Promoting Beneficial Arthropods in Urban Agroecosystems: Focus on Flowers, Maybe Not Native Plants.

(1) Urbanization threatens biodiversity, yet urban native plants support native biodiversity, contributing to conservation and ecosystem services. Within urban agroecosystems, where non-native plants are abundant, native plants may boost the abundance and richness of beneficial arthropods. Nevertheless, current information focuses on pollinators, with little attention being paid to other beneficials, like natural enemies. (2) We examined how the species richness of native plants, garden management, and landscape composition influence the abundance and species richness of all, native, and non-native bees, ladybeetles, ants, and ground-foraging spiders in urban agroecosystems (i.e., urban community gardens) in California. (3) We found that native plants (~10% of species, but only ~2.5% of plant cover) had little influence on arthropods, with negative effects only on non-native spider richness, likely due to the low plant cover provided by native plants. Garden size boosted native and non-native bee abundance and richness and non-native spider richness; floral abundance boosted non-native spider abundance and native and non-native spider richness; and mulch cover and tree and shrub abundance boosted non-native spider richness. Natural habitat cover promoted non-native bee and native ant abundance, but fewer native ladybeetle species were observed. (4) While native plant richness may not strongly influence the abundance and richness of beneficial arthropods, other garden management features could be manipulated to promote the conservation of native organisms or ecosystem services provided by native and non-native organisms within urban agroecosystems.

Multiple ecosystem service synergies and landscape mediation of biodiversity within urban agroecosystems.

Ecosystem services (ESs) are essential for human well-being, especially in urban areas where 60% of the global population will live by 2030. While urban habitats have the potential to support biodiversity and ES, few studies have quantified the impact of local and landscape management across a diverse suite of services. We leverage 5 years of data (>5000 observations) across a network of urban community gardens to determine the drivers of biodiversity and ES trade-offs and synergies. We found multiple synergies and few trade-offs, contrasting previous assumptions that food production is at odds with biodiversity. Furthermore, we show that natural landscape cover interacts with local management to mediate services provided by mobile animals, specifically pest control and pollination. By quantifying the factors that support a diverse suite of ES, we highlight the critical role of garden management and urban planning for optimizing biodiversity and human benefit.

Rarity begets rarity: Social and environmental drivers of rare organisms in cities.

Cities are sometimes characterized as homogenous with species assemblages composed of abundant, generalist species having similar ecological functions. Under this assumption, rare species, or species observed infrequently, would have especially high conservation value in cities for their potential to increase functional diversity. Management to increase the number of rare species in cities could be an important conservation strategy in a rapidly urbanizing world. However, most studies of species rarity define rarity in relatively pristine environments where human management and disturbance is minimized. We know little about what species are rare, how many species are rare, and what management practices promote rare species in urban environments. Here, we identified which plants and species of birds and bees that control pests and pollinate crops are rare in urban gardens and assessed how social, biophysical factors, and cross-taxonomic comparisons influence rare species richness. We found overwhelming numbers of rare species, with more than 50% of plants observed classified as rare. Our results highlight the importance of women, older individuals, and gardeners who live closer to garden sites in increasing the number of rare plants within urban areas. Fewer rare plants were found in older gardens and gardens with more bare soil. There were more rare bird species in larger gardens and more rare bee species for which canopy cover was higher. We also found that in some cases, rarity begets rarity, with positive correlations found between the number of rare plants and bee species and between bee and bird species. Overall, our results suggest that urban gardens include a high number of species existing at low frequency and that social and biophysical factors promoting rare, planned biodiversity can cascade down to promote rare, associated biodiversity.

Differences in insectivore bird diets in coffee agroecosystems driven by obligate or generalist guild, shade management, season, and year.

