Understanding change in benthic marine systems.

BACKGROUND: The unprecedented influence of human activities on natural ecosystems in the 21st century has resulted in increasingly frequent large-scale changes in ecological communities. This has heightened interest in understanding such changes and effective means to manage them. Accurate interpretation of state changes is challenging because of difficulties translating theory to empirical study, and most theory emphasizes systems near equilibrium, which may not be relevant in rapidly changing environments. SCOPE: We review concepts of long-transient stages and phase shifts between stable community states, both smooth, continuous and discontinuous shifts, and the relationships among them. Three principal challenges emerge when applying these concepts. The first is how to interpret observed change in communities - distinguishing multiple stable states from long transients, or reversible shifts in the phase portrait of single attractor systems. The second is how to quantify the magnitudes of three sources of variability that cause switches between community states: (1) 'noise' in species' abundances, (2) 'wiggle' in system parameters and (3) trends in parameters that affect the topography of the basin of attraction. The third challenge is how variability of the system shapes evidence used to interpret community changes. We outline a novel approach using critical length scales to potentially address these challenges. These concepts are highlighted by a review of recent examples involving macroalgae as key players in marine benthic ecosystems. CONCLUSIONS: Real-world examples show three or more stable configurations of ecological communities may exist for a given set of parameters, and transient stages may persist for long periods necessitating their respective consideration. The characteristic length scale (CLS) is a useful metric that uniquely identifies a community 'basin of attraction', enabling phase shifts to be distinguished from long transients. Variabilities of CLSs and time series data may likewise provide proactive management measures to mitigate phase shifts and loss of ecosystem services. Continued challenges remain in distinguishing continuous from discontinuous phase shifts because their respective dynamics lack unique signatures.

Density-dependence and seasonal variation in reproductive output and sporophyte production in the kelp, Ecklonia radiata.

The kelp, Ecklonia radiata, is an abundant subtidal ecosystem engineer in southern Australia. Density-dependent changes in the abiotic environment engineered by Ecklonia may feedback to affect reproduction and subsequent recruitment. Here, we examined: 1) how the reproductive capacity of Ecklonia individuals in the field (zoospores released · mm-2 reproductive tissue) varied with adult density and time, and 2) how the recruitment of microscopic gametophytes and sporophytes was influenced by zoospore density at two times. Zoospore production did not vary with adult density, with only one month out of ten sampled over a 2-y period showing a significant effect of density. However, zoospore production varied hugely over time, being generally highest in mid-autumn and lowest in mid-late summer. There were strong effects of initial zoospore density on gametophyte and sporophyte recruitment with both a minimum and an optimum zoospore density for sporophyte recruitment, but these varied in time. Almost no sporophytes developed when initial zoospore density was <6.5 · mm-2 in spring or <0.5 · mm-2 in winter with optimum densities of 90-355 · mm-2 in spring and 21-261 · mm-2 in winter, which resulted in relatively high recruitment of 4-7 sporophytes · mm-2 . Sporophyte recruitment declined at initial zoospore densities >335 · mm-2 in spring and >261 · mm-2 in winter and was zero at very high zoospore densities. These findings suggest that although adult Ecklonia density does not affect per-capita zoospore production, because there is a minimum zoospore density for sporophyte production, a decline in population-level output could feedback to impact recruitment.

Combating ecosystem collapse from the tropics to the Antarctic.

Globally, collapse of ecosystems-potentially irreversible change to ecosystem structure, composition and function-imperils biodiversity, human health and well-being. We examine the current state and recent trajectories of 19 ecosystems, spanning 58° of latitude across 7.7 M km2 , from Australia's coral reefs to terrestrial Antarctica. Pressures from global climate change and regional human impacts, occurring as chronic 'presses' and/or acute 'pulses', drive ecosystem collapse. Ecosystem responses to 5-17 pressures were categorised as four collapse profiles-abrupt, smooth, stepped and fluctuating. The manifestation of widespread ecosystem collapse is a stark warning of the necessity to take action. We present a three-step assessment and management framework (3As Pathway Awareness, Anticipation and Action) to aid strategic and effective mitigation to alleviate further degradation to help secure our future.

