Linking scaling laws across eukaryotes.

Scaling laws relating body mass to species characteristics are among the most universal quantitative patterns in biology. Within major taxonomic groups, the 4 key ecological variables of metabolism, abundance, growth, and mortality are often well described by power laws with exponents near 3/4 or related to that value, a commonality often attributed to biophysical constraints on metabolism. However, metabolic scaling theories remain widely debated, and the links among the 4 variables have never been formally tested across the full domain of eukaryote life, to which prevailing theory applies. Here we present datasets of unprecedented scope to examine these 4 scaling laws across all eukaryotes and link them to test whether their combinations support theoretical expectations. We find that metabolism and abundance scale with body size in a remarkably reciprocal fashion, with exponents near ±3/4 within groups, as expected from metabolic theory, but with exponents near ±1 across all groups. This reciprocal scaling supports "energetic equivalence" across eukaryotes, which hypothesizes that the partitioning of energy in space across species does not vary significantly with body size. In contrast, growth and mortality rates scale similarly both within and across groups, with exponents of ±1/4. These findings are inconsistent with a metabolic basis for growth and mortality scaling across eukaryotes. We propose that rather than limiting growth, metabolism adjusts to the needs of growth within major groups, and that growth dynamics may offer a viable theoretical basis to biological scaling.

Yellowstone wolves and the forces that structure natural systems.

Since their introduction in 1995 and 1996, wolves have had effects on Yellowstone that ripple across the entire structure of the food web that defines biodiversity in the Northern Rockies ecosystem. Ecological interpretations of the wolves have generated a significant amount of debate about the relative strength of top-down versus bottom-up forces in determining herbivore and vegetation abundance in Yellowstone. Debates such as this are central to the resolution of broader debates about the role of natural enemies and climate as forces that structure food webs and modify ecosystem function. Ecologists need to significantly raise the profile of these discussions; understanding the forces that structure food webs and determine species abundance and the supply of ecosystem services is one of the central scientific questions for this century; its complexity will require new minds, new mathematics, and significant, consistent funding.

The impact of community organization on vector-borne pathogens.

Vector-borne zoonotic disease agents, which are known to often infect multiple species in the wild, have been identified as an emerging threat to human health. Understanding the ecology of these pathogens is especially timely, given the continued anthropogenic impacts on biodiversity. Here, we integrate empirical scaling laws from community ecology within a theoretical reservoir-vector-pathogen framework to study the transmission consequences of host community structure and diversity within large assemblages. We show that heterogeneity in susceptibility of the reservoir species promotes transmission "dilution," while a greater vector species richness "amplifies" it. These contrasting transmission impacts of vector and reservoir communities can yield very different epidemiological patterns. We demonstrate that vector and reservoir species richness can explain per se most of the pathogen transmission observed for West Nile virus in different parts of the United States, giving empirical support for the validity of these opposing theoretically predicted effects. We conclude that, in the context of disease emergence, the integration of a community perspective can provide critical insights into the understanding of pathogen transmission in wildlife.

Ecology of zoonoses: natural and unnatural histories.

More than 60% of human infectious diseases are caused by pathogens shared with wild or domestic animals. Zoonotic disease organisms include those that are endemic in human populations or enzootic in animal populations with frequent cross-species transmission to people. Some of these diseases have only emerged recently. Together, these organisms are responsible for a substantial burden of disease, with endemic and enzootic zoonoses causing about a billion cases of illness in people and millions of deaths every year. Emerging zoonoses are a growing threat to global health and have caused hundreds of billions of US dollars of economic damage in the past 20 years. We aimed to review how zoonotic diseases result from natural pathogen ecology, and how other circumstances, such as animal production, extraction of natural resources, and antimicrobial application change the dynamics of disease exposure to human beings. In view of present anthropogenic trends, a more effective approach to zoonotic disease prevention and control will require a broad view of medicine that emphasises evidence-based decision making and integrates ecological and evolutionary principles of animal, human, and environmental factors. This broad view is essential for the successful development of policies and practices that reduce probability of future zoonotic emergence, targeted surveillance and strategic prevention, and engagement of partners outside the medical community to help improve health outcomes and reduce disease threats.

Balancing economic and epidemiological interventions in the early stages of pathogen emergence.

The global pandemic of COVID-19 has underlined the need for more coordinated responses to emergent pathogens. These responses need to balance epidemic control in ways that concomitantly minimize hospitalizations and economic damages. We develop a hybrid economic-epidemiological modeling framework that allows us to examine the interaction between economic and health impacts over the first period of pathogen emergence when lockdown, testing, and isolation are the only means of containing the epidemic. This operational mathematical setting allows us to determine the optimal policy interventions under a variety of scenarios that might prevail in the first period of a large-scale epidemic outbreak. Combining testing with isolation emerges as a more effective policy than lockdowns, substantially reducing deaths and the number of infected hosts, at lower economic cost. If a lockdown is put in place early in the course of the epidemic, it always dominates the "laissez-faire" policy of doing nothing.