Neotropical shade-grown coffee systems are renowned for their potential to conserve avian biodiversity. Yet, little is known about food resources consumed by insectivorous birds in these systems, the extent of resource competition between resident and migratory birds, or how management of shade trees might influence diet selection. We identified arthropods in stomach contents from obligate and generalist insectivorous birds captured in mist-nets at five coffee farms in Chiapas, Mexico between 2001-2003. Overall stomach contents from 938 individuals revealed dietary differences resulting from changes in seasons, years, and foraging guilds. Of four species sampled across all management systems, Yellow-green Vireo (Vireo flavoviridis) prey differed depending on coffee shade management, consuming more ants in shaded monoculture than polyculture systems. Diets of obligate and generalist resident insectivores were 72% dissimilar with obligate insectivores consuming more Coleoptera and Araneae, and generalist insectivores consuming more Formicidae and other Hymenoptera. This suggests that obligate insectivores target more specialized prey whereas generalist insectivores rely on less favorable, chemically-defended prey found in clumped distributions. Our dataset provides important natural history data for many Nearctic-Neotropical migrants such as Tennessee Warbler (Leiothlypis peregrina; N = 163), Nashville Warbler (Leiothlypis ruficapilla; N = 69), and Swainson's Thrush (Catharus ustulatus; N = 68) and tropical residents including Red-legged Honeycreepers (Cyanerpes cyaneus; N = 70) and Rufous-capped Warblers (Basileuterus rufifrons; N = 56). With declining arthropod populations worldwide, understanding the ecological interactions between obligate and generalist avian insectivores gives researchers the tools to evaluate community stability and inform conservation efforts.

Natural enemy-herbivore networks along local management and landscape gradients in urban agroecosystems.

Ecological networks can provide insight into how biodiversity loss and changes in species interactions impact the delivery of ecosystem services. In agroecosystems that vary in management practices, quantifying changes in ecological network structure across gradients of local and landscape composition can inform both the ecology and function of productive agroecosystems. In this study, we examined natural-enemy-herbivore co-occurrence networks associated with Brassica oleracea (cole crops), a common crop in urban agricultural systems. Specifically, we investigated how local management characteristics of urban community gardens and the landscape composition around them affect (1) the abundance of B. oleracea herbivores and their natural enemies, (2) the natural-enemy : herbivore ratio, and (3) natural-enemy-herbivore co-occurrence network metrics. We sampled herbivores and natural enemies in B. oleracea plants in 24 vegetable gardens in the California, USA central coast region. We also collected information on garden characteristics and land-use cover of the surrounding landscape (2 km radius). We found that increased floral richness and B. oleracea abundance were associated with increased parasitoid abundance, non-aphid herbivore abundance, and increased network vulnerability; increased vegetation complexity suppressed parasitoid abundance, but still boosted network vulnerability. High agricultural land-use cover in the landscape surrounding urban gardens was associated with lower predator, parasitoid, and non-aphid herbivore abundance, lower natural-enemy : herbivore ratios, lower interaction richness, and higher trophic complementarity. While we did not directly measure pest control, higher interaction richness, higher vulnerability, and lower trophic complementarity are associated with higher pest control services in other agroecosystems. Thus, if gardens function similarly to other agroecosystems, our results indicate that increasing vegetation complexity, including trees, shrubs, and plant richness, especially within gardens located in intensively farmed landscapes, could potentially enhance the biodiversity and abundance of natural enemies, supporting ecological networks associated with higher pest control services.

Local and Landscape Drivers of Carabid Activity, Species Richness, and Traits in Urban Gardens in Coastal California.

Urban ecosystems, as mosaics of residential, industrial, commercial, and agricultural land, present challenges for species survival due to impervious surface, degradation, fragmentation, and modification of natural habitat, pollution, and introduced species. Some urban habitats, such as community gardens, support biodiversity and promote ecosystem services. In gardens, local factors (e.g., vegetation, groundcover) and landscape surroundings (e.g., agriculture, built or impervious cover) may influence species abundance, richness, and functional traits that are present. We examined which local and landscape factors within 19 community gardens in the California central coast influence ground beetle (Carabidae) activity density, species richness, functional group richness, and functional traits-body size, wing morphology, and dispersal ability. Gardens with higher crop richness and that are surrounded by agricultural land had greater carabid activity density, while species and functional group richness did not respond to any local or landscape factor. Gardens with more leaf litter had lower carabid activity, and gardens with more leaf litter tended to have more larger carabids. Changes in local (floral abundance, ground cover) and landscape (urban land cover) factors also influenced the distribution of individuals with certain wing morphology and body size traits. Thus, both local and landscape factors influence the taxonomic and functional traits of carabid communities, with potential implications for pest control services that are provided by carabids.

Local- and landscape-scale land cover affects microclimate and water use in urban gardens.

