Not your private tête-à-tête: leveraging the power of higher-order networks to study animal communication.

Animal communication is frequently studied with conventional network representations that link pairs of individuals who interact, for example, through vocalization. However, acoustic signals often have multiple simultaneous receivers, or receivers integrate information from multiple signallers, meaning these interactions are not dyadic. Additionally, non-dyadic social structures often shape an individual's behavioural response to vocal communication. Recently, major advances have been made in the study of these non-dyadic, higher-order networks (e.g. hypergraphs and simplicial complexes). Here, we show how these approaches can provide new insights into vocal communication through three case studies that illustrate how higher-order network models can: (i) alter predictions made about the outcome of vocally coordinated group departures; (ii) generate different patterns of song synchronization from models that only include dyadic interactions; and (iii) inform models of cultural evolution of vocal communication. Together, our examples highlight the potential power of higher-order networks to study animal vocal communication. We then build on our case studies to identify key challenges in applying higher-order network approaches in this context and outline important research questions that these techniques could help answer. This article is part of the theme issue 'The power of sound: unravelling how acoustic communication shapes group dynamics'.

Potential extinction cascades in a desert ecosystem: Linking food web interactions to community viability.

Desert communities are threatened with species loss due to climate change, and their resistance to such losses is unknown. We constructed a food web of the Mojave Desert terrestrial community (300 nodes, 4080 edges) to empirically examine the potential cascading effects of bird extinctions on this desert network, compared to losses of mammals and lizards. We focused on birds because they are already disappearing from the Mojave, and their relative thermal vulnerabilities are known. We quantified bottom-up secondary extinctions and evaluated the relative resistance of the community to losses of each vertebrate group. The impact of random bird species loss was relatively low compared to the consequences of mammal (causing the greatest number of cascading losses) or reptile loss, and birds were relatively less likely to be in trophic positions that could drive top-down effects in apparent competition and tri-tropic cascade motifs. An avian extinction cascade with year-long resident birds caused more secondary extinctions than the cascade involving all bird species for randomized ordered extinctions. Notably, we also found that relatively high interconnectivity among avian species has formed a subweb, enhancing network resistance to bird losses.

Neophobia, but not perch hopping, is sensitive to long-term chronic stress intensity.

To further elucidate the role that wear-and-tear plays in the transition from acute to chronic stress, we manipulated the intensity and duration of applied chronic stress to determine if behavior would respond proportionately. We brought wild house sparrows into captivity and subjected them to high-stress, medium-stress, low-stress, or captivity-only. We varied the number of stressors per day and the duration of stress periods to vary wear-and-tear, and thus the potential to exhibit chronic stress symptoms. The behaviors we assessed were neophobia (the fear of the new; assessed via food approach latency) and perch hopping (activity). We predicted that our birds would show proportionate decreases in neophobia and activity throughout a long-term chronic stress paradigm. Our results indicate that neophobia is sensitive to the intensity of chronic stress, however, the birds became more neophobic, which was the opposite of what we expected. Conversely, perch hopping did not differ across treatment groups and is thus not sensitive to the intensity of chronic stress. Together, these data show that different behavioral measurements are impacted differently by chronic stress.

The interplay of social constraints and individual variation in risk tolerance in the emergence of superspreaders.

Individual host behaviours can drastically impact the spread of infection through a population. Differences in the value individuals place on both socializing with others and avoiding infection have been shown to yield emergent homophily in social networks and thereby shape epidemic outcomes. We build on this understanding to explore how individuals who do not conform to their social surroundings contribute to the propagation of infection during outbreaks. We show how non-conforming individuals, even if they do not directly expose a disproportionate number of other individuals themselves, can become functional superspreaders through an emergent social structure that positions them as the functional links by which infection jumps between otherwise separate communities. Our results can help estimate the potential success of real-world interventions that may be compromised by a small number of non-conformists if their impact is not anticipated, and plan for how best to mitigate their effects on intervention success.

A mathematical representation of the reactive scope model.

