Distinct responses to warming within picoplankton communities across an environmental gradient.

Picophytoplankton are a ubiquitous component of marine plankton communities and are expected to be favored by global increases in seawater temperature and stratification associated with climate change. Eukaryotic and prokaryotic picophytoplankton have distinct ecology, and global models predict that the two groups will respond differently to future climate scenarios. At a nearshore observatory on the Northeast US Shelf, however, decades of year-round monitoring have shown these two groups to be highly synchronized in their responses to environmental variability. To reconcile the differences between regional and global predictions for picophytoplankton dynamics, we here investigate the picophytoplankton community across the continental shelf gradient from the nearshore observatory to the continental slope. We analyze flow cytometry data from 22 research cruises, comparing the response of picoeukaryote and Synechococcus communities to environmental variability across time and space. We find that the mechanisms controlling picophytoplankton abundance differ across taxa, season, and distance from shore. Like the prokaryote, Synechococcus, picoeukaryote division rates are limited nearshore by low temperatures in winter and spring, and higher temperatures offshore lead to an earlier spring bloom. Unlike Synechococcus, picoeukaryote concentration in summer decreases dramatically in offshore surface waters and exhibits deeper subsurface maxima. The offshore picoeukaryote community appears to be nutrient limited in the summer and subject to much greater loss rates than Synechococcus. This work both produces and demonstrates the necessity of taxon- and site-specific knowledge for accurately predicting the responses of picophytoplankton to ongoing environmental change.

Predator switching strength controls stability in diamond-shaped food web models.

In food web models that include more than one prey type for a single predator, it is common for the predator's functional response to include some form of switching-preferential consumption of more abundant prey types. Predator switching promotes coexistence among competing prey types and increases diversity in the prey community. Here, we show how the dynamics of a diamond-shaped food web model of a marine plankton community are sensitive to a parameter that sets the strength of predator switching. Stronger switching destabilizes the model's coexistence equilibrium and leads to the appearance of limit cycles. Stronger switching also increases the evenness of the asymptotic prey community and promotes synchrony in the dynamics of disparate prey types. Given the dependence of model behavior on the strength of predator switching, it is important that modelers carefully consider the parameterization of functional responses that include switching.

The Contributions of Maternal Age Heterogeneity to Variance in Lifetime Reproductive Output.

AbstractVariance among individuals in fitness components reflects both genuine heterogeneity between individuals and stochasticity in events experienced along the life cycle. Maternal age represents a form of heterogeneity that affects both the mean and the variance of lifetime reproductive output (LRO). Here, we quantify the relative contribution of maternal age heterogeneity to the variance in LRO using individual-level laboratory data on the rotifer Brachionus manjavacas to parameterize a multistate age × maternal age matrix model. In B. manjavacas, advanced maternal age has large negative effects on offspring survival and fertility. We used multistate Markov chains with rewards to quantify the contributions to variance in LRO of heterogeneity and of the stochasticity inherent in the outcomes of probabilistic transitions and reproductive events. Under laboratory conditions, maternal age heterogeneity contributes 26% of the variance in LRO. The contribution changes when mortality and fertility are reduced to mimic more ecologically relevant environments. Over the parameter space where populations are near stationarity, maternal age heterogeneity contributes an average of 3% of the variance. Thus, the contributions of maternal age heterogeneity and individual stochasticity can be expected to depend strongly on environmental conditions; over most of the parameter space, the variance in LRO is dominated by stochasticity.

Seasonal environmental variability drives microdiversity within a coastal Synechococcus population.

Marine microbes often show a high degree of physiological or ecological diversity below the species level. This microdiversity raises questions about the processes that drive diversification and permit coexistence of diverse yet closely related marine microbes, especially given the theoretical efficiency of competitive exclusion. Here, we provide insight with an 8-year time series of diversity within Synechococcus, a widespread and important marine picophytoplankter. The population of Synechococcus on the Northeast U.S. Shelf is comprised of six main types, each of which displays a distinct and consistent seasonal pattern. With compositional data analysis, we show that these patterns can be reproduced with a simple model that couples differential responses to temperature and light with the seasonal cycle of the physical environment. These observations support the hypothesis that temporal variability in environmental factors can maintain microdiversity in marine microbial populations. We also identify how seasonal diversity patterns directly determine overarching Synechococcus population abundance features.

Political economy of renewable resource federalism.