Demography of the Intertidal Fucoid Hormosira banksii: Importance of Recruitment to Local Abundance.

Canopy-forming macroalgae form the basis of diverse coastal ecosystems globally. The fucoid Hormosira banksii is often the dominant canopy-forming macroalga in the temperate intertidal of southern Australia and New Zealand, where it is commonly associated with an understory of coralline turf. Hormosira banksii is susceptible to both natural and anthropogenic disturbance and despite its abundance, few studies have examined the demography of this important species. This study determined the demographic response of H. banksii to different gradients of disturbance to both its canopy and to the understory coralline turf. We established plots in which the density of H. banksii and/or understory coralline turf was manipulated in a pulse perturbation to simulate a disturbance event. The manipulated plots contained eight treatments ranging from 100% removal of H. banksii to 100% removal of the understory coralline turf. We then measured recruitment and followed individual recruits for up to 18 months to determine growth and survivorship. We found that H. banksii recruitment was seasonally variable throughout the experiment and highest over summer, survivorship of recruits was generally high, and the species was slow-growing and long-lived. Moreover, the level of disturbance did not seem to affect recruitment, growth, or survivorship and post-recruitment mortality was independent of H. banksii density. In this system, it appears that H. banksii is a relatively long-lived perennial species whose demography is density-independent which appears to allow recovery from disturbance.

Integrated assessment of the spatial distribution and structural dynamics of deep benthic marine communities.

Characterizing the spatial distribution and variation of species communities and validating these characteristics with data from the field are key elements for an ecosystem-based approach to management. However, models of species distributions that yield community structure are usually not linked to models of community dynamics, constraining understanding and management of the ecosystem, particularly in data-poor regions. Here we use a qualitative network model to predict changes in Antarctic benthic community structure between major marine habitats characterized largely by seafloor depth and slope, and use multivariate mixture models of species distributions to validate the community dynamics. We then assess how future increases in primary production associated with anticipated loss of sea-ice may affect the ecosystem. Our study shows how both spatial and structural features of ecosystems in data-poor regions can be analyzed and possible futures assessed, with direct relevance for ecosystem-based management.

Family-level variation in early life-cycle traits of kelp.

Temperate kelp forests (Laminarians) are threatened by temperature stress due to ocean warming and photoinhibition due to increased light associated with canopy loss. However, the potential for evolutionary adaptation in kelp to rapid climate change is not well known. This study examined family-level variation in physiological and photosynthetic traits in the early life-cycle stages of the ecologically important Australasian kelp Ecklonia radiata and the response of E. radiata families to different temperature and light environments using a family × environment design. There was strong family-level variation in traits relating to morphology (surface area measures, branch length, branch count) and photosynthetic performance (Fv /Fm ) in both haploid (gametophyte) and diploid (sporophyte) stages of the life-cycle. Additionally, the presence of family × environment interactions showed that offspring from different families respond differently to temperature and light in the branch length of male gametophytes and oogonia surface area of female gametophytes. Negative responses to high temperatures were stronger for females vs. males. Our findings suggest E. radiata may be able to respond adaptively to climate change but studies partitioning the narrow vs. broad sense components of heritable variation are needed to establish the evolutionary potential of E. radiata to adapt under climate change.

Global patterns of kelp forest change over the past half-century.

