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.

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.

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.

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.

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.

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.

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.

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.

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.

New forms of structure in ecosystems revealed with the Kuramoto model.

Ecological systems, as is often noted, are complex. Equally notable is the generalization that complex systems tend to be oscillatory, whether Huygens' simple patterns of pendulum entrainment or the twisted chaotic orbits of Lorenz' convection rolls. The analytics of oscillators may thus provide insight into the structure of ecological systems. One of the most popular analytical tools for such study is the Kuramoto model of coupled oscillators. We apply this model as a stylized vision of the dynamics of a well-studied system of pests and their enemies, to ask whether its actual natural history is reflected in the dynamics of the qualitatively instantiated Kuramoto model. Emerging from the model is a series of synchrony groups generally corresponding to subnetworks of the natural system, with an overlying chimeric structure, depending on the strength of the inter-oscillator coupling. We conclude that the Kuramoto model presents a novel window through which interesting questions about the structure of ecological systems may emerge.

The assembly and importance of a novel ecosystem: The ant community of coffee farms in Puerto Rico.

Agricultural ecosystems are by their very nature novel and by definition the more general biodiversity associated with them must likewise constitute a novel community. Here, we examine the community of arboreally foraging ants in the coffee agroecosystem of Puerto Rico. We surveyed 20 coffee plants in 25 farms three times in a period of one year. We also conducted a more spatially explicit sampling in two of the farms and conducted a species interaction study between the two most abundant species, Wasmannia auropunctata and Solenopsis invicta, in the laboratory. We find that the majority of the most common species are well-known invasive ants and that there is a highly variable pattern of dominance that varies considerably over the main coffee producing region of Puerto Rico, suggesting an unusual modality of community structure. The distribution pattern of the two most common species, W. auropunctata and S. invicta, suggests strong competitive exclusion. However, they also have opposite relationships with the percent of shade cover, with W. auropunctata showing a positive relationship with shade, while S. invicta has a negative relationship. The spatial distribution of these two dominant species in the two more intensively studied farms suggests that young colonies of S. invicta can displace W. auropunctata. Laboratory experiments confirm this. In addition to the elaboration of the nature and extent of this novel ant community, we speculate on the possibilities of its active inclusion as part of a biological control system dealing with several coffee pests, including one of the ants itself, W. auropunctata.

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.

Response of Coffee Farms to Hurricane Maria: Resistance and Resilience from an Extreme Climatic Event.

Resistance and resilience have become important concepts in the evaluation of disturbance events, providing a framework that is useful in light of the expected increase in frequency and occurrences of hurricanes as a consequence of climate change. Hurricane Maria landed on Puerto Rico as a category 4 storm in September of 2017. Among the affected elements were agricultural systems, including coffee agroecosystems. Historically, coffee has been a major backbone of the island's agricultural sector. Grown with a range of management styles, the coffee agroecosystem provides an excellent model system to study the resistance/resilience of agroecosystems faced with hurricane disturbance. Sampling 28 farms and comparing pre-hurricane data (2013) with post hurricane data we find that management style had only a small effect on either resistance or resilience, likely due to the especially strong nature of the storm. Rather, the socio-political context of individual farms seems to be a more useful predictor of resilience.

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.

Changes in adult sex ratio in wild bee communities are linked to urbanization.

Wild bees are indispensable pollinators, supporting global agricultural yield and angiosperm biodiversity. They are experiencing widespread declines, resulting from multiple interacting factors. The effects of urbanization, a major driver of ecological change, on bee populations are not well understood. Studies examining the aggregate response of wild bee abundance and diversity to urbanization tend to document minor changes. However, the use of aggregate metrics may mask trends in particular functional groups. We surveyed bee communities along an urban-to-rural gradient in SE Michigan, USA, and document a large change in observed sex ratio (OSR) along this gradient. OSR became more male biased as urbanization increased, mainly driven by a decline in medium and large bodied ground-nesting female bees. Nest site preference and body size mediated the effects of urbanization on OSR. Our results suggest that previously documented negative effects of urbanization on ground-nesting bees may underestimate the full impact of urbanization, and highlight the need for improved understanding of sex-based differences in the provision of pollination services by wild bees.