The authority to manage natural capital often follows political boundaries rather than ecological. This mismatch can lead to unsustainable outcomes, as spillovers from one management area to the next may create adverse incentives for local decision making, even within a single country. At the same time, one-size-fits-all approaches of federal (centralized) authority can fail to respond to state (decentralized) heterogeneity and can result in inefficient economic or detrimental ecological outcomes. Here we utilize a spatially explicit coupled natural-human system model of a fishery to illuminate trade-offs posed by the choice between federal vs. state control of renewable resources. We solve for the dynamics of fishing effort and fish stocks that result from different approaches to federal management that vary in terms of flexibility. Adapting numerical methods from engineering, we also solve for the open-loop Nash equilibrium characterizing state management outcomes, where each state anticipates and responds to the choices of the others. We consider traditional federalism questions (state vs. federal management) as well as more contemporary questions about the economic and ecological impacts of shifting regulatory authority from one level to another. The key mechanisms behind the trade-offs include whether differences in local conditions are driven by biological or economic mechanisms; degree of flexibility embedded in the federal management; the spatial and temporal distribution of economic returns across states; and the status-quo management type. While simple rules-of-thumb are elusive, our analysis reveals the complex political economy dimensions of renewable resource federalism.

Seasons of Syn.

Synechococcus is a widespread and important marine primary producer. Time series provide critical information for identifying and understanding the factors that determine abundance patterns. Here, we present the results of analysis of a 16-yr hourly time series of Synechococcus at the Martha's Vineyard Coastal Observatory, obtained with an automated, in situ flow cytometer. We focus on understanding seasonal abundance patterns by examining relationships between cell division rate, loss rate, cellular properties (e.g., cell volume, phycoerythrin fluorescence), and environmental variables (e.g., temperature, light). We find that the drivers of cell division vary with season; cells are temperature-limited in winter and spring, but light-limited in the fall. Losses to the population also vary with season. Our results lead to testable hypotheses about Synechococcus ecophysiology and a working framework for understanding the seasonal controls of Synechococcus cell abundance in a temperate coastal system.

A demographic and evolutionary analysis of maternal effect senescence.

Maternal effect senescence-a decline in offspring survival or fertility with maternal age-has been demonstrated in many taxa, including humans. Despite decades of phenotypic studies, questions remain about how maternal effect senescence impacts evolutionary fitness. To understand the influence of maternal effect senescence on population dynamics, fitness, and selection, we developed matrix population models in which individuals are jointly classified by age and maternal age. We fit these models to data from individual-based culture experiments on the aquatic invertebrate, Brachionus manjavacas (Rotifera). By comparing models with and without maternal effects, we found that maternal effect senescence significantly reduces fitness for B. manjavacas and that this decrease arises primarily through reduced fertility, particularly at maternal ages corresponding to peak reproductive output. We also used the models to estimate selection gradients, which measure the strength of selection, in both high growth rate (laboratory) and two simulated low growth rate environments. In all environments, selection gradients on survival and fertility decrease with increasing age. They also decrease with increasing maternal age for late maternal ages, implying that maternal effect senescence can evolve through the same process as in Hamilton's theory of the evolution of age-related senescence. The models we developed are widely applicable to evaluate the fitness consequences of maternal effect senescence across species with diverse aging and fertility schedule phenotypes.

Dynamics and functional diversity of the smallest phytoplankton on the Northeast US Shelf.

Picophytoplankton are the most abundant primary producers in the ocean. Knowledge of their community dynamics is key to understanding their role in marine food webs and global biogeochemical cycles. To this end, we analyzed a 16-y time series of observations of a phytoplankton community at a nearshore site on the Northeast US Shelf. We used a size-structured population model to estimate in situ division rates for the picoeukaryote assemblage and compared the dynamics with those of the picocyanobacteria Synechococcus at the same location. We found that the picoeukaryotes divide at roughly twice the rate of the more abundant Synechococcus and are subject to greater loss rates (likely from viral lysis and zooplankton grazing). We describe the dynamics of these groups across short and long timescales and conclude that, despite their taxonomic differences, their populations respond similarly to changes in the biotic and abiotic environment. Both groups appear to be temperature limited in the spring and light limited in the fall and to experience greater mortality during the day than at night. Compared with Synechococcus, the picoeukaryotes are subject to greater top-down control and contribute more to the region's primary productivity than their standing stocks suggest.

