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.

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.

Soil management is key to maintaining soil moisture in urban gardens facing changing climatic conditions.

Urban gardens are vital green spaces, providing food for residents and space for engaged citizenry and community development. In California, climate change conditions (heat and drought) are becoming more extreme, threatening the resilience of urban gardens. Water use restrictions limit the timing and amount of water that gardeners can access, exacerbating these climate challenges for urban food production. Together with volunteer gardeners, we examined how ambient temperature, water use, vegetation, ground cover, and soil management affect rates of soil moisture gain and loss in urban gardens for a six-week period in the summer of 2017, during the hottest part of the growing season. We found that plot-level management of soils is essential for creating urban garden plots that maintain stable levels of water within garden soils. Although plots with better soil quality (i.e. water holding capacity) experienced slower rates of soil moisture gain after a watering event, they also experienced slower rates of soil moisture loss after the event, leading to soils with more stable, less fluctuating moisture profiles over time. This may benefit gardeners because under extreme climates (such as heat and drought) and water use restrictions, maintaining more stable soils for their plants means that the soils will retain water over a longer period after each watering event. Overall, such results highlight that better soil management that improves soil quality measures such as water holding capacity are potential solutions for maintaining soil moisture and reducing water use under changing climate conditions.

A new species of myrmecophilous lady beetle in the genus Diomus (Coleoptera: Coccinellidae: Diomini) from Chiapas, Mexico that feeds on green coffee scale, Coccus viridis (Green) (Hemiptera: Coccidae).

A new species of myrmecophilous lady beetle, Diomus lupusapudoves, sp. nov. (Coleoptera: Coccinellidae: Diomini), is described from a coffee agroecosystem in Chiapas, Mexico. The new species was found preying on the green coffee scale pest, Coccus viridis (Green), tended primarily by Azteca sericeasur Longino and Pheidole synanthropica Longino ants. The larval, pupal, and adult stages of the new species are described and habitus illustrations or photos provided along with anatomical details of the adult male and female genitalia. The species is most similar to Diomus thoracicus Fabricius         (=type species of Diomus), another myrmecophile, which inhabits ant nests and feeds on ant brood. The new species has a peculiar onisciform larva that lacks dorsal setae, features that it shares with D. thoracicus. The new species is only the second species in the genus reported as a myrmecophile, although the life histories of most species have been poorly documented.

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.

Trophic cascades in agricultural landscapes: indirect effects of landscape composition on crop yield.

The strength and prevalence of trophic cascades, defined as positive, indirect effects of natural enemies (predatory and parasitic arthropods) on plants, is highly variable in agroecosystems. This variation may in part be due to the spatial or landscape context in which hese trophic cascades occur. In 2011 and 2012, we conducted a natural enemy exclusion experiment in soybean fields along a gradient of landscape composition across southern Wisconsin and Michigan, USA. We used structural equation modeling to ask (1) whether natural enemies influence biocontrol of soybean aphids (SBA) and soybean yield and (2) whether landscape effects on natural enemies influence the strength of the trophic cascades. We found that natural enemies (NE) suppressed aphid populations in both years of our study, and, in 2011, the yield of soybean plants exposed to natural enemies was 37% higher than the yield of plants with aphid populations protected from natural enemies. The strength of the :rophic cascade was also influenced by landscape context. We found that landscapes with a higher proportion of soybean and higher diversity habitats resulted in more NE, fewer aphids, and, in some cases, a trend toward greater soybean yield. These results indicate that landscape context is important for understanding spatial variability in biocontrol and yield, but other factors, such as environmental variability and compensatory growth, might overwhelm the beneficial effects of biocontrol on crop yield.

Stage-dependent responses to emergent habitat heterogeneity: consequences for a predatory insect population in a coffee agroecosystem.