Urban gardens in Central California are highly vulnerable to the effects of climate change, experiencing both extended high heat periods as well as water restrictions because of severe drought conditions. This puts these critical community-based food production systems at risk as California is expected to experience increasing weather extremes. In agricultural systems, increased vegetation complexity, such as greater structure or biodiversity, can increase the resilience of food production systems from climate fluctuations. We test this theory in 15 urban gardens across California's Central Coast. Local- and landscape-scale measures of ground, vegetation, and land cover were collected in and around each garden, while climate loggers recorded temperatures in each garden in 30min increments. Multivariate analyses, using county as a random factor, show that both local- and landscape-scale factors were important. All factors were significant predictors of mean temperature. Tallest vegetation, tree/shrub species richness, grass cover, mulch cover, and landscape level agricultural cover were cooling factors; in contrast, garden size, garden age, rock cover, herbaceous species richness, and landscape level urban cover were warming factors. Results were similar for the maximum temperature analysis except that agriculture land cover and herbaceous species richness were not significant predictors of maximum temperature. Analysis of gardener watering behavior to observed temperatures shows that garden microclimate was significantly related to the number of minutes watered as well as the number of liters of water used per watering event. Thus gardeners seem to respond to garden microclimate in their watering behavior even though this behavior is most probably motivated by a range of other factors such as water regulations and time availability. This research shows that local management of ground cover and vegetation can reduce mean and maximum temperatures in gardens, and the reduced temperatures may influence watering behavior of gardeners.

Local and landscape drivers of predation services in urban gardens.

In agroecosystems, local and landscape features, as well as natural enemy abundance and richness, are significant predictors of predation services that may result in biological control of pests. Despite the increasing importance of urban gardening for provisioning of food to urban populations, most urban gardeners suffer from high pest problems, and have little knowledge about how to manage their plots to increase biological control services. We examined the influence of local, garden scale (i.e., herbaceous and arboreal vegetation abundance and diversity, ground cover) and landscape (i.e., landscape diversity and surrounding land use types) characteristics on predation services provided by naturally occurring predators in 19 urban gardens in the California central coast. We introduced sentinel pests (moth eggs and larvae and pea aphids) onto greenhouse-raised plants taken to gardens and assigned to open or bagged (predator exclosure) treatments. We found high predation rates with between 40% and 90% of prey items removed in open treatments. Predation services varied with local and landscape factors, but significant predictors differed by prey species. Predation of eggs and aphids increased with vegetation complexity in gardens, but larvae predation declined with vegetation complexity. Smaller gardens experienced higher predation services, likely due to increases in predator abundance in smaller gardens. Several ground cover features influenced predation services. In contrast to patterns in rural agricultural landscapes, predation on aphids declined with increases in landscape diversity. In sum, we report the relationships between several local management factors, as well as landscape surroundings, and implications for garden management.

Landscape and Local Correlates of Bee Abundance and Species Richness in Urban Gardens.

Urban gardens may preserve biodiversity as urban population densities increase, but this strongly depends on the characteristics of the gardens and the landscapes in which they are embedded. We investigated whether local and landscape characteristics are important correlates of bee (Hymenoptera: Apiformes) abundance and species richness in urban community gardens. We worked in 19 gardens in the California central coast and sampled bees with aerial nets and pan traps. We measured local characteristics (i.e., vegetation and ground cover) and used the USGS National Land Cover Database to classify the landscape surrounding our garden study sites at 2 km scales. We classified bees according to nesting type (i.e., cavity, ground) and body size and determined which local and landscape characteristics correlate with bee community characteristics. We found 55 bee species. One landscape and several local factors correlated with differences in bee abundance and richness for all bees, cavity-nesting bees, ground-nesting bees, and different sized bees. Generally, bees were more abundant and species rich in bigger gardens, in gardens with higher floral abundance, less mulch cover, more bare ground, and with more grass. Medium bees were less abundant in sites surrounded by more medium intensity developed land within 2 km. The fact that local factors were generally more important drivers of bee abundance and richness indicates a potential for gardeners to promote bee conservation by altering local management practices. In particular, increasing floral abundance, decreasing use of mulch, and providing bare ground may promote bees in urban gardens.

Local and Landscape Correlates of Spider Activity Density and Species Richness in Urban Gardens.