Transmission dynamics and prospects for the elimination of canine rabies.

Rabies has been eliminated from domestic dog populations in Western Europe and North America, but continues to kill many thousands of people throughout Africa and Asia every year. A quantitative understanding of transmission dynamics in domestic dog populations provides critical information to assess whether global elimination of canine rabies is possible. We report extensive observations of individual rabid animals in Tanzania and generate a uniquely detailed analysis of transmission biology, which explains important epidemiological features, including the level of variation in epidemic trajectories. We found that the basic reproductive number for rabies, R0, is very low in our study area in rural Africa (approximately 1.2) and throughout its historic global range (<2). This finding provides strong support for the feasibility of controlling endemic canine rabies by vaccination, even near wildlife areas with large wild carnivore populations. However, we show that rapid turnover of domestic dog populations has been a major obstacle to successful control in developing countries, thus regular pulse vaccinations will be required to maintain population-level immunity between campaigns. Nonetheless our analyses suggest that with sustained, international commitment, global elimination of rabies from domestic dog populations, the most dangerous vector to humans, is a realistic goal.

Spatial guilds in the Serengeti food web revealed by a Bayesian group model.

Food webs, networks of feeding relationships in an ecosystem, provide fundamental insights into mechanisms that determine ecosystem stability and persistence. A standard approach in food-web analysis, and network analysis in general, has been to identify compartments, or modules, defined by many links within compartments and few links between them. This approach can identify large habitat boundaries in the network but may fail to identify other important structures. Empirical analyses of food webs have been further limited by low-resolution data for primary producers. In this paper, we present a Bayesian computational method for identifying group structure using a flexible definition that can describe both functional trophic roles and standard compartments. We apply this method to a newly compiled plant-mammal food web from the Serengeti ecosystem that includes high taxonomic resolution at the plant level, allowing a simultaneous examination of the signature of both habitat and trophic roles in network structure. We find that groups at the plant level reflect habitat structure, coupled at higher trophic levels by groups of herbivores, which are in turn coupled by carnivore groups. Thus the group structure of the Serengeti web represents a mixture of trophic guild structure and spatial pattern, in contrast to the standard compartments typically identified. The network topology supports recent ideas on spatial coupling and energy channels in ecosystems that have been proposed as important for persistence. Furthermore, our Bayesian approach provides a powerful, flexible framework for the study of network structure, and we believe it will prove instrumental in a variety of biological contexts.

Urban habituation, ecological connectivity and epidemic dampening: the emergence of Hendra virus from flying foxes (Pteropus spp.).

Anthropogenic environmental change is often implicated in the emergence of new zoonoses from wildlife; however, there is little mechanistic understanding of these causal links. Here, we examine the transmission dynamics of an emerging zoonotic paramyxovirus, Hendra virus (HeV), in its endemic host, Australian Pteropus bats (fruit bats or flying foxes). HeV is a biosecurity level 4 (BSL-4) pathogen, with a high case-fatality rate in humans and horses. With models parametrized from field and laboratory data, we explore a set of probable contributory mechanisms that explain the spatial and temporal pattern of HeV emergence; including urban habituation and decreased migration-two widely observed changes in flying fox ecology that result from anthropogenic transformation of bat habitat in Australia. Urban habituation increases the number of flying foxes in contact with human and domestic animal populations, and our models suggest that, in addition, decreased bat migratory behaviour could lead to a decline in population immunity, giving rise to more intense outbreaks after local viral reintroduction. Ten of the 14 known HeV outbreaks occurred near urbanized or sedentary flying fox populations, supporting these predictions. We also demonstrate that by incorporating waning maternal immunity into our models, the peak modelled prevalence coincides with the peak annual spill-over hazard for HeV. These results provide the first detailed mechanistic framework for understanding the sporadic temporal pattern of HeV emergence, and of the urban/peri-urban distribution of HeV outbreaks in horses and people.

Climate forcing and desert malaria: the effect of irrigation.

