An immune memory-structured SIS epidemiological model for hyperdiverse pathogens.

A hyperdiverse class of pathogens of humans and wildlife, including the malaria parasite Plasmodium falciparum, relies on multigene families to encode antigenic variation. As a result, high (asymptomatic) prevalence is observed despite high immunity in local populations under high-transmission settings. The vast diversity of "strains" and genes encoding this variation challenges the application of established models for the population dynamics of such infectious diseases. Agent-based models have been formulated to address theory on strain coexistence and structure, but their complexity can limit application to gain insights into population dynamics. Motivated by P. falciparum malaria, we develop an alternative formulation in the form of a structured susceptible-infected-susceptible population model in continuous time, where individuals are classified not only by age, as is standard, but also by the diversity of parasites they have been exposed to and retain in their specific immune memory. We analyze the population dynamics and bifurcation structure of this system of partial-differential equations, showing the existence of alternative steady states and an associated tipping point with transmission intensity. We attribute the critical transition to the positive feedback between parasite genetic diversity and force of infection. Basins of attraction show that intervention must drastically reduce diversity to prevent a rebound to high infection levels. Results emphasize the importance of explicitly considering pathogen diversity and associated specific immune memory in the population dynamics of hyperdiverse epidemiological systems. This statement is discussed in a more general context for ecological competition systems with hyperdiverse trait spaces.

Marine reserves promote cycles in fish populations on ecological and evolutionary time scales.

Marine reserves are considered essential for sustainable fisheries, although their effectiveness compared to traditional fisheries management is debated. The effect of marine reserves is mostly studied on short ecological time scales, whereas fisheries-induced evolution is a well-established consequence of harvesting. Using a size-structured population model for an exploited fish population of which individuals spend their early life stages in a nursery habitat, we show that marine reserves will shift the mode of population regulation from low size-selective survival late in life to low, early-life survival due to strong resource competition. This shift promotes the occurrence of rapid ecological cycles driven by density-dependent recruitment as well as much slower evolutionary cycles driven by selection for the optimal body to leave the nursery grounds, especially with larger marine reserves. The evolutionary changes increase harvesting yields in terms of total biomass but cause disproportionately large decreases in yields of larger, adult fish. Our findings highlight the importance of carefully considering the size of marine reserves and the individual life history of fish when managing eco-evolutionary marine systems to ensure both population persistence as well as stable fisheries yields.

Dynamic population stage structure due to juvenile-adult asymmetry stabilizes complex ecological communities.

Natural ecological communities are diverse, complex, and often surprisingly stable, but the mechanisms underlying their stability remain a theoretical enigma. Interactions such as competition and predation presumably structure communities, yet theory predicts that complex communities are stable only when species growth rates are mostly limited by intraspecific self-regulation rather than by interactions with resources, competitors, and predators. Current theory, however, considers only the network topology of population-level interactions between species and ignores within-population differences, such as between juvenile and adult individuals. Here, using model simulations and analysis, I show that including commonly observed differences in vulnerability to predation and foraging efficiency between juvenile and adult individuals results in up to 10 times larger, more complex communities than observed in simulations without population stage structure. These diverse communities are stable or fluctuate with limited amplitude, although in the model only a single basal species is self-regulated, and the population-level interaction network is highly connected. Analysis of the species interaction matrix predicts the simulated communities to be unstable but for the interaction with the population-structure subsystem, which completely cancels out these instabilities through dynamic changes in population stage structure. Common differences between juveniles and adults and fluctuations in their relative abundance may hence have a decisive influence on the stability of complex natural communities and their vulnerability when environmental conditions change. To explain community persistence, it may not be sufficient to consider only the network of interactions between the constituting species.

Harvesting forage fish can prevent fishing-induced population collapses of large piscivorous fish.

Fisheries have reduced the abundances of large piscivores-such as gadids (cod, pollock, etc.) and tunas-in ecosystems around the world. Fisheries also target smaller species-such as herring, capelin, and sprat-that are important parts of the piscivores' diets. It has been suggested that harvesting of these so-called forage fish will harm piscivores. Multispecies models used for fisheries assessments typically ignore important facets of fish community dynamics, such as individual-level bioenergetics and/or size structure. We test the effects of fishing for both forage fish and piscivores using a dynamic, multitrophic, size-structured, bioenergetics model of the Baltic Sea. In addition, we analyze historical patterns in piscivore-biomass declines and fishing mortalities of piscivores and forage fish using global fish-stock assessment data. Our community-dynamics model shows that piscivores benefit from harvesting of their forage fish when piscivore fishing mortality is high. With substantial harvesting of forage fish, the piscivores can withstand higher fishing mortality. On the other hand, when piscivore fishing mortality is low, piscivore biomass decreases with more fishing of the forage fish. In accordance with these predictions, our statistical analysis of global fisheries data shows a positive interaction between the fishing mortalities of forage-fish stocks and piscivore stocks on the strength of piscivore-biomass declines. While overfishing of forage fish must be prevented, our study shows that reducing fishing pressures on forage fish may have unwanted negative side effects on piscivores. In some cases, decreasing forage-fish exploitation could cause declines, or even collapses, of piscivore stocks.