Researchers have long sought to understand and predict an animal's response to stressful stimuli. Since the introduction of the concept of homeostasis, a variety of model frameworks have been proposed to describe what is necessary for an animal to remain within this stable physiological state and the ramifications of leaving it. Romero et al. (Horm Behav 55(3):375-389, 2009) introduced the reactive scope model to provide a novel conceptual framework for the stress response that assumes an animal's ability to tolerate a stressful stimulus may degrade over time in response to the stimulus. We provide a mathematical formulation for the reactive scope model using a system of ordinary differential equations and show that this model is capable of recreating existing experimental data. We also provide an experimental method that may be used to verify the model as well as several potential additions to the model. If future experimentation provides the necessary data to estimate the model's parameters, the model presented here may be used to make quantitative predictions about physiological mediator levels during a stress response and predict the onset of homeostatic overload.

Varying intensities of chronic stress induce inconsistent responses in weight and plasma metabolites in house sparrows (Passer domesticus).

One of the biggest unanswered questions in the field of stress physiology is whether variation in chronic stress intensity will produce proportional (a gradient or graded) physiological response. We were specifically interested in the timing of the entrance into homeostatic overload, or the start of chronic stress symptoms. To attempt to fill this knowledge gap we split 40 captive house sparrows (Passer domesticus) into four groups (high stress, medium stress, low stress, and a captivity-only control) and subjected them to six bouts of chronic stress over a 6-month period. We varied the number of stressors/day and the length of each individual bout with the goal of producing groups that would experience different magnitudes of wear-and-tear. To evaluate the impact of chronic stress, at the start and end of each stress bout we measured body weight and three plasma metabolites (glucose, ketones, and uric acid) in both a fasted and fed state. All metrics showed significant differences across treatment groups, with the high stress group most frequently showing the greatest changes. However, the changes did not produce a consistent profile that matched the different chronic stress intensities. We also took samples after a prolonged recovery period of 6 weeks after the chronic stressors ended. The only group difference that persisted after 6 weeks was weight-all differences across groups in metabolites recovered. The results indicate that common blood metabolites are sensitive to stressors and may show signs of wear-and-tear, but are not reliable indicators of the intensity of long-term chronic stress. Furthermore, regulatory mechanisms are robust enough to recover within 6 weeks post-stress.

House sparrows prioritize skin repair over constitutive innate immunity during long-term chronic stress.

The reactive scope model was created to address two major unanswered questions in stress physiology: how and when does the adaptive acute stress response turn into harmful chronic stress? Previous studies suggest that immunoenhancement should occur in reactive homeostasis (acute stress) and immunosuppression should occur in homeostatic overload (chronic stress). We used this dichotomy of immune function to further elucidate the transition from acute to chronic stress by treating house sparrows (Passer domesticus) with different intensities of chronic stress and then monitoring their immune function. By varying the number of stressors given per day and the length of chronic stress bouts over a period of 6 months, we produced four treatment groups: high, medium, and low stress, and captivity-only. We tracked immunity through the bacterial killing assay and monitored healing of a 4 mm skin biopsy punch. We hypothesized that higher-stress birds would repair their skin more slowly and have lower bacterial killing capacity. The opposite was true-high-stress birds initially repaired their skin fastest. Additionally, all birds dramatically reduced bacterial killing capacity after the biopsy and increased food-derived uric acid, suggesting increased energy acquisition and a shift in immune resources to a more immediate concern (healing). Once healing finished, only the high-stress birds were unable to recover circulating immune function, suggesting that the combination of high stress and an immune challenge pushed these birds into homeostatic overload. Prioritizing healing over other immunological processes might be the best defense for a bird in its natural habitat.

A 'Portfolio of Model Approximations' approach to understanding invasion success with vector-borne disease.