Kelp forests (Order Laminariales) form key biogenic habitats in coastal regions of temperate and Arctic seas worldwide, providing ecosystem services valued in the range of billions of dollars annually. Although local evidence suggests that kelp forests are increasingly threatened by a variety of stressors, no comprehensive global analysis of change in kelp abundances currently exists. Here, we build and analyze a global database of kelp time series spanning the past half-century to assess regional and global trends in kelp abundances. We detected a high degree of geographic variation in trends, with regional variability in the direction and magnitude of change far exceeding a small global average decline (instantaneous rate of change = -0.018 y-1). Our analysis identified declines in 38% of ecoregions for which there are data (-0.015 to -0.18 y-1), increases in 27% of ecoregions (0.015 to 0.11 y-1), and no detectable change in 35% of ecoregions. These spatially variable trajectories reflected regional differences in the drivers of change, uncertainty in some regions owing to poor spatial and temporal data coverage, and the dynamic nature of kelp populations. We conclude that although global drivers could be affecting kelp forests at multiple scales, local stressors and regional variation in the effects of these drivers dominate kelp dynamics, in contrast to many other marine and terrestrial foundation species.

Phenotypic plasticity and biogeographic variation in physiology of habitat-forming seaweed: response to temperature and nitrate.

Southeastern Australian waters are warming at nearly four times the global average rate (~0.7°C · century(-1) ) driven by strengthening incursions of the warm oligotrophic East Australian Current. The growth rate hypothesis (GRH) predicts that nutrient depletion will impact more severely on seaweeds at high latitudes with compressed growth seasons. This study investigates the effects of temperature and nutrients on the ecophysiology of the habitat-forming seaweed Phyllospora comosa in a laboratory experiment using temperature (12°C, 17°C, 22°C) and nutrient (0.5, 1.0, 3.0 µM NO3 (-) ) scenarios representative of observed variation among geographic regions. Changes in growth, photosynthetic characteristics (via chlorophyll fluorescence), pigment content, tissue chemistry (δ(13) C, % C, % N, C:N) and nucleic acid characteristics (absolute RNA and DNA, RNA:DNA ratios) were determined in seaweeds derived from cool, high-latitude and warm, low-latitude portions of the species' range. Performance of P. comosa was unaffected by nitrate availability but was strongly temperature-dependent, with photosynthetic efficiency, growth, and survival significantly impaired at 22°C. While some physiological processes (photosynthesis, nucleic acid, and accessory pigment synthesis) responded rapidly to temperature, others (C/N dynamics, carbon concentrating processes) were largely invariant and biogeographic variation in these characteristics may only occur through genetic adaptation. No link was detected between nutrient availability, RNA synthesis and growth, and the GRH was not supported in this species. While P. comosa at high latitudes may be less susceptible to oligotrophy than predicted by the GRH, warming water temperatures will have deleterious effects on this species across its range unless rapid adaptation is possible.

Warning signals of regime shifts as intrinsic properties of endogenous dynamics.

Ecosystem dynamics can exhibit large, nonlinear changes after small changes in an environmental parameter that passes a critical threshold. These regime shifts are often associated with loss of biodiversity and ecosystem services. Because critical thresholds for regime shifts are hard to determine with precision, some recent studies have focused on deriving signals from dynamics leading up to the thresholds. Models in these studies depend on using noise terms independent of system parameters and variables to add stochasticity. However, demographic stochasticity, an important source of random variability, arises directly from system dynamics. In this study, a framework is developed for modeling demographic stochasticity in a mechanistic way, incorporating system variables and parameters. This framework is applied to a deterministic, dynamic model of a coral reef benthos. The resulting stochastic model indicates that increasing variance-but not skewness-is consistently found in system dynamics approaching a critical threshold of grazing pressure. Even if the threshold is breached, attraction of transient dynamics by a saddle point provides an opportunity for regime shift reversal by management intervention. These results suggest that early warning signals of regime shifts can arise intrinsically in endogenous dynamics and can be detected without reliance on random environmental forcings.

Novel structural protein in porcine reproductive and respiratory syndrome virus encoded by an alternative ORF5 present in all arteriviruses.