Stony coral populations are more sensitive to changes in vital rates in disturbed environments.

Reef-building corals, like many long-lived organisms, experience environmental change as a combination of separate but concurrent processes, some of which are gradual yet long-lasting, while others are more acute but short-lived. For corals, some chronic environmental stressors, such as rising temperature and ocean acidification, are thought to induce gradual changes in colonies' vital rates. Meanwhile, other environmental changes, such as the intensification of tropical cyclones, change the disturbance regime that corals experience. Here, we use a physiologically structured population model to explore how chronic environmental stressors that impact the vital rates of individual coral colonies interact with the intensity and magnitude of disturbance to affect coral population dynamics and cover. We find that, when disturbances are relatively benign, intraspecific density dependence driven by space competition partially buffers coral populations against gradual changes in vital rates. However, the impact of chronic stressors is amplified in more highly disturbed environments, because disturbance weakens the buffering effect of space competition. We also show that coral cover is more sensitive to changes in colony growth and mortality than to external recruitment, at least in open populations, and that space competition and size structure mediate the extent and pace of coral population recovery following a large-scale mortality event. Understanding the complex interplay among chronic environmental stressors, mass-mortality events, and population size structure sharpens our ability to manage and to restore coral-reef ecosystems in an increasingly disturbed future.

Resonance in Physiologically Structured Population Models.

Ecologists have long sought to understand how the dynamics of natural populations are affected by the environmental variation those populations experience. A transfer function is a useful tool for this purpose, as it uses linearization theory to show how the frequency spectrum of the fluctuations in a population's abundance relates to the frequency spectrum of environmental variation. Here, we show how to derive and to compute the transfer function for a continuous-time model of a population that is structured by a continuous individual-level state variable such as size. To illustrate, we derive, compute, and analyze the transfer function for a size-structured population model of stony corals with open recruitment, parameterized for a common Indo-Pacific coral species complex. This analysis identifies a sharp multi-decade resonance driven by space competition between existing coral colonies and incoming recruits. The resonant frequency is most strongly determined by the rate at which colonies grow, and the potential for resonant oscillations is greatest when colony growth is only weakly density-dependent. While these resonant oscillations are unlikely to be a predominant dynamical feature of degraded reefs, they suggest dynamical possibilities for marine invertebrates in more pristine waters. The size-structured model that we analyze is a leading example of a broader class of physiologically structured population models, and the methods we present should apply to a wide variety of models in this class.

Evolution of Reproduction Periods in Seasonal Environments.

AbstractMany species are subject to seasonal cycles in resource availability, affecting the timing of their reproduction. Using a stage-structured consumer-resource model in which juvenile development and maturation are resource dependent, we study how a species' reproductive schedule evolves, dependent on the seasonality of its resource. We find three qualitatively different reproduction modes. First, continuous income breeding (with adults reproducing throughout the year) evolves in the absence of significant seasonality. Second, seasonal income breeding (with adults reproducing unless they are starving) evolves when resource availability is sufficiently seasonal and juveniles are more efficient resource foragers. Third, seasonal capital breeding (with adults reproducing partly through the use of energy reserves) evolves when resource availability is sufficiently seasonal and adults are more efficient resource foragers. Such capital breeders start reproduction already while their offspring are still experiencing starvation. Changes in seasonality lead to continuous transitions between continuous and seasonal income breeding, but the change between income and capital breeding involves a hysteresis pattern, such that a population's evolutionarily stable reproduction pattern depends on its initial one. Taken together, our findings show how adaptation to seasonal environments can result in a rich array of outcomes, exhibiting seasonal or continuous reproduction with or without energy reserves.

Propensity for Risk in Reproductive Strategy Affects Susceptibility to Anthropogenic Disturbance.