The central challenge of mathematical modeling of real-world systems is to strike an appropriate balance between insightful abstraction and detailed accuracy. Models in mathematical epidemiology frequently tend to either extreme, focusing on analytically provable boundaries in simplified, mass-action approximations, or else relying on calculated numerical solutions and computational simulation experiments to capture nuance and details specific to a particular host-disease system. We propose that there is value in an approach striking a slightly different compromise in which a detailed but analytically difficult system is modeled with careful detail, but then abstraction is applied to the results of numerical solutions to that system, rather than to the biological system itself. In this 'Portfolio of Model Approximations' approach, multiple levels of approximation are used to analyze the model at different scales of complexity. While this method has the potential to introduce error in the translation from model to model, it also has the potential to produce generalizable insight for the set of all similar systems, rather than isolated, tailored results that must be started anew for each next question. In this paper, we demonstrate this process and its value with a case study from evolutionary epidemiology. We consider a modified Susceptible-Infected-Recovered model for a vector-borne pathogen affecting two annually reproducing hosts. From observing patterns in simulations of the system and exploiting basic epidemiological properties, we construct two approximations of the model at different levels of complexity that can be treated as hypotheses about the behavior of the model. We compare the predictions of the approximations to the simulated results and discuss the trade-offs between accuracy and abstraction. We discuss the implications for this particular model, and in the context of mathematical biology in general.

Connecting People to Food: A Network Approach to Alleviating Food Deserts.

Introduction: In 2020, 13.8 million people in the United States struggled with food security. This means they were uncertain whether their food needs would be met. Where someone lives can influence struggles with food security. Food deserts are census tracts that experience high rates of poverty (20 percent of residents at/below poverty thresholds) and low access to grocery stores with nutritious foods. Food deserts and insecurity disproportionately affect disadvantaged communities and may contribute to health issues like diabetes, high blood pressure, and obesity. Public policies can be utilized to lessen the impact of food deserts and one way this can be achieved is through public transit. Methods: We characterized the role public transportation plays in connecting food desert residents with food by formulating network models from data on food deserts, grocery stores, and public transportation systems for five representative locations: Brown Deer, WI; Lawrence, KS; Albuquerque, NM; Charlotte, NC, and Raleigh, NC. We analyzed these networks by looking at centrality measures, specifically degree and closeness. These centrality measures provide insight on the situation regarding grocery store access for food deserts. Results: Results of the degree centrality measure varied across study sites; one site (Lawrence) had at least 1 bus stop within 0.25 miles (0.40 kilometers) of the representative address for each food desert. Conversely, two sites (Charlotte and Raleigh) each had 2 representative addresses with 0 bus stops within 0.75 miles (1.21 kilometers). When using the closeness centrality measure, 2 food deserts in Albuquerque had the highest number of grocery stores within 30 min (22 and 9) while 44% of food deserts in Raleigh had 0 grocery stores within 30 minutes. Conclusions: Using these results, we identify how public transportation could better connect people with food and offer suggestions to city leaders as a way to help eradicate food deserts.

Influence of Lived Experiences on Public Responses to Future Diseases via (De)Sensitization of Concern.

OBJECTIVES: Public responses to a future novel disease might be influenced by a subset of individuals who are either sensitized or desensitized to concern-generating processes through their lived experiences during the coronavirus disease 2019 (COVID-19) pandemic. Such influences may be critical for shaping public health messaging during the next emerging threat. METHODS: This study explored the potential outcomes of the influence of lived experiences by using a dynamic multiplex network model to simulate a COVID-19 outbreak in a population of 2000 individuals, connected by means of disease and communication layers. Then a new disease was introduced, and a subset of individuals (50% or 100% of hospitalized during the COVID-19 outbreak) was assumed to be either sensitized or desensitized to concern-generating processes relative to the general population, which alters their adoption of non-pharmaceutical interventions (social distancing). RESULTS: Altered perceptions and behaviors from lived experiences with COVID-19 did not necessarily result in a strong mitigating effect for the novel outbreak. When public disease response is already strong or sensitization is assumed to be a robust effect, then a sensitized subset may enhance public mitigation of an outbreak through social distancing. CONCLUSIONS: In preparing for future outbreaks, assuming an experienced and disease-aware public may compromise effective design of effective public health messaging and mitigative action.

