• Energy Research

AbstractAutotrophs play an essential role in the cycling of carbon and nutrients, yet disease‐ecosystem relationships are often overlooked in these dynamics. Importantly, the availability of elemental nutrients like nitrogen and phosphorus impacts infectious disease in autotrophs, and disease can induce reciprocal effects on ecosystem nutrient dynamics. Relationships linking infectious disease with ecosystem nutrient dynamics are bidirectional, though the interdependence of these processes has received little attention. We introduce disease‐mediated nutrient dynamics (DND) as a framework to describe the multiple, concurrent pathways linking elemental cycles with infectious disease. We illustrate the impact of disease–ecosystem feedback loops on both disease and ecosystem nutrient dynamics using a simple mathematical model, combining approaches from classical ecological (logistic and Droop growth) and epidemiological (susceptible and infected compartments) theory. Our model incorporates the effects of nutrient availability on the growth rates of susceptible and infected autotroph hosts and tracks the return of nutrients to the environment following host death. While focused on autotroph hosts here, the DND framework is generalizable to higher trophic levels. Our results illustrate the surprisingly complex dynamics of host populations, infection patterns, and ecosystem nutrient cycling that can arise from even a relatively simple feedback between disease and nutrients. Feedback loops in disease‐mediated nutrient dynamics arise via effects of infection and nutrient supply on host stoichiometry and population size. Our model illustrates how host growth rate, defense, and tissue chemistry can impact the dynamics of disease–ecosystem relationships. We use the model to motivate a review of empirical examples from autotroph–pathogen systems in aquatic and terrestrial environments, demonstrating the key role of nutrient–disease and disease–nutrient relationships in real systems. By assessing existing evidence and uncovering data gaps and apparent mismatches between model predictions and the dynamics of empirical systems, we highlight priorities for future research intended to narrow the persistent disciplinary gap between disease and ecosystem ecology. Future empirical and theoretical work explicitly examining the dynamic linkages between disease and ecosystem ecology will inform fundamental understanding for each discipline and will better position the field of ecology to predict the dynamics of disease and elemental cycles in the context of global change.

Intensification of human activities has led to changes in the availabilities of CO2 and nutrients in freshwater ecosystems, which may greatly alter the physiological status of phytoplankton. Viruses require hosts for their reproduction and shifts in phytoplankton host physiology through global environmental change may thus affect viral infections as well. Various studies have investigated the impacts of single environmental factors on phytoplankton virus propagation, yet little is known about the impacts of multiple factors, particularly in freshwater systems. We therefore tested the combined effects of phosphorus limitation and elevated pCO2 on the propagation of a cyanophage infecting a freshwater cyanobacterium. To this end, we cultured Phormidium in P-limited chemostats under ambient (400 μatm) and elevated (800 μatm) pCO2 at growth rates of 0.6, 0.3, and 0.05 d-1. Host C:P ratios generally increased with strengthened P-limitation and with elevated pCO2. Upon host steady state conditions, virus growth characteristics were obtained in separate infection assays where hosts were infected by the double-stranded DNA cyanophage PP. Severe P-limitation (host growth 0.05 d-1) led to a 85% decrease in cyanophage production rate and a 73% decrease in burst size compared to the 0.6 d-1 grown P-limited cultures. Elevated pCO2 induced a 96% increase in cyanophage production rate and a 57% increase in burst size, as well as an 85% shorter latent period as compared to ambient pCO2 at the different host growth rates. In addition, elevated pCO2 caused a decrease in the plaquing efficiency and an increase in the abortion percentage for the 0.05 d-1 P-limited treatment, while the plaquing efficiency increased for the 0.6 d-1 P-limited cultures. Together, our results demonstrate interactive effects of elevated pCO2 and P-limitation on cyanophage propagation, and show that viral propagation is generally constrained by P-limitation but enhanced with elevated pCO2. Our findings indicate that global change will likely have a severe impact on virus growth characteristics and thereby on the control of cyanobacterial hosts in freshwater ecosystems.

