Histoecology: Applying Ecological Principles and Approaches to Describe and Predict Tumor Ecosystem Dynamics Across Space and Time.

Cancer cells exist within a complex spatially structured ecosystem composed of resources and different cell types. As the selective pressures imposed by this environment determine the fate of cancer cells, an improved understanding of how this ecosystem evolves will better elucidate how tumors grow and respond to therapy. State of the art imaging methods can now provide highly resolved descriptions of the microenvironment, yielding the data required for a thorough study of its role in tumor growth and treatment resistance. The field of landscape ecology has been studying such species-environment relationship for decades, and offers many tools and perspectives that cancer researchers could greatly benefit from. Here, we discuss one such tool, species distribution modeling (SDM), that has the potential to, among other things, identify critical environmental factors that drive tumor evolution and predict response to therapy. SDMs only scratch the surface of how ecological theory and methods can be applied to cancer, and we believe further integration will take cancer research in exciting new and productive directions. Significance: Here we describe how species distribution modeling can be used to quantitatively describe the complex relationship between tumor cells and their microenvironment. Such a description facilitates a deeper understanding of cancers eco-evolutionary dynamics, which in turn sheds light on the factors that drive tumor growth and response to treatment.

Birds suppress pests in corn but release them in soybean crops within a mixed prairie/agriculture system.

Birds provide ecosystem services (pest control) in many agroecosystems and have neutral or negative ecological effects (disservices) in others. Large-scale, conventional row crop agriculture is extremely widespread globally, yet few studies of bird effects take place in these agroecosystems. We studied indirect effects of insectivorous birds on corn and soybean crops in fields adjacent to a prairie in Illinois (USA). We hypothesized that prairie birds would forage for arthropods in adjacent crop fields and that the magnitude of services or disservices would decrease with distance from the prairie. We used bird-excluding cages over crops to examine the net effect of birds on corn and soybean grain yield. We also conducted DNA metabarcoding to identify arthropod prey in fecal samples from captured birds. Our exclosure experiments revealed that birds provided net services in corn and net disservices in soybeans. Distance from prairie was not a significant predictor of exclosure treatment effect in either crop. Many bird fecal samples contained DNA from both beneficial arthropods and known economically significant pests of corn, but few economically significant pests of soybeans. Song Sparrows (Melospiza melodia), one of our most captured species, most commonly consumed corn rootworms, an economically significant pest of corn crops. We estimated that birds in this system provided a service worth approximately US $275 ha-1 in corn yield gain, and a disservice valued at approximately $348 ha-1 in soybean yield loss. Our study is the first to demonstrate that birds can provide substantial and economically valuable services in field corn, and disservices in soybean crops. The contrasting findings in the 2 crop systems suggest a range of bird impacts within widespread agroecosystems and demonstrate the importance of quantifying net trophic effects.

Las aves brindan servicios ecosistémicos (control de plagas) en muchos agro-ecosistemas y tienen efectos ecológicos neutrales o negativos (deservicios) en otros. La agricultura convencional a gran escala de cultivos en hilera está ampliamente distribuida a escala global, pero a pesar de esto se han realizado pocos estudios de los efectos de las aves en estos agro-ecosistemas. Estudiamos los efectos indirectos de las aves insectívoras en cultivos de maíz y soja en campos adyacentes a una pradera en Illinois (EEUU). Hipotetizamos que las aves de pradera forrajearían en busca de artrópodos en los campos de cultivo adyacentes y que la magnitud de los servicios o deservicios disminuiría con la distancia desde la pradera. Usamos jaulas de exclusión de aves sobre los cultivos para examinar el efecto neto de las aves en el rendimiento de granos de maíz y soja. También utilizamos el método de código de barras de ADN para identificar presas de artrópodos en las muestras de heces de las aves capturadas. Nuestros experimentos de exclusión revelaron que las aves brindaron servicios netos en el maíz y deservicios netos en la soja. La distancia a las praderas no fue un predictor significativo del efecto del tratamiento de exclusión en ninguno de los cultivos. Muchas muestras de heces de aves contuvieron ADN tanto de artrópodos benéficos como de plagas económicamente significativas de maíz, pero de pocas plagas económicamente significativas de soja. Melospiza melodia, una de nuestras especies más capturadas, mayormente consumió el gusano de la raíz del maíz, una plaga económicamente significativa de este cultivo. Estimamos que las aves en este sistema brindaron un servicio valuado en aproximadamente US $275 ha­1 de ganancias en rendimiento de maíz, y un deservicio valuado en aproximadamente $348 ha­1 de pérdidas en rendimiento de soja. Nuestro estudio es el primero en demostrar que las aves pueden brindar servicios substanciales y económicamente valiosos en los campos de maíz y deservicios en los cultivos de soja. Los hallazgos contrastantes en los dos sistemas de cultivo sugieren un rango de impactos de las aves dentro de los agro-ecosistemas ampliamente distribuidos y demuestra la importancia de cuantificar los efectos tróficos netos.

