Bee species richness through time in an urbanizing landscape of the southeastern United States.

Compared to non-urban environments, cities host ecological communities with altered taxonomic diversity and functional trait composition. However, we know little about how these urban changes take shape over time. Using historical bee (Apoidea: Anthophila) museum specimens supplemented with online repositories and researcher collections, we investigated whether bee species richness tracked urban and human population growth over the past 118 years. We also determined which species were no longer collected, whether those species shared certain traits, and if collector behavior changed over time. We focused on Wake County, North Carolina, United States where human population size has increased over 16 times over the last century along with the urban area within its largest city, Raleigh, which has increased over four times. We estimated bee species richness with occupancy models, and rarefaction and extrapolation curves to account for imperfect detection and sample coverage. To determine if bee traits correlated with when species were collected, we compiled information on native status, nesting habits, diet breadth, and sociality. We used non-metric multidimensional scaling to determine if individual collectors contributed different bee assemblages over time. In total, there were 328 species collected in Wake County. We found that although bee species richness varied, there was no clear trend in bee species richness over time. However, recent collections (since 2003) were missing 195 species, and there was a shift in trait composition, particularly lost species were below-ground nesters. The top collectors in the dataset differed in how often they collected bee species, but this was not consistent between historic and contemporary time periods; some contemporary collectors grouped closer together than others, potentially due to focusing on urban habitats. Use of historical collections and complimentary analyses can fill knowledge gaps to help understand temporal patterns of species richness in taxonomic groups that may not have planned long-term data.

As prey and pollinators, insects increase reproduction and allow for outcrossing in the carnivorous plant Dionaea muscipula.

PREMISE: Understanding the factors that limit reproductive success is a key component of plant biology. Carnivorous plants rely on insects as both nutrient sources and pollinators, providing a unique system for studying the effects of both resource and pollen limitation on plant reproduction. METHODS: We conducted a field experiment using wild-growing Dionaea muscipula J. Ellis (Droseraceae) in which we manipulated prey and pollen in a factorial design and measured flower production, number of fruits, and number of seeds. Because understanding reproduction requires knowledge of a plant species' reproductive and pollination biology, we also examined the pollination system, per-visit pollinator effectiveness, and pollen-ovule (P/O) ratio of D. muscipula. RESULTS: Plants that received supplemental prey produced more flowers than control plants. They also had a higher overall fitness estimate (number of flowers × fruit set (total fruits/total flowers) × seeds per fruit), although this benefit was significant only when prey supplementation occurred in the previous growing season. Neither pollen supplementation nor the interaction between pollen and prey supplementation significantly affected overall plant fitness. CONCLUSIONS: This study reinforces the reliance of D. muscipula on adequate prey capture for flower, fruit, and seed production and a mobile pollen vector for reproduction, indicating the importance of considering insects as part of an effective conservation management plan for this species.

Can behaviour and physiology mitigate effects of warming on ectotherms? A test in urban ants.

Global climate change is expected to have pervasive effects on the diversity and distribution of species, particularly ectotherms whose body temperatures depend on environmental temperatures. However, these impacts remain difficult to predict, in part because ectotherms may adapt or acclimate to novel conditions or may use behavioural thermoregulation to reduce their exposure to stressful microclimates. Here we examine the potential for physiological and behavioural changes to mitigate effects of environmental warming on five species of ants in a temperate forest habitat subject to urban warming. We worked in eight urban and eight non-urban forest sites in North Carolina, USA; sites experienced a 1.1°C range of mean summer air temperatures. At each site, we documented species-specific microclimates (ant operative temperatures, Te ) and ant activity on a transect of 14 bait stations at three times of day. In the laboratory, we measured upper thermal tolerance (CTmax ) and thermal preference (Tpref ) for each focal species. We then asked whether thermal traits shifted at hotter sites, and whether ants avoided non-preferred microclimates in the field. CTmax and Tpref did not increase at warmer sites, indicating that these populations did not adapt or acclimate to urban warming. Consistent with behavioural thermoregulation, four of the five species were less likely to occupy baits where Te departed from Tpref . Apparent thermoregulation resulted from fixed diel activity patterns that helped ants avoid the most inappropriate temperatures but did not compensate for daily or spatial temperature variation: Hotter sites had hotter ants. This study uses a novel approach to detect behavioural thermoregulation and sublethal warming in foraging insects. The results suggest that adaptation and behaviour may not protect common temperate forest ants from a warming climate, and highlight the need to evaluate effects of chronic, sublethal warming on small ectotherms.

Larger pollen loads increase risk of heat stress in foraging bumblebees.

