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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

Scale and strength oak-mesophyte interactions in a transitional oak-hickory forest.

Forests in eastern North America are undergoing rapid compositional changes as they experience novel climate, disturbance, and pest conditions. One striking pattern is the replacement of canopy oaks (Quercus spp.) by mesic, fire-sensitive, shade-tolerant species like red maple (Acer rubrum). To gain insight into the successional patterns driving stand-level canopy oak replacement we ask two questions: (i) What is the spatial association of oak and mesophyte recruitment compared to oak and mesophyte overstory individuals, and (ii) How do oaks and mesophytes differentially respond to canopy openings. We analyzed census data from a 23 ha forest plot surveyed in 2003, 2008 and 2014. We show that oak recruits are negatively associated with overstory red maples and black cherries (Prunus serotina), while mesophytic recruits were positively associated with overstory oaks. Second, we found that proximity to a dead overstory tree increased growth and survival for black cherries, increased growth for red maples, but had no effect on oaks. Black cherries and red maples are therefore better suited than oaks to take advantage of canopy openings and the moderate light available under adult oaks. These same fine scale competitive processes are contributing to canopy oak replacement across eastern North America.

Huffaker revisited: spatial heterogeneity and the coupling of ineffective agents in biological control.

In a classic study, Huffaker demonstrated that abiotic forms of spatial heterogeneity could induce stability in predator-prey interactions. Recent theories suggest that space can also act to destabilize predator-prey systems and that stability can arise from coupling of unstable units. Here, using Huffaker's classic experimental design refitted with modern empirical and statistical techniques, we reassess the effect of space on predator-prey interactions when the prey are pests of agriculture, and when predators must compete with pathogens for shared prey resources. Using an empirical system including aphids, ladybird beetles and entomopathogenic fungi, we show that while two different control agents were ineffective at controlling pests in insolation, coupling them together not only improved control of the pest, but also reduced the occurrence of large, spatially-clustered pest outbreaks. Our results suggest that as agriculture becomes increasingly isolated and consolidated across landscapes, endogenous forms of spatial heterogeneity, which arise from interactions between diverse assemblages of control agents, may break down. We suggest that improving connectivity across landscapes is important for maintaining effective biological control in agroecosystems.

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.

Anolis lizards as biocontrol agents in mainland and island agroecosystems.

Our knowledge of ecological interactions that bolster ecosystem function and productivity has broad applications to the management of agricultural systems. Studies suggest that the presence of generalist predators in agricultural landscapes leads to a decrease in the abundance of herbivorous pests, but our understanding of how these interactions vary across taxa and along gradients of management intensity and eco-geographic space remains incomplete. In this study, we assessed the functional response and biocontrol potential of a highly ubiquitous insectivore (lizards in the genus Anolis) on the world's most important coffee pest, the coffee berry borer (Hypothalemus hampei). We conducted field surveys and laboratory experiments to examine the impact of land-use intensification on species richness and abundance of anoles and the capacity of anoles to reduce berry borer infestations in mainland and island coffee systems. Our results show that anoles significantly reduce coffee infestation rates in laboratory settings (Mexico, p = .03, F = 5.13 df = 1, 35; Puerto Rico, p = .014, F = 8.82, df = 1, 10) and are capable of consuming coffee berry borers in high abundance. Additionally, diversified agroecosystems bolster anole abundance, while high-intensity practices, including the reduction of vegetation complexity and the application of agrochemicals were associated with reduced anole abundance. The results of this study provide supporting evidence of the positive impact of generalist predators on the control of crop pests in agricultural landscapes, and the role of diversified agroecosystems in sustaining both functionally diverse communities and crop production in tropical agroecosystems.