Porcine reproductive and respiratory syndrome virus (PRRSV) is an arterivirus that emerged in the late 1980s in both Europe and North America as the causative agent of porcine reproductive and respiratory syndrome (PRRS), now the most important disease of swine worldwide. Despite extensive characterization of PRRSV proteins by direct analysis and comparison with other arteriviruses, determinants of virulence, pathogenesis and protective immune recognition remain poorly understood. Thus, we hypothesized that additional ORFs are present in the PRRSV genome that may contribute to its biological properties, and so we screened highly purified virions of strain VR2332, the prototype type 2 PRRSV, for evidence of novel polypeptides. A 51 aa polypeptide was discovered that is encoded by an alternative ORF of the subgenomic mRNA encoding the major envelope glycoprotein, GP5, and which is incorporated into virions. The protein, referred to as ORF5a protein, is expressed in infected cells, and pigs infected with PRRSV express anti-ORF5a protein antibodies. A similar ORF is present as an alternative reading frame in all PRRSV subgenomic RNA5 genes and in all other arteriviruses, suggesting that this ORF5a protein plays a significant role in arterivirology. Its discovery also provides a new potential target for immunological and pharmacological intervention in PRRS.

Alternative stable states and phase shifts in coral reefs under anthropogenic stress.

Ecosystems with alternative stable states (ASS) may shift discontinuously from one stable state to another as environmental parameters cross a threshold. Reversal can then be difficult due to hysteresis effects. This contrasts with continuous state changes in response to changing environmental parameters, which are less difficult to reverse. Worldwide degradation of coral reefs, involving "phase shifts" from coral to algal dominance, highlights the pressing need to determine the likelihood of discontinuous phase shifts in coral reefs, in contrast to continuous shifts with no ASS. However, there is little evidence either for or against the existence of ASS for coral reefs. We use dynamic models to investigate the likelihood of continuous and discontinuous phase shifts in coral reefs subject to sustained environmental perturbation by fishing, nutrification, and sedimentation. Our modeling results suggest that coral reefs with or without anthropogenic stress can exhibit ASS, such that discontinuous phase shifts can occur. We also find evidence to support the view that high macroalgal growth rates and low grazing rates on macroalgae favor ASS in coral reefs. Further, our results suggest that the three stressors studied, either alone or in combination, can increase the likelihood of both continuous and discontinuous phase shifts by altering the competitive balance between corals and algae. However, in contrast to continuous phase shifts, we find that discontinuous shifts occur only in model coral reefs with parameter values near the extremes of their empirically determined ranges. This suggests that continuous shifts are more likely than discontinuous shifts in coral reefs. Our results also suggest that, for ecosystems in general, tackling multiple human stressors simultaneously maximizes resilience to phase shifts, ASS, and hysteresis, leading to improvements in ecosystem health and functioning.

Regional-scale scenario modeling for coral reefs: a decision support tool to inform management of a complex system.

The worldwide decline of coral reefs threatens the livelihoods of coastal communities and puts at risk valuable ecosystem services provided by reefs. There is a pressing need for robust predictions of potential futures of coral reef and associated human systems under alternative management scenarios. Understanding and predicting the dynamics of coral reef systems at regional scales of tens to hundreds of kilometers is imperative, because reef systems are connected by physical and socioeconomic processes across regions and often across international boundaries. We present a spatially explicit regional-scale model of ecological dynamics for a general coral reef system. In designing our model as a tool for decision support, we gave precedence to portability and accessibility; the model can be parameterized for dissimilar coral reef systems in different parts of the world, and the model components and outputs are understandable for nonexperts. The model simulates local-scale dynamics, which are coupled across regions through larval connectivity between reefs. We validate our model using an instantiation for the Meso-American Reef system. The model realistically captures local and regional ecological dynamics and responds to external forcings in the form of harvesting, pollution, and physical damage (e.g., hurricanes, coral bleaching) to produce trajectories that largely fall within limits observed in the real system. Moreover, the model demonstrates behaviors that have relevance for management considerations. In particular, differences in larval supply between reef localities drive spatial variability in modeled reef community structure. Reef tracts for which recruitment is low are more vulnerable to natural disturbance and synergistic effects of anthropogenic stressors. Our approach provides a framework for projecting the likelihood of different reef futures at local to regional scales, with important applications for the management of complex coral reef systems.