Global declines in bumblebee populations are linked to climate change, but specific mechanisms imposing thermal stress on these species are poorly known. Here we examine the potential for heat stress in workers foraging for pollen, an essential resource for colony development. Laboratory studies have shown that pollen foraging causes increased thoracic temperatures (Tth) in bees, but this effect has not been examined in bumblebees nor in real-world foraging situations. We examine the effects of increasing pollen load size on Tth of Bombus impatiens workers in the field while accounting for body size and microclimate. We found that Tth increased by 0.07°C for every milligram of pollen carried (p = 0.007), resulting in a 2°C increase across the observed range of pollen load sizes. Bees carrying pollen were predicted to have a Tth 1.7-2.2°C hotter than those without pollen, suggesting that under certain conditions, pollen loads could cause B. impatiens workers to heat from a safe Tth to one within the range of their critical thermal limits that we measured (41.3°C to 48.4°C). Bumblebees likely adopt behavioural or physiological strategies to counteract the thermal stress induced by pollen transport, and these may limit their foraging opportunities as environmental temperatures continue to increase.

Venus Flytrap Rarely Traps Its Pollinators.

Because carnivorous plants rely on arthropods as pollinators and prey, they risk consuming would-be mutualists. We examined this potential conflict in the Venus flytrap (Dionaea muscipula), whose pollinators were previously unknown. Diverse arthropods from two classes and nine orders visited flowers; 56% of visitors carried D. muscipula pollen, often mixed with pollen of coflowering species. Within this diverse, generalized community, certain bee and beetle species appear to be the most important pollinators, on the basis of their abundance, pollen load size, and pollen fidelity. Dionaea muscipula prey spanned four invertebrate classes and 11 orders; spiders, beetles, and ants were most common. At the family and species levels, few taxa were shared between traps and flowers, yielding a near-zero value of niche overlap for these potentially competing structures. Spatial separation of traps and flowers may contribute to partitioning the invertebrate community between nutritional and reproductive functions in D. muscipula.

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.

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.

Seed odor mediates an obligate ant-plant mutualism in Amazonian rainforests.

Seed dispersal mutualisms are essential for the survival of diverse plant species and communities worldwide. Among invertebrates, only ants have a major role in seed dispersal, and thousands of plant species produce seeds specialized for ant dispersal in "diffuse" multispecies interactions. An outstanding but poorly understood ant-seed mutualism occurs in the Amazonian rainforest, where arboreal ants collect seeds of several epiphyte species and cultivate them in nutrient-rich nests, forming abundant and conspicuous hanging gardens known as ant-gardens (AGs). AG ants and plants are dominant members of lowland Amazonian ecosystems, and their interaction is both specific and obligate, but the means by which ants locate, recognize, and accept their mutualist seeds while rejecting other seeds is unknown. Here we address the chemical and behavioral basis of the AG interaction. We show that workers of the AG ant Camponotus femoratus are attracted to odorants emanating from seeds of the AG plant Peperomia macrostachya, and that chemical cues also elicit seed-carrying behavior. We identify five compounds from P. macrostachya seeds that, as a blend, attract C. femoratus workers. This report of attractive odorants from ant-dispersed seeds illustrates the intimacy and complexity of the AG mutualism and begins to illuminate the chemical basis of this important and enigmatic interaction.

The Impact of Prescribed Burning on Native Bee Communities (Hymenoptera: Apoidea: Anthophila) in Longleaf Pine Savannas in the North Carolina Sandhills.

Prescribed burning is a common silvicultural practice used in the management of longleaf pine (Pinus palustris Mill., Pinales: Pinaceae) savannas to reduce hardwood encroachment and ground cover and to maintain biodiversity. We investigated the response of the native bee community (Hymenoptera: Apoidea: Anthophila) in the Sandhills of North Carolina to prescribed burning on a 3-yr rotation over two consecutive years (2012 and 2013). We deployed bee bowl traps in sites that had been burned the year of sampling, 1 yr before, 2 yr before, and in unburned controls. In total, 2,276 bees of 109 species were captured. Bee abundance declined with time since fire, with 2.3 times more bees captured in the most recently burned sites than in unburned controls. Bee diversity also declined with time since fire, with 2.1 times more species captured in the most recently burned sites than in controls. Bee community composition also responded to fire; we present evidence that this response was mediated in part by the effect of fire on the amount of bare ground and canopy cover. Bees nesting aboveground were unaffected by fire, contrary to our expectation that fire would destroy the wood and stems in which these species nest. Our results indicate that prescribed burning is a silvicultural practice consistent with pollinator conservation in longleaf pine ecosystems of the North Carolina sandhills.

Construction of a Compact Low-Cost Radiation Shield for Air-Temperature Sensors in Ecological Field Studies.

