Steven D. Frank

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.

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 2–3°C in the next 50–100 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.

Spatial and Temporal Variation in Natural Enemy Assemblages on Maryland Native Plant Species

Abstract 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.

Reducing Insecticide Volume and Nontarget Effects of Ambrosia Beetle Management in Nurseries

ABSTRACT 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.

Non-Native Ambrosia Beetles as Opportunistic Exploiters of Living but Weakened Trees

Exotic Xylosandrus spp. ambrosia beetles established in non-native habitats have been associated with sudden and extensive attacks on a diverse range of living trees, but factors driving their shift from dying/dead hosts to living and healthy ones are not well understood. We sought to characterize the role of host physiological condition on preference and colonization by two invaders, Xylosandrus germanus and Xylosandrus crassiusculus. When given free-choice under field conditions among flooded and non-flooded deciduous tree species of varying intolerance to flooding, beetles attacked flood-intolerant tree species over more tolerant species within 3 days of initiating flood stress. In particular, flood-intolerant flowering dogwood (Cornus florida) sustained more attacks than flood-tolerant species, including silver maple (Acer saccharinum) and swamp white oak (Quercus bicolor). Ethanol, a key host-derived attractant, was detected at higher concentrations 3 days after initiating flooding within stems of flood intolerant species compared to tolerant and non-flooded species. A positive correlation was also detected between ethanol concentrations in stem tissue and cumulative ambrosia beetle attacks. When adult X. germanus and X. crassiusculus were confined with no-choice to stems of flood-stressed and non-flooded C. florida, more ejected sawdust resulting from tunneling activity was associated with the flood-stressed trees. Furthermore, living foundresses, eggs, larvae, and pupae were only detected within galleries created in stems of flood-stressed trees. Despite a capability to attack diverse tree genera, X. germanus and X. crassiusculus efficiently distinguished among varying host qualities and preferentially targeted trees based on their intolerance of flood stress. Non-flooded trees were not preferred or successfully colonized. This study demonstrates the host-selection strategy exhibited by X. germanus and X. crassiusculus in non-native habitats involves detection of stress-induced ethanol emission and early colonization of living but weakened trees.

The Effects of Urban Warming on Herbivore Abundance and Street Tree Condition

Trees are essential to urban habitats because they provide services that benefit the environment and improve human health. Unfortunately, urban trees often have more herbivorous insect pests than rural trees but the mechanisms and consequences of these infestations are not well documented. Here, we examine how temperature affects the abundance of a scale insect, Melanaspis tenebricosa (Comstock) (Hemiptera: Diaspididae), on one of the most commonly planted street trees in the eastern U.S. Next, we examine how both pest abundance and temperature are associated with water stress, growth, and condition of 26 urban street trees. Although trees in the warmest urban sites grew the most, they were more water stressed and in worse condition than trees in cooler sites. Our analyses indicate that visible declines in tree condition were best explained by scale-insect infestation rather than temperature. To test the broader relevance of these results, we extend our analysis to a database of more than 2700 Raleigh, US street trees. Plotting these trees on a Landsat thermal image of Raleigh, we found that warmer sites had over 70% more trees in poor condition than those in cooler sites. Our results support previous studies linking warmer urban habitats to greater pest abundance and extend this association to show its effect on street tree condition. Our results suggest that street tree condition and ecosystem services may decline as urban expansion and global warming exacerbate the urban heat island effect. Although our non-probability sampling method limits our scope of inference, our results present a gloomy outlook for urban forests and emphasize the need for management tools. Existing urban tree inventories and thermal maps could be used to identify species that would be most suitable for urban conditions.

Effects of alternative food on cannibalism and herbivore suppression by carabid larvae.

1. Predator and alternative food density are important factors influencing herbivore suppression by generalist predators. Herbivore suppression can be reduced if predators forage preferentially on alternative foods. Cannibalism can increase at high predator densities, further reducing herbivore suppression. However, complex interactions are possible, as alternative food can increase predator abundance and survival restoring top‐down effects on herbivores.

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.

Urbanization Increases Pathogen Pressure on Feral and Managed Honey Bees.

Given the role of infectious disease in global pollinator decline, there is a need to understand factors that shape pathogen susceptibility and transmission in bees. Here we ask how urbanization affects the immune response and pathogen load of feral and managed colonies of honey bees (Apis mellifera Linnaeus), the predominant economically important pollinator worldwide. Using quantitative real-time PCR, we measured expression of 4 immune genes and relative abundance of 10 honey bee pathogens. We also measured worker survival in a laboratory bioassay. We found that pathogen pressure on honey bees increased with urbanization and management, and the probability of worker survival declined 3-fold along our urbanization gradient. The effect of management on pathogens appears to be mediated by immunity, with feral bees expressing immune genes at nearly twice the levels of managed bees following an immune challenge. The effect of urbanization, however, was not linked with immunity; instead, urbanization may favor viability and transmission of some disease agents. Feral colonies, with lower disease burdens and stronger immune responses, may illuminate ways to improve honey bee management. The previously unexamined effects of urbanization on honey-bee disease are concerning, suggesting that urban areas may favor problematic diseases of pollinators.