BACKGROUND: Rainfall variability and associated remote sensing indices for vegetation are central to the development of early warning systems for epidemic malaria in arid regions. The considerable change in land-use practices resulting from increasing irrigation in recent decades raises important questions on concomitant change in malaria dynamics and its coupling to climate forcing. Here, the consequences of irrigation level for malaria epidemics are addressed with extensive time series data for confirmed Plasmodium falciparum monthly cases, spanning over two decades for five districts in north-west India. The work specifically focuses on the response of malaria epidemics to rainfall forcing and how this response is affected by increasing irrigation. METHODS AND FINDINGS: Remote sensing data for the Normalized Difference Vegetation Index (NDVI) are used as an integrated measure of rainfall to examine correlation maps within the districts and at regional scales. The analyses specifically address whether irrigation has decreased the coupling between malaria incidence and climate variability, and whether this reflects (1) a breakdown of NDVI as a useful indicator of risk, (2) a weakening of rainfall forcing and a concomitant decrease in epidemic risk, or (3) an increase in the control of malaria transmission. The predictive power of NDVI is compared against that of rainfall, using simple linear models and wavelet analysis to study the association of NDVI and malaria variability in the time and in the frequency domain respectively. CONCLUSIONS: The results show that irrigation dampens the influence of climate forcing on the magnitude and frequency of malaria epidemics and, therefore, reduces their predictability. At low irrigation levels, this decoupling reflects a breakdown of local but not regional NDVI as an indicator of rainfall forcing. At higher levels of irrigation, the weakened role of climate variability may be compounded by increased levels of control; nevertheless this leads to no significant decrease in the actual risk of disease. This implies that irrigation can lead to more endemic conditions for malaria, creating the potential for unexpectedly large epidemics in response to excess rainfall if these climatic events coincide with a relaxation of control over time. The implications of our findings for control policies of epidemic malaria in arid regions are discussed.

Colloquium paper: homage to Linnaeus: how many parasites? How many hosts?

Estimates of the total number of species that inhabit the Earth have increased significantly since Linnaeus's initial catalog of 20,000 species. The best recent estimates suggest that there are approximately 6 million species. More emphasis has been placed on counts of free-living species than on parasitic species. We rectify this by quantifying the numbers and proportion of parasitic species. We estimate that there are between 75,000 and 300,000 helminth species parasitizing the vertebrates. We have no credible way of estimating how many parasitic protozoa, fungi, bacteria, and viruses exist. We estimate that between 3% and 5% of parasitic helminths are threatened with extinction in the next 50 to 100 years. Because patterns of parasite diversity do not clearly map onto patterns of host diversity, we can make very little prediction about geographical patterns of threat to parasites. If the threats reflect those experienced by avian hosts, then we expect climate change to be a major threat to the relatively small proportion of parasite diversity that lives in the polar and temperate regions, whereas habitat destruction will be the major threat to tropical parasite diversity. Recent studies of food webs suggest that approximately 75% of the links in food webs involve a parasitic species; these links are vital for regulation of host abundance and potentially for reducing the impact of toxic pollutants. This implies that parasite extinctions may have unforeseen costs that impact the health and abundance of a large number of free-living species.

Plant ecology: Macroparasitism in plant communities.

Mistletoes, lianas, vines, and epiphytes fulfill many of the population dynamic criteria of animal macroparasites. A new study illustrates elegant ways to quantify cost to the host and how this impacts competition between mistletoe species. It opens the door to a much fuller consideration of plant parasites as macroparasites.

Public parks and the pandemic: How park usage has been affected by COVID-19 policies.

Public parks serve an important societal function as recreational spaces for diverse communities of people, with well documented physical and mental health benefits. As such, parks may be crucial for how people have handled effects of the COVID-19 pandemic, particularly the increasingly limited recreational opportunities, widespread financial uncertainty, and consequent heightened anxiety. Despite the documented benefits of parks, however, many states have instituted park shutdown orders due to fears that public parks could facilitate SARS-CoV-2 transmission. Here we use geotagged social media data from state, county, and local parks throughout New Jersey to examine whether park visitation increased when the COVID-19 pandemic began and whether park shutdown orders were effective at deterring park usage. We compare park usage during four discrete stages of spring 2020: (1) before the pandemic began, (2) during the beginning of the pandemic, (3) during the New Jersey governor's state-wide park shutdown order, and (4) following the lifting of the shutdown. We find that park visitation increased by 63.4% with the onset of the pandemic. The subsequent park shutdown order caused visitation in closed parks to decline by 76.1% while parks that remained open continued to experience elevated visitation levels. Visitation then returned to elevated pre-shutdown levels when closed parks were allowed to reopen. Altogether, our results indicate that parks continue to provide crucial services to society, particularly in stressful times when opportunities for recreation are limited. Furthermore, our results suggest that policies targeting human behavior can be effective and are largely reversible. As such, we should continue to invest in public parks and to explore the role of parks in managing public health and psychological well-being.

Assessing the burden of pregnancy-associated malaria under changing transmission settings.