Low cost temperature sensors are increasingly used by ecologists to assess climatic variation and change on ecologically relevant scales. Although cost-effective, if not deployed with proper solar radiation shielding, the observations recorded from these sensors will be biased and inaccurate. Manufactured radiation shields are effective at minimizing this bias, but are expensive compared to the cost of these sensors. Here, we provide a detailed methodology for constructing a compact version of a previously described custom fabricated radiation shield, which is more accurate than other published shielding methods that attempt to minimize shield size or construction costs. The method requires very little material: corrugated plastic sheets, aluminum foil duct tape, and cable ties. One 15 cm and two 10 cm squares of corrugated plastic are used for each shield. After cutting, scoring, taping and stapling of the sheets, the 10 cm squares form the bottom two layers of the solar radiation shield, while the 15 cm square forms the top layer. The three sheets are held together with cable ties. This compact solar radiation shield can be suspended, or placed against any flat surface. Care must be taken to ensure that the shield is completely parallel to the ground to prevent direct solar radiation from reaching the sensor, possibly causing increased warm biases in sun-exposed sites in the morning and afternoon relative to the original, larger design. Even so, differences in recorded temperatures between the smaller, compact shield design and the original design were small (mean daytime bias = 0.06 °C). Construction costs are less than half of the original shield design, and the new design results in a less conspicuous instrument that may be advantageous in many field ecology settings.

Accurate near surface air temperature measurements are necessary to gauge large-scale ecological responses to global climate change.

Linked Article: https://doi.org/10.1002/ece3.3965.

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.

Urban stress is associated with variation in microbial species composition-but not richness-in Manhattan.

The biological diversity and composition of microorganisms influences both human health outcomes and ecological processes; therefore, understanding the factors that influence microbial biodiversity is key to creating healthy, functional landscapes in which to live. In general, biological diversity is predicted to be limited by habitat size, which for green areas is often reduced in cities, and by chronic disturbance (stress). These hypotheses have not previously been tested in microbial systems in direct comparison to macroorganisms. Here we analyzed bacterial, fungal and ant communities in small road medians (average area 0.0008 km(2)) and larger parks (average area 0.64 km(2)) across Manhattan (NYC). Bacterial species richness was not significantly different between medians and parks, but community composition was significantly distinct. In contrast, ant communities differed both in composition and richness with fewer ant species in medians than parks. Fungi showed no significant variation in composition or richness but had few shared taxa between habitats or sites. The diversity and composition of microbes appears less sensitive to habitat patchiness or urban stress than those of macroorganisms. Microbes and their associated ecosystem services and functions may be more resilient to the negative effects of urbanization than has been previously appreciated.

Cuticular hydrocarbon synthesis and its maternal provisioning to embryos in the viviparous cockroach Diploptera punctata.

Embryos of the viviparous cockroach Diploptera punctata accumulate large amounts of hydrocarbon (HC) of either maternal or embryonic origin. HC synthesis and its accumulation in maternal and embryonic tissues were measured over the course of gestation. Female abdominal integument was the only tissue that synthesized appreciable amounts of HC in vitro, and did so at an increasing rate from the time of mating to mid-pregnancy, when rates of synthesis declined. The embryos synthesized HC at rates <1% those of the female, showing that the majority of HC detected in and on embryos was of maternal origin. The brood sac that houses the developing embryos did not synthesize HC in vitro, indicating that HC must be transported from the female abdominal integument to the embryos. The mass of female epicuticular HC was constant at approximately 183 microg, while her internal HC increased fourfold from mating to mid-pregnancy, then declined until parturition. The decline in internal HC reflected both declining HC synthesis in the female and greater export to the embryos, as embryonic internal HC increased 250-fold prior to parturition. An external HC coating over the oothecal covering and chorion of the embryos increased to mid-pregnancy, then declined. Unlike oviparous cockroaches, D. punctata females fed throughout the reproductive cycle, reflecting the nutritional demands of continuously provisioning the developing embryos.

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.

Divergent chemical cues elicit seed collecting by ants in an obligate multi-species mutualism in lowland Amazonia.

In lowland Amazonian rainforests, specific ants collect seeds of several plant species and cultivate them in arboreal carton nests, forming species-specific symbioses called ant-gardens (AGs). In this obligate mutualism, ants depend on the plants for nest stability and the plants depend on ant nests for substrate and nutrients. AG ants and plants are abundant, dominant members of lowland Amazonian ecosystems, but the cues ants use to recognize the seeds are poorly understood. To address the chemical basis of the ant-seed interaction, we surveyed seed chemistry in nine AG species and eight non-AG congeners. We detected seven phenolic and terpenoid volatiles common to seeds of all or most of the AG species, but a blend of the shared compounds was not attractive to the AG ant Camponotus femoratus. We also analyzed seeds of three AG species (Anthurium gracile, Codonanthe uleana, and Peperomia macrostachya) using behavior-guided fractionation. At least one chromatographic fraction of each seed extract elicited retrieval behavior in C. femoratus, but the active fractions of the three plant species differed in polarity and chemical composition, indicating that shared compounds alone did not explain seed-carrying behavior. We suggest that the various AG seed species must elicit seed-carrying with different chemical cues.