The city as a refuge for insect pollinators.

Research on urban insect pollinators is changing views on the biological value and ecological importance of cities. The abundance and diversity of native bee species in urban landscapes that are absent in nearby rural lands evidence the biological value and ecological importance of cities and have implications for biodiversity conservation. Lagging behind this revised image of the city are urban conservation programs that historically have invested in education and outreach rather than programs designed to achieve high-priority species conservation results. We synthesized research on urban bee species diversity and abundance to determine how urban conservation could be repositioned to better align with new views on the ecological importance of urban landscapes. Due to insect pollinators' relatively small functional requirements-habitat range, life cycle, and nesting behavior-relative to larger mammals, we argue that pollinators put high-priority and high-impact urban conservation within reach. In a rapidly urbanizing world, transforming how environmental managers view the city can improve citizen engagement and contribute to the development of more sustainable urbanization.

Restored connectivity facilitates recruitment by an endemic large-seeded tree in a fragmented tropical landscape.

Many large-seeded Neotropical trees depend on a limited guild of animals for seed dispersal. Fragmented landscapes reduce animal abundance and movement, limiting seed dispersal between distant forest remnants. In 2006, experimental plantings were established in pasture to determine whether plantings enhance seed dispersal and, ultimately, seedling recruitment. We examined patterns of naturally recruited seedlings of Ocotea uxpanapana, a large-seeded bird-dispersed tree endemic to southern Mexico that occurs in the surrounding landscape. We used GIS and least-cost path analysis to ask: (1) Do restoration efforts alter recruitment patterns? (2) What is the importance of canopy cover and likely dispersal pathways to establishment? Patterns of seedling establishment indicated that dispersal agents crossed open pastures to wooded plots. Recruitment was greatest under woody canopies. Also, by reducing movement cost or risk for seed dispersers, wooded canopies increased influx of large, animal-dispersed seeds, thereby restoring a degree of functional connectivity to the landscape. Together, canopy openness and path distance from potential parent trees in the surrounding landscape explained 73% of the variance in O. uxpanapana seedling distribution. Preliminary results suggest that strategic fenced plantings in pastures increase dispersal and establishment of large-seeded trees, thereby accelerating forest succession in restorations and contributing to greater connectivity among forest fragments.

Pathology to enhance precision medicine in oncology: lessons from landscape ecology.

A major goal of modern medicine is increasing patient specificity so that the right treatment is administered to the right patient at the right time with the right dose. While current cancer studies have largely focused on identification of genetic or epigenetic properties of tumor cells, emerging evidence has clearly demonstrated substantial genetic heterogeneity between tumors in the same patient and within subclones of a single tumor. Thus, molecular analysis from populations of cells (either a whole tumor or small biopsy of that tumor) is, at best, an incomplete representation of the underlying biology. These observations indicate a significant need to define intratumoral evolutionary dynamics that yield the observed spatial variations in cellular properties. It is generally accepted that genetic heterogeneity among cancer cells is a manifestation of intratumoral evolution, and this is typically viewed as a consequence of random mutations generated by genomic instability within the cancer cells. We suggest that this represents an incomplete view of Darwinian dynamics, which typically are governed by phenotypic variations in response to spatial and temporal heterogeneity in environmental selection forces. We propose that pathologic feature analysis can provide precise information regarding regional variations in environmental selection forces and phenotypic adaptations. These observations can be integrated using quantitative, spatially explicit methods developed in landscape ecology to interrogate heterogenous biological processes in tumors within individual patients. The ability to investigate tumor heterogeneity has been shown to inform physicians regarding critical aspects of cancer progression including invasion, metastasis, drug resistance, and disease relapse.

Diversity of wild bees supports pollination services in an urbanized landscape.