BACKGROUND: The clinical presentation of pregnancy-associated malaria, or PAM, depends crucially on the particular epidemiological settings. This can potentially lead to an underestimation of its overall burden on the female population, especially in regions prone to epidemic outbreaks and where malaria transmission is generally low. METHODS: Here, by re-examining historical data, it is demonstrated how excess female mortality can be used to evaluate the burden of PAM. A simple mathematical model is then developed to highlight the contrasting signatures of PAM within the endemicity spectrum and to show how PAM is influenced by the intensity and stability of transmission. RESULTS: Both the data and the model show that maternal malaria has a huge impact on the female population. This is particularly pronounced in low-transmission settings during epidemic outbreaks where excess female mortality/morbidity can by far exceed that of a similar endemic setting. CONCLUSION: The results presented here call for active intervention measures not only in highly endemic regions but also, or in particular, in areas where malaria transmission is low and seasonal.

Critical transitions in malaria transmission models are consistently generated by superinfection.

The history of modelling vector-borne infections essentially begins with the papers by Ross on malaria. His models assume that the dynamics of malaria can most simply be characterized by two equations that describe the prevalence of malaria in the human and mosquito hosts. This structure has formed the central core of models for malaria and most other vector-borne diseases for the past century, with additions acknowledging important aetiological details. We partially add to this tradition by describing a malaria model that provides for vital dynamics in the vector and the possibility of super-infection in the human host: reinfection of asymptomatic hosts before they have cleared a prior infection. These key features of malaria aetiology create the potential for break points in the prevalence of infected hosts, sudden transitions that seem to characterize malaria's response to control in different locations. We show that this potential for critical transitions is a general and underappreciated feature of any model for vector-borne diseases with incomplete immunity, including the canonical Ross-McDonald model. Ignoring these details of the host's immune response to infection can potentially lead to serious misunderstanding in the interpretation of malaria distribution patterns and the design of control schemes for other vector-borne diseases. This article is part of the theme issue 'Modelling infectious disease outbreaks in humans, animals and plants: approaches and important themes'. This issue is linked with the subsequent theme issue 'Modelling infectious disease outbreaks in humans, animals and plants: epidemic forecasting and control'.

Spatial spread of an emerging infectious disease: conjunctivitis in House Finches.

In this paper we quantify the rate of spread of the newly emerged pathogen Mycoplasma gallisepticum of the House Finch, Carpodacus mexicanus, in its introduced range. We compare and contrast the rapid, yet decelerating, rate of spread of the pathogen with the slower, yet accelerating rate of spread of the introduced host. Comparing the rate of spread of this pathogen to pathogens in terrestrial mammalian hosts, we see that elevation and factors relating to host abundance restrict disease spread, rather than finding any major effects of discrete barriers or anthropogenic movement. We examine the role of seasonality in the rate of spread, finding that the rate and direction of disease spread relates more to seasonality in host movement than to seasonality in disease prevalence. We conclude that asymptomatic carriers are major transmitters of Mycoplasma gallisepticum into novel locations, a finding which may also be true for many other diseases, such as West Nile Virus and avian influenza.

Human impacts, plant invasion, and imperiled plant species in California.

Invasive species are one of the fastest growing conservation problems. These species homogenize the world's flora and fauna, threaten rare and endemic species, and impose large economic costs. Here, we examine the distribution of 834 of the more than 1000 exotic plant taxa that have become established in California, USA. Total species richness increases with net primary productivity; however, the exotic flora is richest in low-lying coastal sites that harbor large numbers of imperiled species, while native diversity is highest in areas with high mean elevation. Weedy and invasive exotics are more tightly linked to the distribution of imperiled species than the overall pool of exotic species. Structural equation modeling suggests that while human activities, such as urbanization and agriculture, facilitate the initial invasion by exotic plants, exotics spread ahead of the front of human development into areas with high numbers of threatened native plants. The range sizes of exotic taxa are an order of magnitude smaller than for comparable native taxa. The current small range size of exotic species implies that California has a significant "invasion debt" that will be paid as exotic plants expand their range and spread throughout the state.

Managing marine disease emergencies in an era of rapid change.

Infectious marine diseases can decimate populations and are increasing among some taxa due to global change and our increasing reliance on marine environments. Marine diseases become emergencies when significant ecological, economic or social impacts occur. We can prepare for and manage these emergencies through improved surveillance, and the development and iterative refinement of approaches to mitigate disease and its impacts. Improving surveillance requires fast, accurate diagnoses, forecasting disease risk and real-time monitoring of disease-promoting environmental conditions. Diversifying impact mitigation involves increasing host resilience to disease, reducing pathogen abundance and managing environmental factors that facilitate disease. Disease surveillance and mitigation can be adaptive if informed by research advances and catalysed by communication among observers, researchers and decision-makers using information-sharing platforms. Recent increases in the awareness of the threats posed by marine diseases may lead to policy frameworks that facilitate the responses and management that marine disease emergencies require.