Interactive effects of canopy-driven changes in light, scour and water flow on microscopic recruits in kelp.

Ecosystem engineering kelp forms habitat and influences associated communities by altering abiotic conditions. These conditions can also affect the engineer's own demographic rates but the mechanisms underpinning these feedbacks are not well known. Here, we tested the interactive effects of three abiotic factors engineered by the Australasian kelp Ecklonia radiata (light, water flow and scour) on the early survivorship and growth of its outplanted microscopic recruits. After six weeks, recruit survivorship was high in the absence of scour and low light (2-3 times higher than when scour was present) and under low water flow-ambient light conditions. Growth of sporophytes was strongly related to light, with recruits under ambient light approximately four times larger after six weeks. Overall, reduced scour (for survivorship) and ambient light (for growth) appear crucial for maximising E. radiata recruitment suggesting a healthy forest can provide microenvironments to enhance survivorship while gaps in the canopy enhance growth.

Genetic structure of a recent climate change-driven range extension.

The life-history strategies of some species make them strong candidates for rapid exploitation of novel habitat under new climate regimes. Some early-responding species may be considered invasive, and negatively impact on 'naïve' ecosystems. The barrens-forming sea urchin Centrostephanus rodgersii is one such species, having a high dispersal capability and a high-latitude range margin limited only by a developmental temperature threshold. Within this species' range in eastern Australian waters, sea temperatures have increased at greater than double the global average rate. The coinciding poleward range extension of C. rodgersii has caused major ecological changes, threatening reef biodiversity and fisheries productivity. We investigated microsatellite diversity and population structure associated with range expansion by this species. Generalized linear model analyses revealed no reduction in genetic diversity in the newly colonized region. A 'seascape genetics' analysis of genetic distances found no spatial genetic structure associated with the range extension. The distinctive genetic characteristic of the extension zone populations was reduced population-specific F(ST), consistent with very rapid population expansion. Demographic and genetic simulations support our inference of high connectivity between pre- and post-extension zones. Thus, the range shift appears to be a poleward extension of the highly-connected rangewide population of C. rodgersii. This is consistent with advection of larvae by the intensified warm water East Australian current, which has also increased Tasmanian Sea temperatures above the species' lower developmental threshold. Thus, ocean circulation changes have improved the climatic suitability of novel habitat for C. rodgersii and provided the supply of recruits necessary for colonization.

High kelp density attracts fishes except for recruiting cryptobenthic species.

As foundation species, kelp support productive and species rich communities; however, the effects of kelp structure on mobile species within these complex natural systems are often difficult to assess. We used artificial reefs with transplanted kelp to quantify the influence of kelp patch size and density on fish assemblages including the arrival of recruiting cryptobenthic species. Large patches with dense kelp supported the highest abundance, species richness, and diversity of fishes, with the addition of dense kelp tripling biomass and doubling richness. The abundance of recruits in artificial collectors declined with patch size and was halved on reefs with sparse kelp compared to reefs with dense kelp or no kelp. These results highlight the importance of dense kelp cover in facilitating biodiversity and indicate that kelp addition could support the recovery of degraded coastal ecosystems. Kelp also apparently drives complex interactions affecting the recruitment/behaviour of some cryptobenthic species.

Antigen-specific B-cell responses to porcine reproductive and respiratory syndrome virus infection.

