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.

Coupled Oscillators in an Agroecosystem: Integrating Direct and Indirect Effects.

AbstractAgricultural pests are increasingly appreciated as subjects of ecology. One particular case, a pest in coffee production, is analyzed here using the conceptual framework of complex systems, increasingly acknowledged as having an obvious home in the field of ecology, notorious for its complex structures. The particular case analyzed here arguably falls under the control of the complexity of the ecological system rather than of a simple magic bullet of population regulation. The system, which has been under study in southern Mexico for the past quarter century, is analyzed through the lens of neutral oscillations of the classical nondissipative Lotka-Volterra system. Based on three consumer/resource pairs (populations of [1] an ant, [2] a scale insect, [3] a beetle predator of the scale insect, [4] a fungal pathogen of the scale insect, and [5] a fly parasitoid of the ant), this five-dimensional system is well known qualitatively. Coupling all agents through both direct effects and trait-mediated indirect effects, the behavior of the neutral oscillation form of the system reveals a complex set of behaviors, including harmonized invariant sets, chaos, and/or quasiperiodicity. Such behaviors are well-known subjects in the science of complex systems and, it is argued, are ultimately sufficient to effect a degree of regulation on the pest, independent of explicit density-dependent feedback. Control of the system is thus seen as arguably actuated through its complexity, independent of any classic dissipative force.

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.

Distribution of biomass dynamics in relation to tree size in forests across the world.

Tree size shapes forest carbon dynamics and determines how trees interact with their environment, including a changing climate. Here, we conduct the first global analysis of among-site differences in how aboveground biomass stocks and fluxes are distributed with tree size. We analyzed repeat tree censuses from 25 large-scale (4-52 ha) forest plots spanning a broad climatic range over five continents to characterize how aboveground biomass, woody productivity, and woody mortality vary with tree diameter. We examined how the median, dispersion, and skewness of these size-related distributions vary with mean annual temperature and precipitation. In warmer forests, aboveground biomass, woody productivity, and woody mortality were more broadly distributed with respect to tree size. In warmer and wetter forests, aboveground biomass and woody productivity were more right skewed, with a long tail towards large trees. Small trees (1-10 cm diameter) contributed more to productivity and mortality than to biomass, highlighting the importance of including these trees in analyses of forest dynamics. Our findings provide an improved characterization of climate-driven forest differences in the size structure of aboveground biomass and dynamics of that biomass, as well as refined benchmarks for capturing climate influences in vegetation demographic models.

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.

Can Conflicting Selection from Pollinators and Nectar-Robbing Antagonists Drive Adaptive Pollen Limitation? A Conceptual Model and Empirical Test.

AbstractPollen limitation is widespread, despite predictions that it should not be. We propose a novel mechanism generating pollen limitation: conflicting selection by pollinators and antagonists on pollinator attraction traits. We introduce a heuristic model demonstrating antagonist-induced adaptive pollen limitation and present a field study illustrating its occurrence in a wild population. For antagonist-induced adaptive pollen limitation to occur, four criteria must be met: (1) correlated attraction of pollinators and antagonists; (2) greater response by antagonists than pollinators to altered investment in attraction traits; (3) reduced investment in pollinator attraction, leading to pollen limitation; and (4) higher fitness for plants with reduced investment in pollinator attraction. We surveyed nectar robbery and reproductive output for 109 Odontonema cuspidatum (Acanthaceae) plants in a pollen-limited population over 2 years and used experimental floral arrays to evaluate how flower number affects pollination and nectar robbery. Both pollinators and nectar robbers preferred larger floral displays and nectar robbery reduced reproductive output, suggesting conflicting selection. Survey and experimental data agreed closely on the optimum flower number under antagonist-induced pollen limitation; this number was substantially overrepresented in the population. While criteria for antagonist-induced adaptive pollen limitation are restrictive, the necessary conditions may often be realized. Considering interactions beyond the plant-pollinator dyad illuminates previously overlooked mechanisms generating pollen limitation.

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.

Light availability influences the intensity of nectar robbery and its effects on reproduction in a tropical shrub via multiple pathways.

