lifestyle, occurring in the most abundant and diverse group of organisms on earth--the social insects. Two contrasting hypotheses predict the evolutionary consequences of sociality on immune systems. The social group hypothesis posits that sociality leads to stronger individual immune systems because of the higher risk of disease transmission in social species. By contrast, the relaxed selection hypothesis proposes that social species have evolved behavioural immune defences that lower disease risk within the group, resulting in lower immunity at the individual level. We tested these hypotheses by measuring the encapsulation response in 11 eusocial and non-eusocial insect lineages. We built phylogenetic mixed linear models to investigate the effect of behaviour, colony size and body size on cellular immune response. We found a significantly negative effect of colony size on encapsulation response (Markov chain Monte Carlo generalized linear mixed model (mcmcGLMM) p < 0.05; phylogenetic generalized least squares (PGLS) p < 0.05). Our findings suggest that insects living in large societies may rely more on behavioural mechanisms, such as hygienic behaviours, than on immune function to reduce the risk of disease transmission among nest-mates.

Habitat and species identity, not diversity, predict the extent of refuse consumption by urban arthropods.

Urban green spaces provide ecosystem services to city residents, but their management is hindered by a poor understanding of their ecology. We examined a novel ecosystem service relevant to urban public health and esthetics: the consumption of littered food waste by arthropods. Theory and data from natural systems suggest that the magnitude and resilience of this service should increase with biological diversity. We measured food removal by presenting known quantities of cookies, potato chips, and hot dogs in street medians (24 sites) and parks (21 sites) in New York City, USA. At the same sites, we assessed ground-arthropod diversity and abiotic conditions, including history of flooding during Hurricane Sandy 7 months prior to the study. Arthropod diversity was greater in parks (on average 11 hexapod families and 4.7 ant species per site), than in medians (nine hexapod families and 2.7 ant species per site). However, counter to our diversity-based prediction, arthropods in medians removed 2-3 times more food per day than did those in parks. We detected no effect of flooding (at 19 sites) on this service. Instead, greater food removal was associated with the presence of the introduced pavement ant (Tetramorium sp. E) and with hotter, drier conditions that may have increased arthropod metabolism. When vertebrates also had access to food, more was removed, indicating that arthropods and vertebrates compete for littered food. We estimate that arthropods alone could remove 4-6.5 kg of food per year in a single street median, reducing its availability to less desirable fauna such as rats. Our results suggest that species identity and habitat may be more relevant than diversity for predicting urban ecosystem services. Even small green spaces such as street medians provide ecosystem services that may complement those of larger habitat patches across the urban landscape.

Do cities simulate climate change? A comparison of herbivore response to urban and global warming.

Cities experience elevated temperature, CO2 , and nitrogen deposition decades ahead of the global average, such that biological response to urbanization may predict response to future climate change. This hypothesis remains untested due to a lack of complementary urban and long-term observations. Here, we examine the response of an herbivore, the scale insect Melanaspis tenebricosa, to temperature in the context of an urban heat island, a series of historical temperature fluctuations, and recent climate warming. We survey M. tenebricosa on 55 urban street trees in Raleigh, NC, 342 herbarium specimens collected in the rural southeastern United States from 1895 to 2011, and at 20 rural forest sites represented by both modern (2013) and historical samples. We relate scale insect abundance to August temperatures and find that M. tenebricosa is most common in the hottest parts of the city, on historical specimens collected during warm time periods, and in present-day rural forests compared to the same sites when they were cooler. Scale insects reached their highest densities in the city, but abundance peaked at similar temperatures in urban and historical datasets and tracked temperature on a decadal scale. Although urban habitats are highly modified, species response to a key abiotic factor, temperature, was consistent across urban and rural-forest ecosystems. Cities may be an appropriate but underused system for developing and testing hypotheses about biological effects of climate change. Future work should test the applicability of this model to other groups of organisms.

Urban warming trumps natural enemy regulation of herbivorous pests.