Linking Immuno-Epidemiology Principles to Violence.

BACKGROUND: Societies have always struggled with violence, but recently there has been a push to understand violence as a public health issue. This idea has unified professionals in medicine, epidemiological, and psychology with a goal to end violence and heal those exposed to it. Recently, analogies have been made between community-level infectious disease epidemiology and how violence spreads within a community. Experts in public health and medicine suggest an epidemiological framework could be used to study violence. METHODS: Building upon results from community organizations which implement public health-like techniques to stop violence spread, we look to formalize the analogies between violence and infectious diseases. Then expanding on these ideas and using mathematical epidemiological principals, we formulate a susceptible-exposed-infected model to capture violence spread. Further, we ran example numerical simulations to show how a mathematical model can provide insight on prevention strategies. RESULTS: The preliminary simulations show negative effects of violence exposure have a greater impact than positive effects of preventative measures. For example, our simulation shows that when the impact of violence exposure is reduced by half, the amount of violence in a community drastically decreases in the long-term; but to reach this same outcome through an increase in the amount of after exposure support, it must be approximately fivefold. Further, we note that our simulations qualitatively agree with empirical studies. CONCLUSIONS: Having a mathematical model can give insights on the effectiveness of different strategies for violence prevention. Based on our example simulations, the most effective use of community funding is investing in protective factors, instead of support after violence exposure, but of course these results do not stand in isolation and will need to be contextualized with the rest of the research in the field.

A general modeling framework for exploring the impact of individual concern and personal protection on vector-borne disease dynamics.

BACKGROUND: As climate variability and extreme weather events associated with climate change become more prevalent, public health authorities can expect to face an expanding spectrum of vector-borne diseases with increasing incidence and geographical spread. Common interventions include the use of larvicides and adulticides, as well as targeted communications to increase public awareness regarding the need for personal protective measures, such as mosquito repellant, protective clothing, and mosquito nets. Here, we propose a simplified compartmental model of mosquito-borne disease dynamics that incorporates the use of personal protection against mosquito bites influenced by two key individual-level behavioral drivers-concern for being bitten by mosquitos as a nuisance and concern for mosquito-borne disease transmission. METHODS: We propose a modified compartmental model that describes the dynamics of vector-borne disease spread in a naïve population while considering the public demand for community-level control and, importantly, the effects of personal-level protection on population-level outbreak dynamics. We consider scenarios at low, medium, and high levels of community-level vector control, and at each level, we consider combinations of low, medium, and high levels of motivation to use personal protection, namely concern for disease transmission and concern for being bitten in general. RESULTS: When there is very little community-level vector control, nearly the entire population is quickly infected, regardless of personal protection use. When vector control is at an intermediate level, both concerns that motivate the use of personal protection play an important role in reducing disease burden. When authorities have the capacity for high-level community vector control through pesticide use, the motivation to use personal protection to reduce disease transmission has little additional effect on the outbreak. CONCLUSIONS: While results show that personal-level protection alone is not enough to significantly impact an outbreak, personal protective measures can significantly reduce the severity of an outbreak in conjunction with community-level control. Furthermore, the model provides insight for targeting public health messaging to increase the use of personal protection based on concerns related to being bitten by mosquitos or vector-borne disease transmission.

Considering humans as habitat reveals evidence of successional disease ecology among human pathogens.

The realization that ecological principles play an important role in infectious disease dynamics has led to a renaissance in epidemiological theory. Ideas from ecological succession theory have begun to inform an understanding of the relationship between the individual microbiome and health but have not yet been applied to investigate broader, population-level epidemiological dynamics. We consider human hosts as habitat and apply ideas from succession to immune memory and multi-pathogen dynamics in populations. We demonstrate that ecologically meaningful life history characteristics of pathogens and parasites, rather than epidemiological features alone, are likely to play a meaningful role in determining the age at which people have the greatest probability of being infected. Our results indicate the potential importance of microbiome succession in determining disease incidence and highlight the need to explore how pathogen life history traits and host ecology influence successional dynamics. We conclude by exploring some of the implications that inclusion of successional theory might have for understanding the ecology of diseases and their hosts.