Advancing an interdisciplinary framework to study seed dispersal ecology.

Although dispersal is generally viewed as a crucial determinant for the fitness of any organism, our understanding of its role in the persistence and spread of plant populations remains incomplete. Generalizing and predicting dispersal processes are challenging due to context dependence of seed dispersal, environmental heterogeneity and interdependent processes occurring over multiple spatial and temporal scales. Current population models often use simple phenomenological descriptions of dispersal processes, limiting their ability to examine the role of population persistence and spread, especially under global change. To move seed dispersal ecology forward, we need to evaluate the impact of any single seed dispersal event within the full spatial and temporal context of a plant's life history and environmental variability that ultimately influences a population's ability to persist and spread. In this perspective, we provide guidance on integrating empirical and theoretical approaches that account for the context dependency of seed dispersal to improve our ability to generalize and predict the consequences of dispersal, and its anthropogenic alteration, across systems. We synthesize suitable theoretical frameworks for this work and discuss concepts, approaches and available data from diverse subdisciplines to help operationalize concepts, highlight recent breakthroughs across research areas and discuss ongoing challenges and open questions. We address knowledge gaps in the movement ecology of seeds and the integration of dispersal and demography that could benefit from such a synthesis. With an interdisciplinary perspective, we will be able to better understand how global change will impact seed dispersal processes, and potential cascading effects on plant population persistence, spread and biodiversity.

Intraguild predation enables coexistence of competing phytoplankton in a well-mixed water column.

Resource competition theory predicts that when two species compete for a single, finite resource, the better competitor should exclude the other. However, in some cases, weaker competitors can persist through intraguild predation, that is, by eating their stronger competitor. Mixotrophs, species that meet their carbon demand by combining photosynthesis and phagotrophic heterotrophy, may function as intraguild predators when they consume the phototrophs with which they compete for light. Thus, theory predicts that mixotrophy may allow for coexistence of two species on a single limiting resource. We tested this prediction by developing a new mathematical model for a unicellular mixotroph and phytoplankter that compete for light, and comparing the model's predictions with a laboratory experimental system. We find that, like other intraguild predators, mixotrophs can persist when an ecosystem is sufficiently productive (i.e., the supply of the limiting resource, light, is relatively high), or when species interactions are strong (i.e., attack rates and conversion efficiencies are high). Both our mathematical and laboratory models show that, depending upon the environment and species traits, a variety of equilibrium outcomes, ranging from competitive exclusion to coexistence, are possible.

The formation of marine kin structure: effects of dispersal, larval cohesion, and variable reproductive success.

The spatial distribution of relatives has profound effects on kin interactions, inbreeding, and inclusive fitness. Yet, in the marine environment, the processes that generate patterns of kin structure remain understudied because larval dispersal on ocean currents was historically assumed to disrupt kin associations. Recent genetic evidence of co-occurring siblings challenges this assumption and raises the intriguing question of how siblings are found together after a (potentially) disruptive larval phase. Here, we develop individual-based models to explore how stochastic processes operating at the individual level affect expected kinship at equilibrium. Specifically, we predict how limited dispersal, sibling cohesion, and variability in reproductive success differentially affect patterns of kin structure. All three mechanisms increase mean kinship within populations, but their spatial effects are markedly different. We find that (1) when dispersal is limited, kinship declines monotonically as a function of the distance between individuals; (2) when siblings disperse cohesively, kinship increases within a site relative to between sites; and (3) when reproductive success varies, kinship increases equally at all distances. The differential effects of these processes therefore only become apparent when individuals are sampled at multiple spatial scales. Notably, our models suggest that aggregative larval behaviors, such as sibling cohesion, are not necessary to explain documented levels of relatedness within marine populations. Together, these findings establish a theoretical framework for disentangling the drivers of marine kin structure.

Sex difference and Allee effects shape the dynamics of sex-structured invasions.