Trees provide ecosystem services that counter negative effects of urban habitats on human and environmental health. Unfortunately, herbivorous arthropod pests are often more abundant on urban than rural trees, reducing tree growth, survival, and ecosystem services. Previous research where vegetation complexity was reduced has attributed elevated urban pest abundance to decreased regulation by natural enemies. However, reducing vegetation complexity, particularly the density of overstory trees, also makes cities hotter than natural habitats. We ask how urban habitat characteristics influence an abiotic factor, temperature, and a biotic factor, natural enemy abundance, in regulating the abundance of an urban forest pest, the gloomy scale, (Melanaspis tenebricosa). We used a map of surface temperature to select red maple trees (Acer rubrum) at warmer and cooler sites in Raleigh, North Carolina, USA. We quantified habitat complexity by measuring impervious surface cover, local vegetation structural complexity, and landscape scale vegetation cover around each tree. Using path analysis, we determined that impervious surface (the most important habitat variable) increased scale insect abundance by increasing tree canopy temperature, rather than by reducing natural enemy abundance or percent parasitism. As a mechanism for this response, we found that increasing temperature significantly increases scale insect fecundity and contributes to greater population increase. Specifically, adult female M. tenebricosa egg sets increased by approximately 14 eggs for every 1°C increase in temperature. Climate change models predict that the global climate will increase by 2­3°C in the next 50­100 years, which we found would increase scale insect abundance by three orders of magnitude. This result supports predictions that urban and natural forests will face greater herbivory in the future, and suggests that a primary cause could be direct, positive effects of warming on herbivore fitness rather than altered trophic interactions.

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.

Differential feeding on ornamental plants by Duponchelia fovealis (Lepidoptera: Crambidae) larvae.

Duponchelia fovealis (Zeller) (Lepidoptera: Crambidae) is a polyphagous pest that feeds on a variety of ornamental and crop plants. At least 47 plant families have been identified as hosts for D. fovealis in literature based on empirical data and observations. This list is surely incomplete based on the broad feeding habits of D. fovealis. We sought to expand the list of known D. fovealis host plants and to identify species that may be less preferred or not fed upon by D. fovealis. We used laboratory feeding assays to measure D. fovealis consumption rate of leaf disks from 32 herbaceous plant species and 32 woody species grown outdoors throughout the Southeastern United States, and 24 tropical species typically grown as house plants. These plants were from 65 genera and 36 families. Between the 3 ornamental plant groups, we tested (herbaceous, woody, and tropical) that, after 24 h, plants in the tropical group were the least consumed by D. fovealis. After 24 h, the average proportion of leaf disks eaten by D. fovealis was 0.80 or higher for 5 herbaceous and 12 woody species. Proportions of leaf disks eaten varied at the family and genus level in many cases. Our research can improve integrated pest management of D. fovealis by informing growers that plants may be at more or less risk of infestation and damage by larvae.

Scale Insects Support Natural Enemies in Both Landscape Trees and Shrubs Below Them.

Scale insects are frequently abundant on urban trees. Although scales can worsen tree condition, some tree species tolerate moderate scale densities. Scales are prey for many natural enemies. Therefore, scale-infested trees may conserve natural enemies in their canopies and in nearby plants. We examined if scale-infested oaks-Quercus phellos L.-hosted more natural enemies than scale-uninfested oaks-Q. acutissima Carruth. and Q. lyrata Walter in Raleigh, NC. USA. We also tested if natural enemies were more abundant in holly shrubs (Ilex spp.) planted below scale-infested compared to scale-uninfested oaks. We collected natural enemies from the canopies of both tree types and from holly shrubs planted below these trees. To determine if tree type affected the abundance of natural enemies that passively dispersed to shrubs, we created hanging cup traps to collect arthropods as they fell from trees. To determine if natural enemies became more abundant on shrubs below scale-infested compared to scale-uninfested trees over short time scales, we collected natural enemies from holly shrubs below each tree type at three to six-day intervals. Scale-infested trees hosted more natural enemies than scale-uninfested trees and shrubs below scale-infested trees hosted more natural enemies than shrubs under scale-uninfested trees. Natural enemy abundance in hanging cup traps did not differ by tree type; however, shrubs underneath scale-infested trees accumulated more natural enemies than shrubs under scale-uninfested trees in six to nine days. Tolerating moderate pest densities in urban trees may support natural enemy communities, and thus biological control services, in shrubs below them.

Reducing insecticide volume and nontarget effects of ambrosia beetle management in nurseries.

Ambrosia beetles (Coleoptera: Curculionidae: Scolytinae) are increasingly important pests of nursery-grown trees because of the arrival of several invasive species. Ambrosia beetles bore into young trees and inoculate them with ambrosia fungus, which interferes with vascular transport resulting in limb or tree death. In spring, when beetles are active, growers make frequent applications of pyrethroid insecticides to susceptible tree species to deter beetles from boring into trees. Applications often are made with airblast sprayers that forcefully release insecticide mist that billows through nursery beds. Our objective was to compare the environmental, nontarget, and economic effects of airblast sprayer applications to applications made with a new dual-nozzle spray wand that makes targeted applications only to tree trunks where beetles attack. Through replicated experiments at commercial nurseries, we found that 5 times more insecticide was released by airblast sprayers than the manual spray wand. The extra insecticide from airblast applications landed on tree canopies, between rows, and left the nursery beds as drift. As a consequence of not spraying tree canopies, 50% more natural enemies and 50% fewer spider mites were captured in nursery beds treated with the manual spray wand than beds treated with the airblast sprayer. Manual applications require 12 times more labor than airblast applications. However, increased need for expensive miticide applications may make manual applications an economically feasible strategy for integrated pest management (IPM) of ambrosia beetles in nurseries.

