Intransitivity as a dynamic assembly engine of competitive communities.

Historically, those ecological communities thought to be dominated by competitive interactions among their component species have been assumed to exhibit transitive competition, that is, a hierarchy of competitive strength from most dominant to most submissive. A surge of recent literature takes issue with this assumption and notes that some species in some communities are intransitive, where a rock/scissors/paper arrangement characterizes some components of some communities. We here propose a merging of these two ideas, wherein an intransitive subgroup of species connects with a distinct subcomponent that is organized hierarchically, such that the expected eventual takeover by the dominant competitor in the hierarchy is thwarted, and the entire community can be sustained. This means that the combination of transitive and intransitive structures can maintain many species even when competition is strong. Here, we develop this theoretical framework using a simple variant on the Lotka-Volterra competition equations to illustrate the process. We also present data for the ant community in a coffee agroecosystem in Puerto Rico, that appears to be organized in this way. A detailed study on one typical coffee farm illustrates an intransitive loop of three species that seems to maintain a distinct competitive community of at least 13 additional species.

Tree Effects on Coffee Leaf Rust at Field and Landscape Scales.

Although integrating trees into agricultural systems (i.e., agroforestry systems) provides many valuable ecosystem services, the trees can also interact with plant diseases. We demonstrate that a detailed understanding of how plant diseases interact with trees in agroforestry systems is necessary to identify key tree canopy characteristics, leaf traits, spatial arrangements, and management options that can help control plant diseases at different spatial scales. We focus our analysis on how trees affect coffee leaf rust, a major disease affecting one of the world's most significant crop commodities. We show that trees can both promote and discourage the development of coffee leaf rust at the plot scale via microclimate modifications in the understory. Based on our understanding of the role of tree characteristics in shaping the microclimate, we identify several canopy characteristics and leaf traits that can help manage coffee leaf rust at the plot scale: namely, thin canopies with high openness, short base height, horizontal branching, and small, dentate leaves. In contrast, at the edge of coffee farms, having large trees with high canopy volume and small, thick, waxy leaves is more useful to reduce throughflow wind speeds and intercept the airborne dispersal of urediniospores, an important consideration to control disease at the landscape scale. Seasonal pruning can help shape trees into the desired form, and trees can be spatially arranged to optimize desired effects. This case study demonstrates the added value of combining process-based epidemiology studies with functional trait ecology to improve disease management in agroforestry systems.

The effects of ants on pest control: a meta-analysis.

Environmental impacts of conventional agriculture have generated interest in sustainable agriculture. Biological pest control is a fundamental tool, and ants are key players providing ecological services, as well as some disservices. We have used a meta-analytical approach to investigate the contribution of ants to biological control, considering their effects on pest and natural enemy abundance, plant damage and crop yield. We also evaluated whether the effects of ants are modulated by traits of ants, pests and other natural enemies, as well as by field size, crop system and experiment duration. Overall (considering all meta-analyses), from 52 studies on 17 different crops, we found that ants decrease the abundance of non-honeydew-producing pests, decrease plant damage and increase crop yield (services). In addition, ants decrease the abundance of natural enemies, mainly the generalist ones, and increase honeydew-producing pest abundance (disservices). We show that the pest control and plant protection provided by ants are boosted in shaded crops compared to monocultures. Furthermore, ants increase crop yield in shaded crops, and this effect increases with time. Finally, we bring new insights such as the importance of shaded crops to ant services, providing a good tool for farmers and stakeholders considering sustainable farming practices.

An aggressive nonconsumptive effect mediates pest control and multipredator interactions in a coffee agroecosystem.

Natural pest control is an alternative to pesticide use in agriculture, and may help to curb insect declines and promote crop production. Nonconsumptive interactions in natural pest control that historically have received far less attention than consumptive interactions, may have distinct impacts on pest damage suppression and may also mediate positive multipredator interactions. Additionally, when nonconsumptive effects are driven by natural enemy aggression, variation in alternative resources for enemies may impact the strength of pest control. Here we study control of the coffee berry borer (CBB), Hypothenemus hampei, by a keystone arboreal ant species, Azteca sericeasur, which exhibits a nonconsumptive effect on CBB by throwing them off coffee plants. We conducted two experiments to investigate: (1) if the strength of this behavior is driven by spatial or temporal variability in scale insect density (an alternative resource that Azteca tends for honeydew), (2) if this behavior mediates positive interactions between Azteca and other ground-foraging ants, and (3) the effect this behavior has on the overall suppression of CBB damage in multipredator scenarios. Our behavioral experiment showed that nearly all interactions between Azteca and CBB are nonconsumptive and that this behavior occurs more frequently in the dry season and with higher densities of scale insects on coffee branches. Our multipredator experiment revealed that borers thrown off coffee plants by Azteca can survive and potentially damage other nearby plants but may be suppressed by ground-foraging ants. Although we found no non-additive effects between Azteca and ground-foraging ants on overall CBB damage, together, both species resulted in the lowest level of plant damage with the subsequent reduction in "spillover" damage caused by thrown CBB, indicating spatial complementarity between predators. These results present a unique case of natural pest control, in which damage suppression is driven almost exclusively by nonconsumptive natural enemy aggression, as opposed to consumption or prey behavioral changes. Furthermore, our results demonstrate the variability that may occur in nonconsumptive pest control interactions when natural enemy aggressive behavior is impacted by alternative resources, and also show how these nonconsumptive effects can mediate positive interactions between natural enemies to enhance overall crop damage reduction.