Plantings in residential neighborhoods can support wild pollinators. However, it is unknown how effectively wild pollinators maintain pollination services in small, urban gardens with diverse floral resources. We used a 'mobile garden' experimental design, whereby potted plants of cucumber, eggplant, and purple coneflower were brought to 30 residential yards in Chicago, IL, USA, to enable direct assessment of pollination services provided by wild pollinator communities. We measured fruit and seed set and investigated the effect of within-yard characteristics and adjacent floral resources on plant pollination. Increased pollinator visitation and taxonomic richness generally led to increases in fruit and seed set for all focal plants. Furthermore, fruit and seed set were correlated across the three species, suggesting that pollination services vary across the landscape in ways that are consistent among different plant species. Plant species varied in terms of which pollinator groups provided the most visits and benefit for pollination. Cucumber pollination was linked to visitation by small sweat bees (Lasioglossum spp.), whereas eggplant pollination was linked to visits by bumble bees. Purple coneflower was visited by the most diverse group of pollinators and, perhaps due to this phenomenon, was more effectively pollinated in florally-rich gardens. Our results demonstrate how a diversity of wild bees supports pollination of multiple plant species, highlighting the importance of pollinator conservation within cities. Non-crop resources should continue to be planted in urban gardens, as these resources have a neutral and potentially positive effect on crop pollination.

Effect of Number of Bombus impatiens (Hymenoptera: Apidae) Visits on Eggplant Yield.

Eggplant (Solanum melongena L.) is a crop with perfect flowers capable of self-pollination. Insect pollination enhances fruit set, but little is known about how pollination success varies by number of visits from bumble bees. To quantify the efficiency of bumble bees at pollinating eggplants, we allowed 1, 2, 6, and 12 bumble bees (Bombus impatiens Cresson) to visit eggplant flowers and compared percentage of flowers that set fruit, fruit weight, and seed set after 3 wk. We compared yield from these visit numbers to eggplant flowers that were left open for unlimited visitation. Eggplant flowers set the most fruit from open-pollination and 12 visits. Larger, seedier fruits were formed in open-pollinated flowers. However, fruit characteristics in the 12 visit treatment were similar to lower visitation frequencies. We confirm B. impatiens as an efficient eggplant pollinator and document the greatest benefit from 12 bumble bee visits and open-pollinated flowers. To maintain effective eggplant pollination, local conditions must be conducive for bumble bee colony establishment and repeated pollen foraging trips.

Having our yards and sharing them too: the collective effects of yards on native bird species in an urban landscape.

Residential yards comprise a substantial portion of urban landscapes, and the collective effects of the management of many individual yards may "scale up" to affect urban biodiversity. We conducted bird surveys and social surveys in Chicago-area (Illinois, USA) residential neighborhoods to identify the relative importance of yard design and management activities for native birds. We found that groups of neighboring yards, in the aggregate, were more important for native bird species richness than environmental characteristics at the neighborhood or landscape scale. The ratio of evergreen to deciduous trees in yards and the percentage of yards with trees and plants with fruits or berries were positively associated with native bird species richness, whereas the number of outdoor cats had a negative association. The number of birdfeeders was not an important predictor for native species richness. We also found that migratory birds were observed on transects with more wildlife-friendly features in yards, and nonnative birds were observed on transects with greater numbers of outdoor cats and dogs. Our results highlight the potential importance of residential matrix management as a conservation strategy in urban areas.

Landscape connectivity and seed dispersal characteristics inform the best management strategy for exotic plants.

Exotic plant invasions have triggered environmental and economic problems throughout the world. Our ability to manage these invasions is hindered by the difficulty of predicting spread in fragmented landscapes. Because the spatial pattern of invasions depends on the dispersal characteristics of the invasive species and the configuration of suitable habitat within the landscape, a universal management strategy is unlikely to succeed for any particular species. We suggest that the most effective management strategy may be an adaptive one that shifts from local control to landscape management depending on the specific invader and landscape. In particular, we addressed the question of where management activities should be focused to minimize spread of the invading species. By simulating an invasion across a real landscape (Antietam National Battlefield in Maryland, USA), we examined the importance of patch size and connectivity to management success. We found that the best management strategy depended on the dispersal characteristics of the exotic species. Species with a high probability of random long-distance dispersal were best managed by focusing on the largest patches, while species with a lower probability of random long-distance dispersal were best managed by considering landscape configuration and connectivity of the patches. Connectivity metrics from network analysis were useful for identifying the most effective places to focus management efforts. These results provide insight into invasion patterns of various species and suggest a general rule for managers in National Parks and other places where invasive species are a concern.

Assessing four methods for establishing native plants on urban vacant land.