Capturing complex interactions in disease ecology with simplicial sets.

Network approaches have revolutionized the study of ecological interactions. Social, movement and ecological networks have all been integral to studying infectious disease ecology. However, conventional (dyadic) network approaches are limited in their ability to capture higher-order interactions. We present simplicial sets as a tool that addresses this limitation. First, we explain what simplicial sets are. Second, we explain why their use would be beneficial in different subject areas. Third, we detail where these areas are: social, transmission, movement/spatial and ecological networks and when using them would help most in each context. To demonstrate their application, we develop a novel approach to identify how pathogens persist within a host population. Fourth, we provide an overview of how to use simplicial sets, highlighting specific metrics, generative models and software. Finally, we synthesize key research questions simplicial sets will help us answer and draw attention to methodological developments that will facilitate this.

How reported outbreak data can shape individual behavior in a social world.

Agencies reporting on disease outbreaks face many choices about what to report and the scale of its dissemination. Reporting impacts an epidemic by influencing individual decisions directly, and the social network in which they are made. We simulated a dynamic multiplex network model-with coupled infection and communication layers-to examine behavioral impacts from the nature and scale of epidemiological information reporting. We explored how adherence to protective behaviors (social distancing) can be facilitated through epidemiological reporting, social construction of perceived risk, and local monitoring of direct connections, but eroded via social reassurance. We varied reported information (total active cases, daily new cases, hospitalizations, hospital capacity exceeded, or deaths) at one of two scales (population level or community level). Total active and new case reporting at the population level were the most effective approaches, relative to the other reporting approaches. Case reporting, which synergizes with test-trace-and-isolate and vaccination policies, should remain a priority throughout an epidemic.

High prevalence does not necessarily equal maintenance species: Avoiding biased claims of disease reservoirs when using surveillance data.

Many pathogens of public health and conservation concern persist in host communities. Identifying candidate maintenance and reservoir species is therefore a central component of disease management. The term maintenance species implies that if all species but the putative maintenance species were removed, then the pathogen would still persist. In the absence of field manipulations, this statement inherently requires a causal or mechanistic model to assess. However, we lack a systematic understanding of (i) how often conclusions are made about maintenance and reservoir species without reference to mechanistic models (ii) what types of biases may be associated with these conclusions and (iii) how explicitly invoking causal or mechanistic modelling can help ameliorate these biases. Filling these knowledge gaps is critical for robust inference about pathogen persistence and spillover in multihost-parasite systems, with clear implications for human and wildlife health. To address these gaps, we performed a literature review on the evidence previous studies have used to make claims regarding maintenance or reservoir species. We then developed multihost-parasite models to explore and demonstrate common biases that could arise when inferring maintenance potential from observational prevalence data. Finally, we developed new theory to show how model-driven inference of maintenance species can minimize and eliminate emergent biases. In our review, we found that 83% of studies used some form of observational prevalence data to draw conclusions on maintenance potential and only 6% of these studies combined observational data with mechanistic modelling. Using our model, we demonstrate how the community, spatial and temporal context of observational data can lead to substantial biases in inferences of maintenance potential. Importantly, our theory identifies that model-driven inference of maintenance species elucidates other streams of observational data that can be leveraged to correct these biases. Model-driven inference is an essential, yet underused, component of multidisciplinary studies that make inference about host reservoir and maintenance species. Better integration of wildlife disease surveillance and mechanistic models is necessary to improve the robustness and reproducibility of our conclusions regarding maintenance and reservoir species.

Balancing timeliness of reporting with increasing testing probability for epidemic data.