Hysteresis and critical transitions in a coffee agroecosystem.

Seeking to employ ecological principles in agricultural management, a classical ecological debate provides a useful framing. Whether ecosystems are controlled from above (predators are the limiting force over herbivores) or from below (overutilization of plant resources is the limiting force over herbivores) is a debate that has motivated much research. The dichotomous nature of the debate (above or below) has been criticized as too limiting, especially in light of contemporary appreciation of ecological complexity-control is more likely from a panoply of direct and indirect interactions. In the context of the agroecosystem, regulation is assumed to be from above and pests are controlled, a way of using ecological insights in service of an essential ecosystem service-pest control. However, this obvious resolution of the old debate does not negate the deeper appreciation of complexity-the natural enemies themselves constitute a complex system. Here we use some key concepts from complexity science to interrogate the natural functioning of pest regulation through spatially explicit dynamics of a predator and a disease operating simultaneously but distributed in space. Using the green coffee scale insect as a focal species, we argue that certain key ideas of complexity science shed light on how that system operates. In particular, a hysteretic pattern associated with distance to a keystone ant is evident.

Endogenous spatial pattern formation from two intersecting ecological mechanisms: the dynamic coexistence of two noxious invasive ant species in Puerto Rico.

Endogenous (or autonomous, or emergent) spatial pattern formation is a subject transcending a variety of sciences. In ecology, there is growing interest in how spatial patterns can 'emerge' from internal system processes and simultaneously affect those very processes. A classic situation emerges when a predator's focus on a dominant competitor releases competitive pressure on a subdominant competitor, allowing coexistence of the two. If this idea is formulated spatially, two interesting consequences immediately arise. First, a spatial predator/prey system may take the form of a Turing instability, in which an activator (the dispersing prey population) is contained by a repressor (the more rapidly dispersing predator population) generating a spatial pattern of clusters of prey and predators, and second, an indirect intransitive loop (where A beats B beats C beats A) emerges from the simple fact that the system is spatial. Two common invasive ant species, Wasmannia auropunctata and Solenopsis invicta, and the parasitic phorid flies of S. invicta commonly coexist in Puerto Rico. Emergent spatial patterns generated by the combination of the Turing mechanism and the indirect intransitive loop are likely to be common here. This theoretical framework and the realities of the natural history in the field could explain both the long-term coexistence of these two species, and the highly variable pattern of their occurrence across a large landscape.

From endogenous to exogenous pattern formation: Invasive plant species changes the spatial distribution of a native ant.

Invasive species are a significant threat to global biodiversity, but our understanding of how invasive species impact native communities across space and time remains limited. Based on observations in an old field in Southeast Michigan spanning 35 years, our study documents significant impacts of habitat change, likely driven by the invasion of the shrub, Elaeagnus umbellata, on the nest distribution patterns and population demographics of a native ant species, Formica obscuripes. Landcover change in aerial photographs indicates that E. umbellata expanded aggressively, transforming a large proportion of the original open field into dense shrubland. By comparing the ant's landcover preferences before and after the invasion, we demonstrate that this species experienced a significant unfavorable change in its foraging areas. We also find that shrub landcover significantly moderates aggression between nests, suggesting nests are more related where there is more E. umbellata. This may represent a shift in reproductive strategy from queen flights, reported in the past, to asexual nest budding. Our results suggest that E. umbellata may affect the spatial distribution of F. obscuripes by shifting the drivers of nest pattern formation from an endogenous process (queen flights), which led to a uniform pattern, to a process that is both endogenous (nest budding) and exogenous (loss of preferred habitat), resulting in a significantly different clustered pattern. The number and sizes of F. obscuripes nests in our study site are projected to decrease in the next 40 years, although further study of this population's colony structures is needed to understand the extent of this decrease. Elaeagnus umbellata is a common invasive shrub, and similar impacts on native species might occur in its invasive range, or in areas with similar shrub invasions.