Urban greening increases vegetation and can restore ecological functions to urban systems. It has ties to restoration ecology, which aims to return degraded land to diverse, functional ecosystems. Both practices can be applied to maximizing ecosystem services and habitat in vacant lots, which are abundant in post-industrial cities, including Chicago, Illinois (USA), where our study took place. We tested four methods for increasing native plant diversity in vacant lots, ranging from low input to resource-intensive: seed bombing, broadcast seeding, planting plugs, and gardening. After three growing seasons, we assessed the growth of eight target native species and all non-target species. We expected that intensive treatments would have more target species stems and flowers and fewer non-target species, but we found that less-intensive options often produce equal or better results. From this, we recommend broadcast seeding as a viable, low-cost method for improving habitat and biodiversity in vacant lots.

Butterfly declines in protected areas of Illinois: Assessing the influence of two decades of climate and landscape change.

Despite increasing concern regarding broad-scale declines in insects, there are few published long-term, systematic butterfly surveys in North America, and fewer still that have incorporated the influence of changing climate and landscape variables. In this study, we analyzed 20 years of citizen science data at seven consistently monitored protected areas in Illinois, U.S.A. We used mixed models and PERMANOVA to evaluate trends in butterfly abundance, richness, and composition while also evaluating the effects of temperature and land use. Overall butterfly richness, but not abundance, increased in warmer years. Surprisingly, richness also was positively related to percent impervious surface (at the 2 km radius scale), highlighting the conservation value of protected areas in urban landscapes (or alternately, the potential negative aspects of agriculture). Precipitation had a significant and variable influence through time on overall butterfly abundance and abundance of resident species, larval host plant specialists, and univoltine species. Importantly, models incorporating the influence of changing temperature, precipitation, and impervious surface indicated a significant overall decline in both butterfly abundance and species richness, with an estimated abundance decrease of 3.8%/year and richness decrease of 1.6%/year (52.5% and 27.1% cumulatively from 1999 to 2018). Abundance and richness declines were also noted across all investigated functional groups except non-resident (migratory) species. Butterfly community composition changed through time, but we did not find evidence of systematic biotic homogenization, perhaps because declines were occurring in nearly all functional groups. Finally, at the site-level, declines in either richness or abundance occurred at five of seven locations, with only the two largest locations (>300 Ha) not exhibiting declines. Our results mirror those of other long-term butterfly studies predominantly in Europe and North America that have found associations of butterflies with climate variables and general declines in butterfly richness and abundance.

A multiscale network analysis of protected-area connectivity for mammals in the United States.

Protected areas must be close, or connected, enough to allow for the preservation of large-scale ecological and evolutionary processes, such as gene flow, migration, and range shifts in response to climate change. Nevertheless, it is unknown whether the network of protected areas in the United States is connected in a way that will preserve biodiversity over large temporal and spatial scales. It is also unclear whether protected-area networks that function for larger species will function for smaller species. We assessed the connectivity of protected areas in the three largest biomes in the United States. With methods from graph theory--a branch of mathematics that deals with connectivity and flow--we identified and measured networks of protected areas for three different groups of mammals. We also examined the value of using umbrella species (typically large-bodied, far-ranging mammals) in designing large-scale networks of protected areas. Although the total amount of protected land varied greatly among biomes in the United States, overall connectivity did not. In general, protected-area networks were well connected for large mammals but not for smaller mammals. Additionally, it was not possible to predict connectivity for small mammals on the basis of connectivity for large mammals, which suggests the umbrella species approach may not be an appropriate design strategy for conservation networks intended to protect many species. Our findings indicate different strategies should be used to increase the likelihood of persistence for different groups of species. Strategic linkages of existing lands should be a conservation priority for smaller mammals, whereas conservation of larger mammals would benefit most from the protection of more land.

Graph models of habitat mosaics.

Graph theory is a body of mathematics dealing with problems of connectivity, flow, and routing in networks ranging from social groups to computer networks. Recently, network applications have erupted in many fields, and graph models are now being applied in landscape ecology and conservation biology, particularly for applications couched in metapopulation theory. In these applications, graph nodes represent habitat patches or local populations and links indicate functional connections among populations (i.e. via dispersal). Graphs are models of more complicated real systems, and so it is appropriate to review these applications from the perspective of modelling in general. Here we review recent applications of network theory to habitat patches in landscape mosaics. We consider (1) the conceptual model underlying these applications; (2) formalization and implementation of the graph model; (3) model parameterization; (4) model testing, insights, and predictions available through graph analyses; and (5) potential implications for conservation biology and related applications. In general, and for a variety of ecological systems, we find the graph model a remarkably robust framework for applications concerned with habitat connectivity. We close with suggestions for further work on the parameterization and validation of graph models, and point to some promising analytic insights.

The role of landscape connectivity in assembling exotic plant communities: a network analysis.