PREMISE: The multiple exogenous pathways by which light availability affects plant reproduction (e.g., via influence on attraction of mutualists and antagonists) remain surprisingly understudied. The light environment experienced by a parent can also have transgenerational effects on offspring via these same pathways. METHODS: We evaluated (a) the influence of light availability on floral traits in Odontonema cuspidatum, (b) the relative importance of the pathways by which light influences nectar robbery and reproductive output, and (c) the role of parental light environment in mediating these relationships. We conducted a reciprocal translocation experiment using clonally propagated ramets and field surveys of naturally occurring plants. RESULTS: Light availability influenced multiple floral traits, including flower number and nectar volume, which in turn influenced nectar robbery. But nectar robbery was also directly influenced by light availability, due to light effects on nectar robber foraging behavior or neighborhood floral context. Parental light environment mediated the link between light availability and nectar robber attraction, suggesting local adaptation to low-light environments in floral visitor attraction. However, we found no transgenerational effect on reproduction. CONCLUSIONS: Our findings demonstrate that exogenous pathways by which light influences plants (particularly through effects on floral antagonists) can complicate the positive relationship between light availability and plant reproduction. Our results are among the first to document effects of light on floral antagonists and clonal transgenerational effects on flower visitor attraction traits.

Effect of coffee agriculture management on the population structure of a forest dwelling rodent (Heteromys desmarestianus goldmani).

Most of the natural habitat in tropical regions exists as scattered fragments embedded in a matrix of different agricultural uses. As a result of this agricultural expansion, habitat loss and fragmentation have become the main drivers of biodiversity loss. Understanding the long-term effects of agricultural management on populations is of great importance for the development of successful conservation strategies. Our study uses genetic data to determine the effect of agricultural management practices on the population structure of a common tropical forest rodent (Heteromys desmarestianus goldmani). We sampled 136 individuals from one forest fragment and three coffee farms representing varying degrees of management intensity in southern Mexico. Using microsatellite markers, we evaluated the genetic structure of H. d. goldmani in the study area. Our results show higher genetic differentiation and lower connectivity for individuals within high and medium intensity coffee farms than for those near and within the forest fragments. Our results suggest that the population structure observed is driven by landscape characteristics other than distance.

Successional dynamics in Neotropical forests are as uncertain as they are predictable.

Although forest succession has traditionally been approached as a deterministic process, successional trajectories of vegetation change vary widely, even among nearby stands with similar environmental conditions and disturbance histories. Here, we provide the first attempt, to our knowledge, to quantify predictability and uncertainty during succession based on the most extensive long-term datasets ever assembled for Neotropical forests. We develop a novel approach that integrates deterministic and stochastic components into different candidate models describing the dynamical interactions among three widely used and interrelated forest attributes--stem density, basal area, and species density. Within each of the seven study sites, successional trajectories were highly idiosyncratic, even when controlling for prior land use, environment, and initial conditions in these attributes. Plot factors were far more important than stand age in explaining successional trajectories. For each site, the best-fit model was able to capture the complete set of time series in certain attributes only when both the deterministic and stochastic components were set to similar magnitudes. Surprisingly, predictability of stem density, basal area, and species density did not show consistent trends across attributes, study sites, or land use history, and was independent of plot size and time series length. The model developed here represents the best approach, to date, for characterizing autogenic successional dynamics and demonstrates the low predictability of successional trajectories. These high levels of uncertainty suggest that the impacts of allogenic factors on rates of change during tropical forest succession are far more pervasive than previously thought, challenging the way ecologists view and investigate forest regeneration.

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.

The Big Rust and the Red Queen: Long-Term Perspectives on Coffee Rust Research.

Since 2008, there has been a cluster of outbreaks of the coffee rust (Hemileia vastatrix) across the coffee-growing regions of the Americas, which have been collectively described as the Big Rust. These outbreaks have caused significant hardship to coffee producers and laborers. This essay situates the Big Rust in a broader historical context. Over the past two centuries, coffee farmers have had to deal with the "curse of the Red Queen"-the need to constantly innovate in the face of an increasing range of threats, which includes the rust. Over the 20th century, particularly after World War II, national governments and international organizations developed a network of national, regional, and international coffee research institutions. These public institutions played a vital role in helping coffee farmers manage the rust. Coffee farmers have pursued four major strategies for managing the rust: bioprospecting for resistant coffee plants, breeding resistant coffee plants, chemical control, and agroecological control. Currently, the main challenge for researchers is to develop rust control strategies that are both ecologically and economically viable for coffee farmers, in the context of a volatile, deregulated coffee industry and the emergent challenges of climate change.

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.

Self-organized spatial pattern determines biodiversity in spatial competition.

In a simple cellular automata model it is shown that self-organization of spatial pattern in a community of strong competitors may generate a previously unrecognized mechanism of species richness determination. Employing some well-known general properties of interspecific competition, we elaborate a theoretical framework that generates both spatial mosaics and spiral waves within the same conceptual framework, dependent on the covariance of competition. We demonstrate that the qualitative nature of the spatial pattern depends on the "balance" of competition and that the number of species retained in the community depends on this spatial patterning.

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.

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.