Interactions among members of biological communities can create spatial patterns that effectively generate habitat heterogeneity for other members in the community, and this heterogeneity might be crucial for their persistence. For example, stage-dependent vulnerability of a predatory lady beetle to aggression of the ant, Azteca instabilis, creates two habitat types that are utilized differently by the immature and adult life stages of the beetle. Due to a mutualistic association between A. instabilis and the hemipteran Coccus viridis - which is A. orbigera main prey in the area - only plants around ant nests have high C. viridis populations. Here, we report on a series of surveys at three different scales aimed at detecting how the presence and clustered distribution of ant nests affect the distribution of the different life stages of this predatory lady beetle in a coffee farm in Chiapas, Mexico. Both beetle adults and larvae were more abundant in areas with ant nests, but adults were restricted to the peripheries of highest ant activity and outside the reach of coffee bushes containing the highest densities of lady beetle larvae. The abundance of adult beetles located around trees with ants increased with the size of the ant nest clusters but the relationship is not significant for larvae. Thus, we suggest that A. orbigera undergoes an ontogenetic niche shift, not through shifting prey species, but through stage-specific vulnerability differences against a competitor that renders areas of abundant prey populations inaccessible for adults but not for larvae. Together with evidence presented elsewhere, this study shows how an important predator is not only dependent on the existence of two qualitatively distinct habitat types, but also on the spatial distribution of these habitats. We suggest that this dependency arises due to the different responses that the predator's life stages have to this emergent spatial pattern.

Perennial grasslands enhance biodiversity and multiple ecosystem services in bioenergy landscapes.

Agriculture is being challenged to provide food, and increasingly fuel, for an expanding global population. Producing bioenergy crops on marginal lands--farmland suboptimal for food crops--could help meet energy goals while minimizing competition with food production. However, the ecological costs and benefits of growing bioenergy feedstocks--primarily annual grain crops--on marginal lands have been questioned. Here we show that perennial bioenergy crops provide an alternative to annual grains that increases biodiversity of multiple taxa and sustain a variety of ecosystem functions, promoting the creation of multifunctional agricultural landscapes. We found that switchgrass and prairie plantings harbored significantly greater plant, methanotrophic bacteria, arthropod, and bird diversity than maize. Although biomass production was greater in maize, all other ecosystem services, including methane consumption, pest suppression, pollination, and conservation of grassland birds, were higher in perennial grasslands. Moreover, we found that the linkage between biodiversity and ecosystem services is dependent not only on the choice of bioenergy crop but also on its location relative to other habitats, with local landscape context as important as crop choice in determining provision of some services. Our study suggests that bioenergy policy that supports coordinated land use can diversify agricultural landscapes and sustain multiple critical ecosystem services.

Cascading trait-mediated interactions induced by ant pheromones.

Trait-mediated indirect interactions (TMII) can be as important as density-mediated indirect interactions. Here, we provide evidence for a novel trait-mediated cascade (where one TMII affects another TMII) and demonstrate that the mechanism consists of a predator eavesdropping on chemical signaling. Ants protect scale insects from predation by adult coccinellid beetles - the first TMII. However, parasitic phorid flies reduce ant foraging activity by 50% - the second TMII, providing a window of opportunity for female beetles to oviposit in high-quality microsites. Beetle larvae are protected from ant predation and benefit from living in patches with high scale densities. We demonstrate that female beetles can detect pheromones released by the ant when attacked by phorids, and that only females, and especially gravid females, are attracted to the ant pheromone. As ants reduce their movement when under attack by phorids, we conclude that phorids facilitate beetle oviposition, thus producing the TMII cascade.

Ecological complexity in a coffee agroecosystem: spatial heterogeneity, population persistence and biological control.

BACKGROUND: Spatial heterogeneity is essential for the persistence of many inherently unstable systems such as predator-prey and parasitoid-host interactions. Since biological interactions themselves can create heterogeneity in space, the heterogeneity necessary for the persistence of an unstable system could be the result of local interactions involving elements of the unstable system itself. METHODOLOGY/PRINCIPAL FINDINGS: Here we report on a predatory ladybird beetle whose natural history suggests that the beetle requires the patchy distribution of the mutualism between its prey, the green coffee scale, and the arboreal ant, Azteca instabilis. Based on known ecological interactions and the natural history of the system, we constructed a spatially-explicit model and showed that the clustered spatial pattern of ant nests facilitates the persistence of the beetle populations. Furthermore, we show that the dynamics of the beetle consuming the scale insects can cause the clustered distribution of the mutualistic ants in the first place. CONCLUSIONS/SIGNIFICANCE: From a theoretical point of view, our model represents a novel situation in which a predator indirectly causes a spatial pattern of an organism other than its prey, and in doing so facilitates its own persistence. From a practical point of view, it is noteworthy that one of the elements in the system is a persistent pest of coffee, an important world commodity. This pest, we argue, is kept within limits of control through a complex web of ecological interactions that involves the emergent spatial pattern.