The rate at which a population grows and spreads can depend on individual behaviour and interactions with others. In many species with two sexes, males and females differ in key life-history traits (e.g. growth, survival and dispersal), which can scale up to affect population rates of growth and spread. In sexually reproducing species, the mechanics of locating mates and reproducing successfully introduce further complications for predicting the invasion speed (spread rate), as both can change nonlinearly with density. Most models of population spread are based on one sex, or include limited aspects of sex differences. Here we ask whether and how the dynamics of finding mates interact with sex-specific life-history traits to influence the rate of population spread. We present a hybrid approach for modelling invasions of populations with two sexes that links individual-level mating behaviour (in an individual-based model) to population-level dynamics (in an integrodifference equation model). We find that limiting the amount of time during which individuals can search for mates causes a demographic Allee effect which can slow, delay, or even prevent an invasion. Furthermore, any sex-based asymmetries in life history or behaviour (skewed sex ratio, sex-biased dispersal, and sex-specific mating behaviours) amplify these effects. In contrast, allowing individuals to mate more than once ameliorates these effects, enabling polygynandrous populations to invade under conditions where monogamously mating populations would fail to establish. We show that details of individuals' mating behaviour can impact the rate of population spread. Based on our results, we propose a stricter definition of a mate-finding Allee effect, which is not met by the commonly used minimum mating function. Our modelling approach, which links individual- and population-level dynamics in a single model, may be useful for exploring other aspects of individual behaviour that are thought to impact the rate of population spread.

Density dependence in demography and dispersal generates fluctuating invasion speeds.

Density dependence plays an important role in population regulation and is known to generate temporal fluctuations in population density. However, the ways in which density dependence affects spatial population processes, such as species invasions, are less understood. Although classical ecological theory suggests that invasions should advance at a constant speed, empirical work is illuminating the highly variable nature of biological invasions, which often exhibit nonconstant spreading speeds, even in simple, controlled settings. Here, we explore endogenous density dependence as a mechanism for inducing variability in biological invasions with a set of population models that incorporate density dependence in demographic and dispersal parameters. We show that density dependence in demography at low population densities-i.e., an Allee effect-combined with spatiotemporal variability in population density behind the invasion front can produce fluctuations in spreading speed. The density fluctuations behind the front can arise from either overcompensatory population growth or density-dependent dispersal, both of which are common in nature. Our results show that simple rules can generate complex spread dynamics and highlight a source of variability in biological invasions that may aid in ecological forecasting.

Physiological and ecological drivers of early spring blooms of a coastal phytoplankter.

Climate affects the timing and magnitude of phytoplankton blooms that fuel marine food webs and influence global biogeochemical cycles. Changes in bloom timing have been detected in some cases, but the underlying mechanisms remain elusive, contributing to uncertainty in long-term predictions of climate change impacts. Here we describe a 13-year hourly time series from the New England shelf of data on the coastal phytoplankter Synechococcus, during which the timing of its spring bloom varied by 4 weeks. We show that multiyear trends are due to temperature-induced changes in cell division rate, with earlier blooms driven by warmer spring water temperatures. Synechococcus loss rates shift in tandem with division rates, suggesting a balance between growth and loss that has persisted despite phenological shifts and environmental change.

Multiple Friends with Benefits: An Optimal Mutualist Management Strategy?

Most mutualisms in nature involve interactions between multispecies mutualist guilds and multiple partner species. While mechanisms such as niche partitioning can explain part of this diversity, the presence of low-quality partners, which produce relatively low returns on investment compared with other guild members, is not well understood. Here, we consider a novel explanation for this persistence: that low-quality partners are actively maintained by their hosts as part of a growth-maximizing strategy, even in the presence of higher-quality alternatives. We use a model inspired by the interaction between host trees and ectomycorrhizal fungi to demonstrate that when the environment is variable, trees maintain low-quality fungal partners that they would not otherwise maintain in constant environments. This active investment, which emerges as a response to saturating returns on investment in higher-quality partners, could contribute to the maintenance of diversity in multispecies mutualisms.

High-seas fish wars generate marine reserves.

The effective management of marine fisheries is an ongoing challenge at the intersection of biology, economics, and policy. One way in which fish stocks-and their habitats-can be protected is through the establishment of marine reserves, areas that are closed to fishing. Although the potential economic benefits of such reserves have been shown for single-owner fisheries, their implementation quickly becomes complicated when more than one noncooperating harvester is involved in fishery management, which is the case on the high seas. How do multiple self-interested actors distribute their fishing effort to maximize their individual economic gains in the presence of others? Here, we use a game theoretic model to compare the effort distributions of multiple noncooperating harvesters with the effort distributions in the benchmark sole owner and open access cases. In addition to comparing aggregate rent, stock size, and fishing effort, we focus on the occurrence, size, and location of marine reserves. We show that marine reserves are a component of many noncooperative Cournot-Nash equilibria. Furthermore, as the number of harvesters increases, (i) both total unfished area and the size of binding reserves (those that actually constrain behavior) may increase, although the latter eventually asymptotically decreases; (ii) total rents and stock size both decline; and (iii) aggregate effort used (i.e., employment) can either increase or decrease, perhaps nonmonotonically.