AbstractAnimals initiate, interrupt, or invest resources in reproduction in light of their physiology and the environment. The energetic risks entailed in an individual's reproductive strategy can influence the ability to cope with additional stressors, such as anthropogenic climate change and disturbance. To explore the trade-offs between internal state, external resource availability, and reproduction, we applied state-dependent life-history theory (SDLHT) to a dynamic energy budget (DEB) model for long-finned pilot whales (Globicephala melas). We investigated the reproductive strategies emerging from the interplay between fitness maximization and propensity to take energetic risks, as well as the resulting susceptibility of individual vital rates to disturbance. Without disturbance, facultative reproductive behavior from SDLHT and fixed rules in the DEB model led to comparable individual fitness. However, under disturbance, the reproductive strategies emerging from SDLHT increased vulnerability to energetic risks, resulting in lower fitness than fixed rules. These fragile strategies might therefore be unlikely to evolve in the first place. Heterogeneous resource availability favored more cautious (and thus more robust) strategies, particularly when knowledge of resource variation was accurate. Our results demonstrate that the assumptions regarding the dynamic trade-offs underlying an individual's decision-making can have important consequences for predicting the effects of anthropogenic stressors on wildlife populations.

Population-level effects of acoustic disturbance in Atlantic cod: a size-structured analysis based on energy budgets.

Anthropogenic underwater noise may negatively affect marine animals. Yet, while fishes are highly sensitive to sounds, effects of acoustic disturbances on fishes have not been extensively studied at the population level. In this study, we use a size-structured model based on energy budgets to analyse potential population-level effects of anthropogenic noise on Atlantic cod (Gadus morhua). Using the model framework, we assess the impact of four possible effect pathways of disturbance on the cod population growth rate. Through increased stress, changes in foraging and movement behaviour, and effects on the auditory system, anthropogenic noise can lead to (i) increased energy expenditure, (ii) reduced food intake, (iii) increased mortality, and (iv) reduced reproductive output. Our results show that population growth rates are particularly sensitive to changes in energy expenditure and food intake because they indirectly affect the age of maturation, survival and fecundity. Sub-lethal effects of sound exposure may thus affect populations of cod and fishes with similar life histories more than lethal effects of sound exposure. Moreover, anthropogenic noise may negatively affect populations when causing persistent increases of energy expenditure or decreases of food intake. Effects of specific acoustic pollutants on energy acquisition and expenditure should therefore be further investigated.

Ontogenetic niche shifts as a driver of seasonal migration.

Ontogenetic niche shifts have helped to understand population dynamics. Here we show that ontogenetic niche shifts also offer an explanation, complementary to traditional concepts, as to why certain species show seasonal migration. We describe how demographic processes (survival, reproduction and migration) and associated ecological requirements of species may change with ontogenetic stage (juvenile, adult) and across the migratory range (breeding, non-breeding). We apply this concept to widely different species (dark-bellied brent geese (Branta b. bernicla), humpback whales (Megaptera novaeangliae) and migratory Pacific salmon (Oncorhynchus gorbuscha) to check the generality of this hypothesis. Consistent with the idea that ontogenetic niche shifts are an important driver of seasonal migration, we find that growth and survival of juvenile life stages profit most from ecological conditions that are specific to breeding areas. We suggest that matrix population modelling techniques are promising to detect the importance of the ontogenetic niche shifts in maintaining migratory strategies. As a proof of concept, we applied a first analysis to resident, partial migratory and fully migratory populations of barnacle geese (Branta leucopsis). We argue that recognition of the costs and benefits of migration, and how these vary with life stages, is important to understand and conserve migration under global environmental change.

Effects of life history and individual development on community dynamics: A review of counterintuitive consequences.

Even though individual life history is the focus of much ecological research, its importance for the dynamics and structure of ecological communities is unclear, or is it a topic of much ongoing research. In this paper I highlight the key life history traits that may lead to effects of life history or ontogeny on ecological communities. I show that asymmetries in the extent of food limitation between individuals in different life stage can give rise to an increase in efficiency with which resources are used for population growth when conditions change. This change in efficiency may result in a positive relationship between stage-specific density and mortality. The positive relationship between density and mortality in turn leads to predictions about community structure that are not only diametrically opposite to the expectations based on theory that ignores population structure but are also intuitively hard to accept. I provide a few examples that illustrate how taking into account intraspecific differences due to ontogeny radically changes the theoretical expectations regarding the possible outcomes of community dynamics. As the most compelling example I show how a so-called double-handicapped looser, that is, a consumer species that is both competitively inferior in the absence of predators and experiences higher mortality when predators are present, can nonetheless oust its opponent that it competes with for the same resource and is exposed to the same predator.