Mutualisms and population regulation: mechanism matters.

For both applied and theoretical ecological science, the mutualism between ants and their hemipteran partners is iconic. In this well-studied interaction, ants are assumed to provide hemipterans protection from natural enemies in exchange for nutritive honeydew. Despite decades of research and the potential importance in pest control, the precise mechanism producing this mutualism remains contested. By analyzing maximum likelihood parameter estimates of a hemipteran population model, we show that the mechanism of the mutualism is direct, via improved hemipteran growth rates, as opposed to the frequently assumed indirect mechanism, via harassment of the specialist parasites and predators of the hemipterans. Broadly, this study demonstrates that the management of mutualism-based ecosystem services requires a mechanistic understanding of mutualistic interactions. A consequence of this finding is the counter intuitive demonstration that preserving ant participation in the ant-hemipteran mutualism may be the best way of insuring pest control.

Cheating on a mutualism: indirect benefits of ant attendance to a coccidophagous coccinellid.

Coccinellids (Coleoptera: Coccinellidae) are generally unable to prey on ant-tended prey. However, particular coccinellid species have morphological, behavioral, or chemical characteristics that render them immune to ant attacks, and some species are even restricted to ant-tending areas. The benefit gained from living in close association with ants can be twofold: (1) gaining access to high-density prey areas and (2) gaining enemy-free space. Here, the myrmecophily of Azya orbigera Mulsant (Coleoptera: Coccinellidae), an important predator of the green coffee scale, Coccus viridis (Green) (Hemiptera: Coccidae), is reported. In this paper, three main questions were studied. (1) Are the waxy filaments of A. orbigera larvae effective as defense against attacks of the mutualistic ant partner of C. viridis, Azteca instabilis F. Smith (Hymenoptera: Formicidae)? (2) Does A. instabilis reduce the rate at which A. orbigera larvae prey on scales? (3) Do A. orbigera larvae gain enemy-free space by living in close association with A. instabilis? Laboratory and field experiments were conducted to answer these questions. We found that, because of the sticky waxy filaments of A. orbigera larvae, A. instabilis is incapable of effectively attacking them and, therefore, the predation rate of A. orbigera on C. viridis does not decrease in the presence of ants. Furthermore, A. instabilis showed aggressive behavior toward A. orbigera's parasitoids, and the presence of ants reduced the parasitism suffered by A. orbigera. This is the first time that this kind of indirect positive effect is reported for an ant and a coccidophagous coccinellid. Furthermore, this indirect positive effect may be key to the persistence of A. orbigera's populations.

Effects of predation pressure on species packing on a resource gradient: insights from nonlinear dynamics.

The classical case of three competitors arranged on a resource gradient such that the central competitor will be excluded due to competition from the other two is studied from the point of view of the effects of added predators. The basic formulation is motivated by a desire to understand the effects of asymmetries in multidimensional Lotka-Volterra systems. We first study the effects of perfectly specialist predators and find a rich collection of possible behaviors of the system including (1) extinction of all predators and subsequent extinction of the subordinate competitor, (2) dominant competitors and their predators coexist but the subdominant competitor goes extinct, (3) all species except the predator of the subordinate competitor coexist in coordinated phase-reversed chaos, (4) exclusion of one or more species occurs through an expanding heteroclinic cycle, and (5) all species coexist in an uncoordinated chaos. We then study the effects of five qualitatively distinct forms of polyphagy. In one case, corresponding to the well-known vulnerability to predation versus competitive ability trade-off, it is possible to have the subordinate competitor be the only survivor in the system. The other three cases of polyphagy lead to distortions in the basic pattern seen in the previously analyzed specialist case. Studying this case of ecologically motivated asymmetries in the basic Lotka-Volterra formulation is a step in the direction of fully understanding interacting populations.