Acquired phototrophy stabilises coexistence and shapes intrinsic dynamics of an intraguild predator and its prey.

In marine ecosystems, acquired phototrophs - organisms that obtain their photosynthetic ability by hosting endosymbionts or stealing plastids from their prey - are omnipresent. Such taxa function as intraguild predators yet depend on their prey to periodically obtain chloroplasts. We present a new theory for the effects of acquired phototrophy on community dynamics by analysing a mathematical model of this predator-prey interaction and experimentally verifying its predictions with a laboratory model system. We show that acquired phototrophy stabilises coexistence, but that the nature of this coexistence exhibits a 'paradox of enrichment': as light increases, the coexistence between the acquired phototroph and its prey transitions from a stable equilibrium to boom-bust cycles whose amplitude increases with light availability. In contrast, heterotrophs and mixotrophic acquired phototrophs (that obtain < 30% of their carbon from photosynthesis) do not exhibit such cycles. This prediction matches field observations, in which only strict ( > 95% of carbon from photosynthesis) acquired phototrophs form blooms.

Generational Spreading Speed and the Dynamics of Population Range Expansion.

Some of the most fundamental quantities in population ecology describe the growth and spread of populations. Population dynamics are often characterized by the annual rate of increase, λ, or the generational rate of increase, R0. Analyses involving R0 have deepened our understanding of disease dynamics and life-history complexities beyond that afforded by analysis of annual growth alone. While range expansion is quantified by the annual spreading speed, a spatial analog of λ, an R0-like expression for the rate of spread is missing. Using integrodifference models, we derive the appropriate generational spreading speed for populations with complex (stage-structured) life histories. The resulting measure, relevant to locations near the expanding edge of a (re)colonizing population, incorporates both local population growth and explicit spatial dispersal rather than solely growth across a population, as is the case for R0. The calculations for generational spreading speed are often simpler than those for annual spreading speed, and analytic or partial analytic solutions can yield insight into the processes that facilitate or slow a population's spatial spread. We analyze the spatial dynamics of green crabs, sea otters, and teasel as examples to demonstrate the flexibility of our methods and the intuitive insights that they afford.

Diel size distributions reveal seasonal growth dynamics of a coastal phytoplankter.

Phytoplankton account for roughly half of global primary production; it is vital that we understand the processes that control their abundance. A key process is cell division. We have, however, been unable to estimate division rate in natural populations at the appropriate timescale (hours to days) for extended periods of time (months to years). For phytoplankton, the diel change in cell size distribution is related to division rate, which offers an avenue to obtain estimates from in situ observations. We show that a matrix population model, fit to hourly cell size distributions, accurately estimates division rates of both cultured and natural populations of Synechococcus. Application of the model to Synechococcus at the Martha's Vineyard Coastal Observatory provides an unprecedented view that reveals a distinct seasonality in division rates. This information allows us to separate the effects of growth and loss quantitatively over an entire seasonal cycle. We find that division and loss processes are tightly coupled throughout the year. The large seasonal changes in cell abundance are the result of periods of time (weeks to months) when there are small systematic differences that favor either net growth or loss. We also find that temperature plays a critical role in limiting division rate during the annual spring bloom. This approach opens a path to quantify the role of Synechococcus in ecological and biogeochemical processes in natural systems.

Habitat damage, marine reserves, and the value of spatial management.

The biological benefits of marine reserves have garnered favor in the conservation community, but "no-take" reserve implementation is complicated by the economic interests of fishery stakeholders. There are now a number of studies examining the conditions under which marine reserves can provide both economic and ecological benefits. A potentially important reality of fishing that these studies overlook is that fishing can damage the habitat of the target stock. Here, we construct an equilibrium bioeconomic model that incorporates this habitat damage and show that the designation of marine reserves, coupled with the implementation of a tax on fishing effort, becomes both biologically and economically favorable as habitat sensitivity increases. We also study the effects of varied degrees of spatial control on fisheries management. Together, our results provide further evidence for the potential monetary and biological value of spatial management, and the possibility of a mutually beneficial resolution to the fisherman-conservationist marine reserve designation dilemma.