Floral resource availability from groundcover promotes bee abundance in coffee agroecosystems.

Patterns of bee abundance and diversity across different spatial scales have received thorough research consideration. However, the impact of short- and long-term temporal resource availability on biodiversity has been less explored. This is highly relevant in tropical agricultural systems for pollinators, as many foraging periods of pollinators extend beyond flowering of any single crop species. In this study, we sought to understand how bee communities in tropical agroecosystems changed between seasons, and if short- and long-term floral resource availability influenced their diversity and abundance. We used a threshold analysis approach in order to explore this relationship at two time scales. This study took place in a region dominated by coffee agroecosystems in Southern Mexico. This was an ideal system because the landscape offers a range of coffee management regimes that maintain heterogeneity in floral resource availability spatially and temporally. We found that the bee community varies significantly between seasons. There were higher abundances of native social, solitary and managed honey bees during the dry season when coffee flowers. Additionally, we found that floral resources from groundcover, but not trees, were associated with bee abundance. Further, the temporal scale of the availability of these resources is important, whereby short-term floral resource availability appears particularly important in maintaining high bee abundance at sites with lower seasonal complementarity. We argue that in addition to spatial resource heterogeneity, temporal resource heterogeneity is critical in explaining bee community patterns, and should thus be considered to promote pollinator conservation.

Local and Landscape Constraints on Coffee Leafhopper (Hemiptera: Cicadellidae) Diversity.

The intensification of agriculture drives many ecological and environmental consequences including impacts on crop pest populations and communities. These changes are manifested at multiple scales including small-scale management practices and changes to the composition of land-use types in the surrounding landscape. In this study, we sought to examine the influence of local and landscape-scale agricultural factors on a leafhopper herbivore community in Mexican coffee plantations. We sampled leafhopper (Hemiptera: Cicadellidae) diversity in 38 sites from 9 coffee plantations of the Soconusco region of Chiapas, Mexico. While local management factors such as coffee density, branches per coffee bush, tree species, and density were not important in explaining leafhopper abundance and richness, shade management at the landscape level and elevation significantly affected leafhoppers. Specifically, the percentage of low-shade coffee in the landscape (1,000-m radius surrounding sites) increased total leafhopper abundance. In addition, Shannon's diversity of leafhoppers was increased with coffee density. Our results show that abundance and diversity of leafhoppers are greater in simplified landscapes, thereby suggesting that these landscapes will have higher pest pressure and may be more at-risk for diseases vectored by these species in an economically important crop.

A social-ecological perspective on harmonizing food security and biodiversity conservation.

The major challenges of improving food security and biodiversity conservation are intricately linked. To date, the intersection of food security and biodiversity conservation has been viewed primarily through an agricultural "production lens"-for example, via the land sparing/sharing framework, or the concept of sustainable intensification. However, a productionist perspective has been criticized for being too narrow, and failing to consider other relevant factors, including policy, equity, and diversity. We propose an approach that conceptualizes rural landscapes as social-ecological systems embedded within intersecting multi-scalar processes. Based on such a framing, empirical research can be more clearly set in the context of system properties that may influence food security, biodiversity conservation, or both. We illustrate our approach through a description of contrasting agricultural systems within Brazil's Cerrado region. We emphasize the need for new empirical research involving systematic comparisons of social-ecological system properties in landscapes threatened by food insecurity and ecosystem degradation.

Identification of Putative Coffee Rust Mycoparasites via Single-Molecule DNA Sequencing of Infected Pustules.

The interaction of crop pests with their natural enemies is a fundament to their control. Natural enemies of fungal pathogens of crops are poorly known relative to those of insect pests, despite the diversity of fungal pathogens and their economic importance. Currently, many regions across Latin America are experiencing unprecedented epidemics of coffee rust (Hemileia vastatrix). Identification of natural enemies of coffee rust could aid in developing management strategies or in pinpointing species that could be used for biocontrol. In the present study, we characterized fungal communities associated with coffee rust lesions by single-molecule DNA sequencing of fungal rRNA gene bar codes from leaf discs (≈28 mm(2)) containing rust lesions and control discs with no rust lesions. The leaf disc communities were hyperdiverse in terms of fungi, with up to 69 operational taxonomic units (putative species) per control disc, and the diversity was only slightly reduced in rust-infected discs, with up to 63 putative species. However, geography had a greater influence on the fungal community than whether the disc was infected by coffee rust. Through comparisons between control and rust-infected leaf discs, as well as taxonomic criteria, we identified 15 putative mycoparasitic fungi. These fungi are concentrated in the fungal family Cordycipitaceae and the order Tremellales. These data emphasize the complexity of diverse fungi of unknown ecological function within a leaf that might influence plant disease epidemics or lead to the development of species for biocontrol of fungal disease.