Urbanization is a major threat to arthropod biodiversity and abundance due to reduction and loss of suitable natural habitat. Green spaces and small-scale agricultural areas may provide habitat and resources for arthropods within densely developed cities. We studied spider activity density (a measure of both abundance and degree of movement) and diversity in urban gardens in Santa Cruz, Santa Clara, and Monterey counties in central California, USA. We sampled for spiders with pitfall traps and sampled 38 local site characteristics for 5 mo in 19 garden sites to determine the relative importance of individual local factors. We also analyzed 16 landscape variables at 500-m and 1-km buffers surrounding each garden to determine the significance of landscape factors. We identified individuals from the most common families to species and identified individuals from other families to morphospecies. Species from the families Lycosidae and Gnaphosidae composed 81% of total adult spider individuals. Most of the significant factors that correlated with spider activity density and richness were local rather than landscape factors. Spider activity density and richness increased with mulch cover and flowering plant species, and decreased with bare soil. Thus, changes in local garden management have the potential to promote diversity of functionally important spiders in urban environments.

Epiphyte biodiversity in the coffee agricultural matrix: canopy stratification and distance from forest fragments.

Quality of the agricultural matrix profoundly affects biodiversity and dispersal in agricultural areas. Vegetatively complex coffee agroecosystems maintain species richness at larger distances from the forest. Epiphytes colonize canopy trees and provide resources for birds and insects and thus effects of agricultural production on epiphytes may affect other species. We compared diversity, composition, and vertical stratification of epiphytes in a forest fragment and in two coffee farms differing in management intensity in southern Mexico. We also examined spatial distribution of epiphytes with respect to the forest fragment to examine quality of the two agricultural matrix types for epiphyte conservation. We sampled vascular epiphytes in a forest fragment, a shade polyculture farm, and a shade monoculture farm at 100 m, 200 m, and 400 m from the forest. Epiphyte and orchid richness was greater in the forest than in the monoculture but richness was similar in the forest and polyculture farm. Epiphyte species composition differed with habitat type, but not with distance from the forest. In the forest, epiphytes were distributed throughout tree canopies, but in the farms, epiphytes were primarily found on trunks and larger branches. Epiphyte richness and species similarity to forest species declined with distance from the forest fragment in the monoculture, but richness and similarity to forest species did not decline with distance from forest in the polyculture. This suggests polyculture coffee has greater conservation value. In contrast, monoculture coffee is likely a sink habitat for epiphytes dispersing from forests into coffee. Coffee farms differ from forests in terms of the habitat they provide and species composition, thus protecting forest fragments is essential for epiphyte conservation. Nonetheless, in agricultural landscapes, vegetatively complex coffee farms may contribute to conservation of epiphytes more than other agricultural land uses.

Biodiversity loss in Latin American coffee landscapes: review of the evidence on ants, birds, and trees.

Studies have documented biodiversity losses due to intensification of coffee management (reduction in canopy richness and complexity). Nevertheless, questions remain regarding relative sensitivity of different taxa, habitat specialists, and functional groups, and whether implications for biodiversity conservation vary across regions.We quantitatively reviewed data from ant, bird, and tree biodiversity studies in coffee agroecosystems to address the following questions: Does species richness decline with intensification or with individual vegetation characteristics? Are there significant losses of species richness in coffee-management systems compared with forests? Is species loss greater for forest species or for particular functional groups?and Are ants or birds more strongly affected by intensification? Across studies, ant and bird richness declined with management intensification and with changes in vegetation. Species richness of all ants and birds and of forest ant and bird species was lower in most coffee agroecosystems than in forests, but rustic coffee (grown under native forest canopies) had equal or greater ant and bird richness than nearby forests. Sun coffee(grown without canopy trees) sustained the highest species losses, and species loss of forest ant, bird, and tree species increased with management intensity. Losses of ant and bird species were similar, although losses of forest ants were more drastic in rustic coffee. Richness of migratory birds and of birds that forage across vegetation strata was less affected by intensification than richness of resident, canopy, and understory bird species. Rustic farms protected more species than other coffee systems, and loss of species depended greatly on habitat specialization and functional traits. We recommend that forest be protected, rustic coffee be promoted,and intensive coffee farms be restored by augmenting native tree density and richness and allowing growth of epiphytes. We also recommend that future research focus on potential trade-offs between biodiversity conservation and farmer livelihoods stemming from coffee production.

Birds as predators in tropical agroforestry systems.