AbstractHosts rely on the availability of nutrients for growth, and for defense against pathogens. At the same time, changes in host nutrition can alter the dynamics of pathogens that rely on their host for reproduction. For primary producer hosts, enhanced nutrient loads may increase host biomass or pathogen reproduction, promoting faster density‐dependent pathogen transmission. However, the effect of elevated nutrients may be reduced if hosts allocate a growth‐limiting nutrient to pathogen defense. In canonical disease models, transmission is not a function of nutrient availability. Yet, including nutrient availability is necessary to mechanistically understand the response of infection to changes in the environment. Here, we explore the implications of nutrient‐mediated pathogen infectivity and host immunity on infection outcomes. We developed a stoichiometric disease model that explicitly integrates the contrasting dependencies of pathogen infectivity and host immunity on nitrogen (N) and parameterized it for an algal‐host system. Our findings reveal dynamic shifts in host biomass build‐up, pathogen prevalence, and the force of infection along N supply gradients with N‐mediated host infectivity and immunity, compared with a model in which the transmission rate was fixed. We show contrasting responses in pathogen performance with increasing N supply between N‐mediated infectivity and N‐mediated immunity, revealing an optimum for pathogen transmission at intermediate N supply. This was caused by N limitation of the pathogen at a low N supply and by pathogen suppression via enhanced host immunity at a high N supply. By integrating both nutrient‐mediated pathogen infectivity and host immunity into a stoichiometric model, we provide a theoretical framework that is a first step in reconciling the contrasting role nutrients can have on host–pathogen dynamics.

AbstractThe physiological performance of organisms depends on their environmental context, resulting in performance–response curves along environmental gradients. Parasite performance–response curves are generally expected to be broader than those of their hosts due to shorter generation times and hence faster adaptation. However, certain environmental conditions may limit parasite performance more than that of the host, thereby providing an environmental refuge from disease. Thermal disease refuges have been extensively studied in response to climate warming, but other environmental factors may also provide environmental disease refuges which, in turn, respond to global change. Here, we (1) showcase laboratory and natural examples of refuges from parasites along various environmental gradients, and (2) provide hypotheses on how global environmental change may affect these refuges. We strive to synthesize knowledge on potential environmental disease refuges along different environmental gradients including salinity and nutrients, in both natural and food‐production systems. Although scaling up from single host–parasite relationships along one environmental gradient to their interaction outcome in the full complexity of natural environments remains difficult, integrating host and parasite performance–response can serve to formulate testable hypotheses about the variability in parasitism outcomes and the occurrence of environmental disease refuges under current and future environmental conditions.

AbstractClimate change is expected to favour infectious diseases across ecosystems worldwide. In freshwater and marine environments, parasites play a crucial role in controlling plankton population dynamics. Infection of phytoplankton populations will cause a transfer of carbon and nutrients into parasites, which may change the type of food available for higher trophic levels. Some phytoplankton species are inedible to zooplankton, and the termination of their population by parasites may liberate otherwise unavailable carbon and nutrients. Phytoplankton spring blooms often consist of large diatoms inedible for zooplankton, but the zoospores of their fungal parasites may serve as a food source for this higher trophic level. Here, we investigated the impact of warming on the fungal infection of a natural phytoplankton spring bloom and followed the response of a zooplankton community. Experiments were performed in ca. 1000 L indoor mesocosms exposed to a controlled seasonal temperature cycle and a warm (+4 °C) treatment in the period from March to June 2014. The spring bloom was dominated by the diatom Synedra. At the peak of infection over 40% of the Synedra population was infected by a fungal parasite (i.e. a chytrid) in both treatments. Warming did not affect the onset of the Synedra bloom, but accelerated its termination. Peak population density of Synedra tended to be lower in the warm treatments. Furthermore, Synedra carbon: phosphorus stoichiometry increased during the bloom, particularly in the control treatments. This indicates enhanced phosphorus limitation in the control treatments, which may have constrained chytrid development. Timing of the rotifer Keratella advanced in the warm treatments and closely followed chytrid infections. The chytrids' zoospores may thus have served as an alternative food source to Keratella. Our study thus emphasizes the importance of incorporating not only nutrient limitation and grazing, but also parasitism in understanding the response of plankton communities towards global warming.