The Evolutionary Ecology of Metamorphosis.

Almost all animal species undergo metamorphosis, even though empirical data show that this life-history strategy evolved only a few times. Why is metamorphosis so widespread, and why has it evolved? Here we study the evolution of metamorphosis by using a fully size-structured population model in conjunction with the adaptive-dynamics approach. We assume that individuals compete for two food sources; one of these, the primary food source, is available to individuals of all sizes. The secondary food source is available only to large individuals. Without metamorphosis, unresolvable tensions arise for species faced with the opportunity of specializing on such a secondary food source. We show that metamorphosis can evolve as a way to resolve these tensions, such that small individuals specialize on the primary food source while large individuals specialize on the secondary food source. We find, however, that metamorphosis evolves only when the supply rate of the secondary food source exceeds a high threshold. Individuals postpone metamorphosis when the ecological conditions under which metamorphosis originally evolved deteriorate but will often not abandon this life-history strategy, even if it causes population extinction through evolutionary trapping. In summary, our results show that metamorphosis is not easy to evolve but that, once evolved, it is hard to lose. These findings can explain the widespread occurrence of metamorphosis in the animal kingdom despite its few evolutionary origins.

Bio-energetic modeling of medium-sized cetaceans shows high sensitivity to disturbance in seasons of low resource supply.

Understanding the full scope of human impact on wildlife populations requires a framework to assess the population-level repercussions of nonlethal disturbance. The Population Consequences of Disturbance (PCoD) framework provides such an approach, by linking the effects of disturbance on the behavior and physiology of individuals to their population-level consequences. Bio-energetic models have been used as implementations of PCoD, as these integrate the behavioral and physiological state of an individual with the state of the environment, to mediate between disturbance and biological significant changes in vital rates (survival, growth, and reproduction). To assess which levels of disturbance lead to adverse effects on population growth rate requires a bio-energetic model that covers the complete life cycle of the organism under study. In a density-independent setting, the expected lifetime reproductive output of a single female can then be used to predict the level of disturbance that leads to population decline. Here, we present such a model for a medium-sized cetacean, the long-finned pilot whale (Globicephala melas). Disturbance is modeled as a yearly recurrent period of no resource feeding for the pilot whale female and her calf. Short periods of disturbance lead to the pre-weaned death of the first one or more calves of the young female. Higher disturbance levels also affect survival of calves produced later in the life of the female, in addition to degrading female survival. The level of disturbance that leads to a negative population growth rate strongly depends on the available resources in the environment. This has important repercussion for the timing of disturbance if resource availability fluctuates seasonally. The model predicts that pilot whales can tolerate on average three times longer periods of disturbance in seasons of high resource availability, compared to disturbance happening when resources are low. Although our model is specifically parameterized for pilot whales, it provides useful insights into the general consequences of nonlethal disturbance. If appropriate data on life history and energetics are available, it can be used to provide management advice for specific species or populations.

Environmental change effects on life-history traits and population dynamics of anadromous fishes.

Migration, the recurring movement of individuals between a breeding and a non-breeding habitat, is a widespread phenomenon in the animal kingdom. Since the life cycle of migratory species involves two habitats, they are particularly vulnerable to environmental change, which may affect either of these habitats as well as the travel between them. In this study, we aim to reveal the consequences of environmental change affecting older life-history stages for the population dynamics and the individual life history of a migratory population. We formulate a population model based on the individual energetics and life history to study how increased energetic cost of the breeding travel and reduced survival and food availability in the non-breeding habitat affect an anadromous fish population. These unfavourable conditions have impacts at the individual and the population level. First, when conditions deteriorate individuals in the breeding habitat have a higher body growth rate as a consequence of reductions in spawning that reduce competition. Second, population abundance decreases, and its dynamics change from a regular annual cycle to oscillations with a period of four years. The oscillations are caused by the density-dependent feedback between individuals within a cohort through the food abundance in the breeding habitat, which results in alternation of a strong and a weak cohort. Our results explain how environmental change, by affecting older life-history stages, has multiple consequences for other life stages and for the entire population. We discuss these results in the context of empirical data and highlight the need for mechanistic understanding of the interactions between life-history and population dynamics in response to environmental change.

Large-amplitude consumer-resource cycles allow for the evolution of ontogenetic niche shifts in consumer life history.