Landscape fragmentation and exotic species invasions are two modern-day forces that have strong and largely irreversible effects on native diversity worldwide. The spatial arrangement of habitat fragments is critical in affecting movement of individuals through a landscape, but little is known about how invasive species respond to landscape configuration relative to native species. This information is crucial for managing the global threat of invasive species spread. Using network analysis and partial Mantel tests to control for covarying environmental conditions, we show that forest plant communities in a fragmented landscape have spatial structure that is best captured by a network representation of landscape connectivity. This spatial structure is less pronounced in invasive species and exotic species dispersed by animals. Our research suggests that invasive species can spread more easily in fragmented landscapes than native species, which may make communities more homogeneous over time.

Assessing social and biophysical drivers of spontaneous plant diversity and structure in urban vacant lots.

Vacant lots are typically viewed as urban blight but are also green spaces that provide wildlife habitat and ecosystem services in urban landscapes. Vacant lot vegetation results from interacting biophysical and social forces, and studying vacant lot ecology is an opportunity to examine urban socio-environmental intersections. Here, we assess vegetation patterns in vacant lots across Chicago, IL (USA), and ask two questions: 1) How does diversity and structure vary, and 2) how do social and biophysical drivers contribute to this variation? We conducted vegetation surveys in 35 vacant lots in the summer of 2015. In each lot, we identified all herbaceous plants (excluding turf grasses) and woody seedlings and measured species richness, evenness, vegetation height, and total vegetated area. We used field sampled data about human activities and land use in vacant lots (e.g., presence of a path, trash and turf), coupled with sociodemographic data (e.g., income, ethnicity), and fine-scale land cover to construct two models for each vegetation measure: a best-fit biophysical model and a best-fit social model. We then used variation partitioning to compare the relative strength of these models and any overlap between them. In total, we identified 109 plant species. Species evenness was high, suggesting that there are few rare species in this system. Species richness and vegetation height were better explained by social models, while vegetated area and evenness were better explained by biophysical models. We saw evidence of overlapping explanatory power between the social and biophysical domains. The amount of trash in a lot was the most significant variable, explaining three of our vegetation measures. Lots with higher amounts of trash had higher richness and evenness, and lower vegetated area. This assessment of patterns of vegetation in Chicago's vacant lots provides insight into how habitat differs across the city and informs urban conservation paradigms.

A graph-theory framework for evaluating landscape connectivity and conservation planning.

Connectivity of habitat patches is thought to be important for movement of genes, individuals, populations, and species over multiple temporal and spatial scales. We used graph theory to characterize multiple aspects of landscape connectivity in a habitat network in the North Carolina Piedmont (U.S.A). We compared this landscape with simulated networks with known topology, resistance to disturbance, and rate of movement. We introduced graph measures such as compartmentalization and clustering, which can be used to identify locations on the landscape that may be especially resilient to human development or areas that may be most suitable for conservation. Our analyses indicated that for songbirds the Piedmont habitat network was well connected. Furthermore, the habitat network had commonalities with planar networks, which exhibit slow movement, and scale-free networks, which are resistant to random disturbances. These results suggest that connectivity in the habitat network was high enough to prevent the negative consequences of isolation but not so high as to allow rapid spread of disease. Our graph-theory framework provided insight into regional and emergent global network properties in an intuitive and visual way and allowed us to make inferences about rates and paths of species movements and vulnerability to disturbance. This approach can be applied easily to assessing habitat connectivity in any fragmented or patchy landscape.

Graph theory as a proxy for spatially explicit population models in conservation planning.

Spatially explicit population models (SEPMs) are often considered the best way to predict and manage species distributions in spatially heterogeneous landscapes. However, they are computationally intensive and require extensive knowledge of species' biology and behavior, limiting their application in many cases. An alternative to SEPMs is graph theory, which has minimal data requirements and efficient algorithms. Although only recently introduced to landscape ecology, graph theory is well suited to ecological applications concerned with connectivity or movement. This paper compares the performance of graph theory to a SEPM in selecting important habitat patches for Wood Thrush (Hylocichla mustelina) conservation. We use both models to identify habitat patches that act as population sources and persistent patches and also use graph theory to identify patches that act as stepping stones for dispersal. Correlations of patch rankings were very high between the two models. In addition, graph theory offers the ability to identify patches that are very important to habitat connectivity and thus long-term population persistence across the landscape. We show that graph theory makes very similar predictions in most cases and in other cases offers insight not available from the SEPM, and we conclude that graph theory is a suitable and possibly preferable alternative to SEPMs for species conservation in heterogeneous landscapes.