Can Cities Activate Sleeper Species and Predict Future Forest Pests? A Case Study of Scale Insects.

Sleeper species are innocuous native or naturalized species that exhibit invasive characteristics and become pests in response to environmental change. Climate warming is expected to increase arthropod damage in forests, in part, by transforming innocuous herbivores into severe pests: awakening sleeper species. Urban areas are warmer than natural areas due to the urban heat island effect and so the trees and pests in cities already experience temperatures predicted to occur in 50-100 years. We posit that arthropod species that become pests of urban trees are those that benefit from warming and thus should be monitored as potential sleeper species in forests. We illustrate this with two case studies of scale insects that are important pests of urban trees in parts of the US. Melanaspis tenebricosa and Parthenolecanium quercifex are geographically native to the US but take on invasive characteristics such as higher survival and reproduction and become disconnected from natural enemies on urban trees due to the urban heat island effect. This allows them to reach high densities and damage their host trees. Parthenolecanium quercifex density increases up to 12 times on urban willow oaks with just 2 °C of warming due to higher survival and adaptation to warmer temperatures. The urban heat island effect also creates a phenological mismatch between P. quercifex and its parasitoid complex, and so egg production is higher. Melanaspis tenebricosa density can increase 300 times on urban red maples with 2.5 °C of warming. This too is due to direct effects of warmer temperatures on survival and fecundity but M. tenebricosa also benefits from the drought stress incurred by warmer urban trees. These effects combine to increase M. tenebricosa density in forests as well as on urban trees at latitudes higher than its native range. We illustrate how cities provide a unique opportunity to study the complex effects of warming on insect herbivores. Studying pestilent urban species could be a pragmatic approach for identifying and preparing for sleeper species.

Thermal Tolerance of Gloomy Scale (Hemiptera: Diaspididae) in the Eastern United States.

An insect species' geographic distribution is probably delimited in part by physiological tolerances of environmental temperatures. Gloomy scale (Melanaspis tenebricosa (Comstock)) is a native insect herbivore in eastern U.S. forests. In eastern U.S. cities, where temperatures are warmer than nearby natural areas, M. tenebricosa is a primary pest of red maple (Acer rubrum L.; Sapindales: Sapindaceae) With warming, M. tenebricosa may spread to new cities or become pestilent in forests. To better understand current and future M. tenebricosa distribution boundaries, we examined M. tenebricosa thermal tolerance under laboratory conditions. We selected five hot and five cold experimental temperatures representative of locations in the known M. tenebricosa distribution. We built models to predict scale mortality based on duration of exposure to warm or cold experimental temperatures. We then used these models to estimate upper and lower lethal durations, i.e., temperature exposure durations that result in 50% mortality. We tested the thermal tolerance for M. tenebricosa populations from northern, mid, and southern locations of the species' known distribution. Scales were more heat and cold tolerant of temperatures representative of the midlatitudes of their distribution where their densities are the greatest. Moreover, the scale population from the northern distribution boundary could tolerate cold temperatures from the northern boundary for twice as long as the population collected near the southern boundary. Our results suggest that as the climate warms the M. tenebricosa distribution may expand poleward, but experience a contraction at its southern boundary.

Chronology of Gloomy Scale (Hemiptera: Diaspididae) Infestations on Urban Trees.

Pest abundance on urban trees often increases with surrounding impervious surface. Gloomy scale (Melanaspis tenebricosa Comstock; Hemiptera: Diaspididae), a pest of red maples (Acer rubrum L.; Sapindales: Sapindaceae) in the southeast United States, reaches injurious levels in cities and reduces tree condition. Here, we use a chronosequence field study in Raleigh, NC, to investigate patterns in gloomy scale densities over time from the nursery to 13 yr after tree planting, with a goal of informing more efficient management of gloomy scale on urban trees. We examine how impervious surfaces affect the progression of infestations and how infestations affect tree condition. We find that gloomy scale densities remain low on trees until at least seven seasons after tree planting, providing a key timepoint for starting scouting efforts. Scouting should focus on tree branches, not tree trunks. Scale density on tree branches increases with impervious surface across the entire studied tree age range and increases faster on individual trees that are planted in areas with high impervious surface cover. There is a lag between the onset of pest infestations and a decline in tree condition, indicating that gloomy scale management should begin prior to a visible decline in tree condition. Our results inform management of gloomy scale in cities.

Urban forest fragments buffer trees from warming and pests.