Biodiversity conservation in agriculture requires a multi-scale approach.

Biodiversity loss--one of the most prominent forms of modern environmental change--has been heavily driven by terrestrial habitat loss and, in particular, the spread and intensification of agriculture. Expanding agricultural land-use has led to the search for strong conservation strategies, with some suggesting that biodiversity conservation in agriculture is best maximized by reducing local management intensity, such as fertilizer and pesticide application. Others highlight the importance of landscape-level approaches that incorporate natural or semi-natural areas in landscapes surrounding farms. Here, we show that both of these practices are valuable to the conservation of biodiversity, and that either local or landscape factors can be most crucial to conservation planning depending on which types of organisms one wishes to save. We performed a quantitative review of 266 observations taken from 31 studies that compared the impacts of localized (within farm) management strategies and landscape complexity (around farms) on the richness and abundance of plant, invertebrate and vertebrate species in agro-ecosystems. While both factors significantly impacted species richness, the richness of sessile plants increased with less-intensive local management, but did not significantly respond to landscape complexity. By contrast, the richness of mobile vertebrates increased with landscape complexity, but did not significantly increase with less-intensive local management. Invertebrate richness and abundance responded to both factors. Our analyses point to clear differences in how various groups of organisms respond to differing scales of management, and suggest that preservation of multiple taxonomic groups will require multiple scales of conservation.

Clusters of ant colonies and robust criticality in a tropical agroecosystem.

Although sometimes difficult to measure at large scales, spatial pattern is important in natural biological spaces as a determinant of key ecological properties such as species diversity, stability, resiliency and others. Here we demonstrate, at a large spatial scale, that a common species of tropical arboreal ant forms clusters of nests through a combination of local satellite colony formation and density-dependent control by natural enemies, mainly a parasitic fly. Cluster sizes fall off as a power law consistent with a so-called robust critical state. This endogenous cluster formation at a critical state is a unique example of an insect population forming a non-random pattern at a large spatial scale. Furthermore, because the species is a keystone of a larger network that contributes to the ecosystem function of pest control, this is an example of how spatial dynamics at a large scale can affect ecosystem service at a local level.

Combining intransitive and higher-order effects in a coupled oscillator framework: A case study of an ant community.

A growing body of literature recognizes that pairwise species interactions are not necessarily an appropriate metaphorical molecule of community ecology. Two examples are intransitive competition and nonlinear higher-order effects. While these two processes have been discussed extensively, the explicit analysis of how the two of them behave when simultaneously part of the same dynamic system has not yet been explored theoretically. A concrete situation exists on coffee farms in Puerto Rico in which three ant species form an intransitive competitive triplet, and that triplet is strongly influenced, nonlinearly, by a fly parasitoid that modifies the competitive ability of one of the species. Using this arrangement as a template, we explore the dynamical consequences with a simple ordinary differential equation (ODE) model. Results are complicated and include alternative periodic and chaotic attractors. The qualitative structures of those complications, however, may be approximately retrieved from the basic natural history of the system.

The agroecological matrix as alternative to the land-sparing/agriculture intensification model.

Among the myriad complications involved in the current food crisis, the relationship between agriculture and the rest of nature is one of the most important yet remains only incompletely analyzed. Particularly in tropical areas, agriculture is frequently seen as the antithesis of the natural world, where the problem is framed as one of minimizing land devoted to agriculture so as to devote more to conservation of biodiversity and other ecosystem services. In particular, the "forest transition model" projects an overly optimistic vision of a future where increased agricultural intensification (to produce more per hectare) and/or increased rural-to-urban migration (to reduce the rural population that cuts forest for agriculture) suggests a near future of much tropical aforestation and higher agricultural production. Reviewing recent developments in ecological theory (showing the importance of migration between fragments and local extinction rates) coupled with empirical evidence, we argue that there is little to suggest that the forest transition model is useful for tropical areas, at least under current sociopolitical structures. A model that incorporates the agricultural matrix as an integral component of conservation programs is proposed. Furthermore, we suggest that this model will be most successful within a framework of small-scale agroecological production.

Exploring scenarios for the food system-zoonotic risk interface.