Reporting of epidemiological data requires coordinated action by numerous agencies, across a multitude of logistical steps. Using collated and reported information to inform direct interventions can be challenging due to associated delays. Mitigation can, however, occur indirectly through the public generation of concern, which facilitates adherence to protective behaviors. We utilized a coupled-dynamic multiplex network model with a communication- and disease-layer to examine how variation in reporting delay and testing probability are likely to impact adherence to protective behaviors, such as reducing physical contact. Individual concern mediated adherence and was informed by new- or active-case reporting, at the population- or community-level. Individuals received information from the communication layer: direct connections that were sick or adherent to protective behaviors increased their concern, but absence of illness eroded concern. Models revealed that the relative benefit of timely reporting and a high probability of testing was contingent on how much information was already obtained. With low rates of testing, increasing testing probability was of greater mitigating value. With high rates of testing, maximizing timeliness was of greater value. Population-level reporting provided advanced warning of disease risk from nearby communities; but we explore the relative costs and benefits of delays due to scale against the assumption that people may prioritize community-level information. Our findings emphasize the interaction of testing accuracy and reporting timeliness for the indirect mitigation of disease in a complex social system.

How Drivers of Seasonality in Respiratory Infections May Impact Vaccine Strategy: A Case Study in How Coronavirus Disease 2019 (COVID-19) May Help Us Solve One of Influenza's Biggest Challenges.

Vaccines against seasonal infections like influenza offer a recurring testbed, encompassing challenges in design, implementation, and uptake to combat a both familiar and ever-shifting threat. One of the pervading mysteries of influenza epidemiology is what causes the distinctive seasonal outbreak pattern. Proposed theories each suggest different paths forward in being able to tailor precision vaccines and/or deploy them most effectively. One of the greatest challenges in contrasting and supporting these theories is, of course, that there is no means by which to actually test them. In this communication we revisit theories and explore how the ongoing coronavirus disease 2019 (COVID-19) pandemic might provide a unique opportunity to better understand the global circulation of respiratory infections. We discuss how vaccine strategies may be targeted and improved by both isolating drivers and understanding the immunological consequences of seasonality, and how these insights about influenza vaccines may generalize to vaccines for other seasonal respiratory infections.

Diversity in valuing social contact and risk tolerance leading to the emergence of homophily in populations facing infectious threats.

How self-organization leads to the emergence of structure in social populations remains a fascinating and open question in the study of complex systems. One frequently observed structure that emerges again and again across systems is that of self-similar community, i.e., homophily. We use a game theoretic perspective to explore a case in which individuals choose affiliation partnerships based on only two factors: the value they place on having social contacts, and their risk tolerance for exposure to threat derived from social contact (e.g., infectious disease, threatening ideas, etc.). We show how diversity along just these two influences is sufficient to cause the emergence of self-organizing homophily in the population. We further consider a case in which extrinsic social factors influence the desire to maintain particular social ties, and show the robustness of emergent homophilic patterns to these additional influences. These results demonstrate how observable population-level homophily may arise out of individual behaviors that balance the value of social contacts against the potential risks associated with those contacts. We present and discuss these results in the context of outbreaks of infectious disease in human populations. Complementing the standard narrative about how social division alters epidemiological risk, we here show how epidemiological risk may deepen social divisions in human populations.

Carceral Amplification of COVID-19: Impacts for Community, Corrections Officer, and Incarcerated Population Risks.

COVID-19 is challenging many societal institutions, including our criminal justice systems. Some have proposed or enacted (e.g., the State of New Jersey) reductions in the jail and/or prison populations. We present a mathematical model to explore the epidemiologic impact of such interventions in jails and contrast them with the consequences of maintaining unaltered practices. We consider infection risk and likely in-custody deaths, and estimate how within-jail dynamics lead to spill-over risks, not only affecting incarcerated people but increasing exposure, infection, and death rates for both corrections officers and the broader community beyond the justice system. We show that, given a typical jail-community dynamic, operating in a business-as-usual way results in substantial, rapid, and ongoing loss of life. Our results are consistent with the hypothesis that large-scale reductions in arrest and speeding of releases are likely to save the lives of incarcerated people, jail staff, and the wider community.