Trees are important components of urban landscapes because of the ecosystem services they provide. However, the effects of urbanization, particularly high temperatures, can benefit chronic insect pests and threaten ecosystem services offered by urban trees. Urban forest fragments are an often-overlooked component of the greater urban forest which may help to mitigate the damaging effects of urbanization. Melanaspis tenebricosa (gloomy scale) is a common pest of Acer rubrum (red maple) that becomes more abundant because of the urban heat island effect. We conducted observational and manipulative field experiments to test the hypothesis that trees in urban forest fragments would be cooler than those in surrounding ornamental landscapes and would thus have fewer M. tenebricosa, particularly in a hot mid-latitude city. Trees in forest fragments were 1.3° cooler and had three orders of magnitude fewer M. tenebricosa than trees in ornamental landscapes in Raleigh, NC USA. However, there was no difference in M. tenebricosa density between forest and landscape trees in Newark, DE and Philadelphia, PA USA which are 3.95 degrees of latitude higher, and nearer to the northern range extent. Trees in landscapes and forest fragments did not differ in predawn water potential, a measure of water stress, but likely differed in soil composition and moisture. We used potted trees to control for these differences and found that M. tenebricosa density still increased three times more in landscapes than forests suggesting temperature and not tree stress is the dominant factor. Taken together our results indicate two things. First, that trees growing in urban forest fragments are buffered from a chronic urban tree pest due to lower temperatures. Second, that temperature-driven differences in M. tenebricosa density which we saw in Raleigh could predict future density of the pest in higher latitude cities as the climate warms.

Exotic urban trees conserve similar natural enemy communities to native congeners but have fewer pests.

Urban trees serve a critical conservation function by supporting arthropod and vertebrate communities but are often subject to arthropod pest infestations. Native trees are thought to support richer arthropod communities than exotic trees but may also be more susceptible to herbivorous pests. Exotic trees may be less susceptible to herbivores but provide less conservation value as a consequence. We tested the hypotheses that native species in Acer and Quercus would have more herbivorous pests than exotic congeners and different communities of arthropod natural enemies. The density of scale insects, common urban tree pests, was greatest on a native Acer and a native Quercus than exotic congeners in both years of our research (2012 and 2016) and sometimes reached damaging levels. However, differences in predator and parasitoid abundance, diversity, and communities were not consistent between native and exotic species in either genus and were generally similar. For example, in 2012 neither predator nor parasitoid abundance differed among native and exotic Acer congeners but in 2016 a native species, A. saccharum, had the least of both groups. A native, Q. phellos, had significantly more predators and parasitoids in 2012 than its native and exotic congeners but no differences in 2016. Parasitoid communities were significantly different among Acer species and Quercus species due in each case to greater abundance of a single family on one native tree species. These native and exotic tree species could help conserve arthropod natural enemies and achieve pest management goals.

Spatial and temporal variation in natural enemy assemblages on Maryland native plant species.

Habitat manipulation is a branch of conservation biological control in which vegetation complexity and diversity are increased in managed landscapes to provide food and other resources for arthropod natural enemies. This is often achieved by maintaining noncrop plant material such as flowering strips and beetle banks that provide natural enemies with nectar and pollen, alternative prey, shelter from disturbance, and overwintering sites. In most cases, plant material used in habitat manipulation programs is not native to the area in which it is planted. Using native plant species in conservation biological control could serve a dual function of suppressing pest arthropod outbreaks and promoting other valuable ecosystem services associated with native plant communities. We evaluated 10 plant species native to Maryland for their attractiveness to foliar and ground-dwelling natural enemies. Plants that showed particular promise were Monarda punctata, Pycnanthemum tenuifolium, and Eupatorium hyssopifolium, which generally harbored the greatest abundance of foliar predators and parasitoids, although abundance varied over time. Among ground-dwelling natural enemies, total predator and parasitoid abundance differed between plant species, but carabid and spider abundance did not. Matching certain plant species and their allied natural enemies with specific pest complexes may be enhanced by identifying the composition of natural enemy assemblages at different times of year and in both foliar and ground habitat strata.

Urban plants and climate drive unique arthropod interactions with unpredictable consequences.

Urban areas, a rapidly expanding land cover type, are composed of a mix of impervious surfaces, ornamental plants, and remnant habitat, which alters abiotic conditions and affects arthropod community assemblages and trophic interactions. Importantly, these effects often reduce arthropod diversity and may increase, reduce, or not change individual species or trophic interactions, which affects human and environmental health. Despite the pace of urbanization, drivers and consequences of change in urban arthropod communities remains poorly understood. Here, we review recent findings that shed light on the effects of urbanization on plants and abiotic conditions that drive arthropod community composition and trophic interactions, with discussion of how these effects conflict with human values and can be mitigated for future urbanization.