Insectivorous birds reduce arthropod abundances and their damage to plants in some, but not all, studies where predation by birds has been assessed. The variation in bird effects may be due to characteristics such as plant productivity or quality, habitat complexity, and/or species diversity of predator and prey assemblages. Since agroforestry systems vary in such characteristics, these systems provide a good starting point for understanding when and where we can expect predation by birds to be important. We analyze data from bird exclosure studies in forests and agroforestry systems to ask whether birds consistently reduce their arthropod prey base and whether bird predation differs between forests and agroforestry systems. Further, we focus on agroforestry systems to ask whether the magnitude of bird predation (1) differs between canopy trees and understory plants, (2) differs when migratory birds are present or absent, and (3) correlates with bird abundance and diversity. We found that, across all studies, birds reduce all arthropods, herbivores, carnivores, and plant damage. We observed no difference in the magnitude of bird effects between agroforestry systems and forests despite simplified habitat structure and plant diversity in agroforests. Within agroforestry systems, bird reduction of arthropods was greater in the canopy than the crop layer. Top-down effects of bird predation were especially strong during censuses when migratory birds were present in agroforestry systems. Importantly, the diversity of the predator assemblage correlated with the magnitude of predator effects; where the diversity of birds, especially migratory birds, was greater, birds reduced arthropod densities to a greater extent. We outline potential mechanisms for relationships between bird predator, insect prey, and habitat characteristics, and we suggest future studies using tropical agroforests as a model system to further test these areas of ecological theory.

Field-testing ecological and economic benefits of coffee certification programs.

Coffee agroecosystems are critical to the success of conservation efforts in Latin America because of their ecological and economic importance. Coffee certification programs may offer one way to protect biodiversity and maintain farmer livelihoods. Established coffee certification programs fall into three distinct, but not mutually exclusive categories: organic, fair trade, and shade. The results of previous studies demonstrate that shade certification can benefit biodiversity, but it remains unclear whether a farmer's participation in any certification program can provide both ecological and economic benefits. To assess the value of coffee certification for conservation efforts in the region, we examined economic and ecological aspects of coffee production for eight coffee cooperatives in Chiapas, Mexico, that were certified organic, certified organic and fair trade, or uncertified. We compared vegetation and ant and bird diversity in coffee farms and forests, and interviewed farmers to determine coffee yield, gross revenue from coffee production, and area in coffee production. Although there are no shade-certified farms in the study region, we used vegetation data to determine whether cooperatives would qualify for shade certification. We found no differences in vegetation characteristics, ant or bird species richness, or fraction of forest fauna in farms based on certification. Farmers with organic and organic and fair-trade certification had more land under cultivation and in some cases higher revenue than uncertified farmers. Coffee production area did not vary among farm types. No cooperative passed shade-coffee certification standards because the plantations lacked vertical stratification, yet vegetation variables for shade certification significantly correlated with ant and bird diversity. Although farmers in the Chiapas highlands with organic and/or fair-trade certification may reap some economic benefits from their certification status, their farms may not protect as much biodiversity as shade-certified farms. Working toward triple certification (organic, fair trade, and shade) at the farm level may enhance biodiversity protection, increase benefits to farmers, and lead to more successful conservation strategies in coffee-growing regions.

Impacts of major predators on tropical agroforest arthropods: comparisons within and across taxa.

In food web studies, taxonomically unrelated predators are often grouped into trophic levels regardless of their relative importance on prey assemblages, multiple predator effects, or interactions such as omnivory. Ants and birds are important predators likely to differentially shape arthropod assemblages, but no studies have compared their effects on a shared prey base. In two separate studies, we excluded birds and ants from branches of a canopy tree ( Inga micheliana) in a coffee farm in Mexico for 2 months in the dry and wet seasons of 2002. We investigated changes in arthropod densities with and without predation pressure from (1) birds and (2) ant assemblages dominated by one of two ant species ( Azteca instabilis and Camponotus senex). We first analyzed individual effects of each predator (birds, Azteca instabilis, and C. senex) then used a per day effect metric to compare differences in effects across (birds vs ants) and within predator taxa (the two ant species). Individually, birds reduced densities of total and large arthropods and some arthropod orders (e.g., spiders, beetles, roaches) in both seasons. Azteca instabilis did not significantly affect arthropods (total, small, large or specific orders). Camponotus senex, however, tended to remove arthropods (total, small), especially in the dry season, and affected arthropod densities of some orders both positively and negatively. Predators greatly differed in their effects on Inga arthropods (for all, small, large, and individual orders of arthropods) both in sign (+/-) and magnitudes of effects. Birds had stronger negative effects on arthropods than ants and the two dominant ant species had stronger effects on arthropods in different seasons. Our results show that aggregating taxonomically related and unrelated predators into trophic levels without prior experimental data quantifying the sign and strengths of effects may lead to a misrepresentation of food web interactions.