The unprecedented economic and health impacts of the COVID-19 pandemic have shown the global necessity of mitigating the underlying drivers of zoonotic spillover events, which occur at the human-wildlife and domesticated animal interface. Spillover events are associated to varying degrees with high habitat fragmentation, biodiversity loss through land use change, high livestock densities, agricultural inputs, and wildlife hunting-all facets of food systems. As such, the structure and characteristics of food systems can be considered key determinants of modern pandemic risks. This means that emerging infectious diseases should be more explicitly addressed in the discourse of food systems to mitigate the likelihood and impacts of spillover events. Here, we adopt a scenario framework to highlight the many connections among food systems, zoonotic diseases, and sustainability. We identify two overarching dimensions: the extent of land use for food production and the agricultural practices employed that shape four archetypal food systems, each with a distinct risk profile with respect to zoonotic spillovers and differing dimensions of sustainability. Prophylactic measures to curb the emergence of zoonotic diseases are therefore closely linked to diets and food policies. Future research directions should explore more closely how they impact the risk of spillover events.

Surprising effects of cascading higher order interactions.

Most species are embedded in multi-interaction networks. Consequently, theories focusing on simple pair-wise interactions cannot predict ecological and/or evolutionary outcomes. This study explores how cascading higher-order interactions (HOIs) would affect the population dynamics of a focal species. Employing a system that involves a myrmecophylic beetle, a parasitic wasp that attacks the beetle, an ant, and a parasitic fly that attacks the ant, the study explores how none, one, and two HOIs affect the parasitism and the sex ratio of the beetle. We conducted mesocosm experiments to examine these HOIs on beetle survival and sex ratio and found that the 1st degree HOI does not change the beetle's survival rate or sex ratio. However, the 2nd degree HOI significantly reduces the beetle's survival rate and changes its sex ratio from even to strongly female-biased. We applied Bayes' theorem to analyze the per capita survival probability of female vs. male beetles and suggested that the unexpected results might arise from complex eco-evolutionary dynamics involved with the 1st and 2nd degree HOIs. Field data suggested the HOIs significantly regulate the sex ratio of the beetle. As the same structure of HOIs appears in other systems, we believe the complexity associated with the 2nd degree HOI would be more common than known and deserve more scientific attention.

Spatiotemporal Foraging Dynamics of Solenopsis invicta (Hymenoptera: Formicidae) and its Potential Effects on the Spatial Structure of Interspecific Competition.

The ant communities on coffee farms in the West/Central Mountains of Puerto Rico are composed of mainly invasive species, although many have a long history of occupation and are effectively naturalized. The ecological forces that maintain such communities are thus of interest, and are evidently related to the spatial patterns in which they inevitably occur. Furthermore, the spatial patterns in which members of the native ant community forage almost certainly include limitations related to the structure of the networks of subterranean foraging tunnels that extend from the nest mounds of Solenopsis invicta. Here we explore some details of that structure. We ask, what is the pattern of foraging exit holes and the gaps between them, and how does that pattern change from farm to farm and from time to time? We encounter typical underground foraging trails punctuated by foraging exits, which, we propose, create a structure above ground of relatively small foraging exits in a matrix of effective foraging gaps. This pattern varies from nest to nest and farm to farm. Other ant species clearly occupy those gaps and seem to gain some of their resilience in the system from this peculiarity of S. invicta's foraging area structure.

Reduced rainfall and resistant varieties mediate a critical transition in the coffee rust disease.

Critical transitions, sudden responses to slow changes in environmental drivers, are inherent in many dynamic processes, prompting a search for early warning signals. We apply this framework to understanding the coffee rust disease, which experienced an unprecedented outbreak in Mesoamerica in 2012-2013, likely a critical transition. Based on monthly infection data from 128 study quadrats in a 45-ha plot in southern Mexico from 2014 to 2020, we find that the persistent seasonal epidemic following the initial outbreak collapses in an evident subsequent critical transition. Characteristic signals of "critical slowing down" precede this collapse and are correlated with reduced rainfall, as expected from climate change, and planting of rust-resistant varieties, an ongoing management intervention. Recoveries from catastrophes may themselves be experienced as a critical transition and managers should consider the larger dynamical landscape for the possibility of subsequent transitions. Early warning signals could therefore be useful when evaluating mitigation effectiveness.

A way forward for biodiversity conservation: high-quality landscapes.

We are losing biodiversity quickly, not simply because of development but due to poor spatial planning. Recent findings propose thoughtful configurations and management of human-modified landscapes to protect biodiversity while allowing food production. This opens up a range of feasible actions in the conservation agenda, which overlap with food sovereignty initiatives.