In many size-structured populations individuals change resources during the course of their ontogenetic development. Different resources often require different adaptations to be effectively exploited. This leads to a trade-off between small and large individuals in direct developing species. Specialization on the resource used later in life turns out to be hardly possible in case of equilibrium dynamics. However, size-structured populations often exhibit population cycles. Non-equilibrium dynamics can change evolutionary behavior when compared with equilibrium dynamics. Here, we study the evolution of specialization on a secondary resource that is available only to large individuals, using the framework of adaptive dynamics. We show that in case of small-amplitude cycles, specialization on a secondary resource is hardly possible. Specialization will either decrease the resource intake of large individuals or severely increase competition among small individuals such that they cannot mature. Specialization on a secondary resource is often possible in case the population exhibits large-amplitude cycles. Specialization in that case increases the resource intake of large individuals and therefore prevents starvation. While specialization on a secondary resource increases competition among small individuals, maturation is still possible in case of large-amplitude cycles. We furthermore show that there is ecological bistability where small- and large-amplitude cycles coexist, giving rise to evolutionary bistability.

Predator Persistence through Variability of Resource Productivity in Tritrophic Systems.

The trophic structure of species communities depends on the energy transfer between trophic levels. Primary productivity varies strongly through time, challenging the persistence of species at higher trophic levels. Yet resource variability has mostly been studied in systems with only one or two trophic levels. We test the effect of variability in resource productivity in a tritrophic model system including a resource, a size-structured consumer, and a size-specific predator. The model complies with fundamental principles of mass conservation and the body-size dependence of individual-level energetics and predator-prey interactions. Surprisingly, we find that resource variability may promote predator persistence. The positive effect of variability on the predator arises through periods with starvation mortality of juvenile prey, which reduces the intraspecific competition in the prey population. With increasing variability in productivity and starvation mortality in the juvenile prey, the prey availability increases in the size range preferred by the predator. The positive effect of prey mortality on the trophic transfer efficiency depends on the biologically realistic consideration of body size-dependent and food-dependent functions for growth and reproduction in our model. Our findings show that variability may promote the trophic transfer efficiency, indicating that environmental variability may sustain species at higher trophic levels in natural ecosystems.

A Parent-Offspring Trade-Off Limits the Evolution of an Ontogenetic Niche Shift.

Many free-living animal species, including the majority of fish, insects, and amphibians, change their food and habitat during their life. Even though these ontogenetic changes in niche are common, it is not well understood which ecological conditions have favored the evolution of these shifts. Using an adaptive dynamics approach, we show that it is evolutionarily advantageous to switch to an alternative food source in the course of ontogeny when this results in a higher intake rate for the switching consumers. Individuals are, however, not able to specialize on this new food source when this negatively affects the performance early in life on the original food source. Selection on these early life stages is so strong that in species with a complete diet shift, evolution results in large juveniles and adults that are maladapted to the alternative food source while their offspring are specialized on the original food source when young. These outcomes suggest strong selection to decouple the different life stages, such that they can maximize their performance on different food sources independently from each other. Metamorphosis could be a way to decouple the different life stages and therefore evolve in species that feed on multiple food sources during their life.

Alternative stable states in a stage-structured consumer-resource biomass model with niche shift and seasonal reproduction.

We formulate and analyze a stage-structured consumer-resource biomass model, in which consumers reproduce in a pulsed event at the beginning of a growing season and furthermore go through a niche shift during their life history. We show that the resulting semi-discrete model can exhibit two stable states that can be characterized as a development-controlled state and a reproduction-controlled state. Varying resource availabilities and varying the extent of the niche shift determines whether juveniles or adults are more limited by their resource(s) and can lead to switches between the alternative stable states. Furthermore, we quantify the persistence of the consumer population and the occurrence of the two alternative stable states as a function of resource availabilities and extent of the niche shift. All the results show that irrespective of the type of reproduction of the consumers (continuous or seasonal), the stage-structured model will exhibit alternative stable states as long as development of the juvenile stage and reproduction of the adult stage are both resource-dependent.

Cohort dynamics give rise to alternative stable community states.

Many ecological systems can exhibit alternative stable states (ASS), which implies that ecological communities may diverge depending on their initial state, despite identical environmental conditions. Here we present a new mechanism that can cause ASS in competition systems. Using a physiologically structured model of competing populations, representing Baltic Sea sprat and herring and their resources, we show how cohort-driven population cycles may result in priority effects leading to ASS. Similar mechanisms could, depending on mortality level, also result in a "resident strikes back" phenomenon. We argue that the prerequisites for the occurrence of ASS in our model system, that is, communities with competing populations exhibiting cohort cycles and variation in size at maturation, may be common in ecological systems.