Porcine reproductive and respiratory syndrome virus (PRRSV) causes an acute, viremic infection of 4 to 6 weeks, followed by a persistent infection lasting for several months. We characterized antibody and B-cell responses to viral proteins in acute and persistent infection to better understand the immunological basis of the prolonged infection. The humoral immune response to PRRSV was robust overall and varied among individual viral proteins, with the important exception of a delayed and relatively weak response to envelope glycoprotein 5 (GP5). Memory B cells were in secondary lymphoid organs, not in bone marrow or Peyer's patches, in contrast to the case for many mammalian species. Potent anti-PRRSV memory responses were elicited to recall antigen in vitro, even though a second infection did not increase the B-cell response in vivo, suggesting that productive reinfection does not occur in vivo. Antibody titers to several viral proteins decline over time, even though abundant antigen is known to be present in lymphoid tissues, possibly indicating ineffective antigen presentation. The appearance of antibodies to GP5 is delayed relative to the resolution of viremia, suggesting that anti-GP5 antibodies are not crucial for resolving viremia. Lastly, viral infection had no immunosuppressive effect on the humoral response to a second, unrelated antigen. Taking these data together, the active effector and memory B-cell responses to PRRSV are robust, and over time the humoral immune response to PRRSV is effective. However, the delayed response against GP5 early in infection may contribute to the prolonged acute infection and the establishment of persistence.

Resilience and stability of kelp forests: The importance of patch dynamics and environment-engineer feedbacks.

Habitat forming 'ecosystem engineers' such as kelp species create complex habitats that support biodiverse and productive communities. Studies of the resilience and stability of ecosystem engineers have typically focussed on the role of external factors such as disturbance. However, their population dynamics are also likely to be influenced by internal processes, such that the environmental modifications caused by engineer species feedback to affect their own demography (e.g. recruitment, survivorship). In numerous regions globally, kelp forests are declining and experiencing reductions in patch size and kelp density. To explore how resilience and stability of kelp habitats is influenced by this habitat degradation, we created an array of patch reefs of various sizes and supporting adult Ecklonia radiata kelp transplanted at different densities. This enabled testing of how sub-canopy abiotic conditions change with reductions in patch size and adult kelp density, and how this influenced demographic processes of microscopic and macroscopic juvenile kelp. We found that ecosystem engineering by adult E. radiata modified the environment to reduce sub-canopy water flow, sedimentation, and irradiance. However, the capacity of adult kelp canopy to engineer abiotic change was dependent on patch size, and to a lesser extent, kelp density. Reductions in patch size and kelp density also impaired the recruitment, growth and survivorship of microscopic and macroscopic juvenile E. radiata, and even after the provisioning of established juveniles, demographic processes were impaired in the absence of sufficient adult kelp. These results are consistent with the hypothesis that ecosystem engineering by adult E. radiata facilitates development of juvenile conspecifics. Habitat degradation seems to impair the ability of E. radiata to engineer abiotic change, causing breakdown of positive intraspecific feedback and collapse of demographic functions, and overall, leading to reductions in ecosystem stability and resilience well before local extirpation.

Understanding interactions between plasticity, adaptation and range shifts in response to marine environmental change.

Climate change is leading to shifts in species geographical distributions, but populations are also probably adapting to environmental change at different rates across their range. Owing to a lack of natural and empirical data on the influence of phenotypic adaptation on range shifts of marine species, we provide a general conceptual model for understanding population responses to climate change that incorporates plasticity and adaptation to environmental change in marine ecosystems. We use this conceptual model to help inform where within the geographical range each mechanism will probably operate most strongly and explore the supporting evidence in species. We then expand the discussion from a single-species perspective to community-level responses and use the conceptual model to visualize and guide research into the important yet poorly understood processes of plasticity and adaptation. This article is part of the theme issue 'The role of plasticity in phenotypic adaptation to rapid environmental change'.

Abundance and richness of key Antarctic seafloor fauna correlates with modelled food availability.

Most seafloor communities at depths below the photosynthesis zone rely on food that sinks through the water column. However, the nature and strength of this pelagic-benthic coupling and its influence on the structure and diversity of seafloor communities is unclear, especially around Antarctica where ecological data are sparse. Here we show that the strength of pelagic-benthic coupling along the East Antarctic shelf depends on both physical processes and the types of benthic organisms considered. In an approach based on modelling food availability, we combine remotely sensed sea-surface chlorophyll-a, a regional ocean model and diatom abundances from sediment grabs with particle tracking and show that fluctuating seabed currents are crucial in the redistribution of surface productivity at the seafloor. The estimated availability of suspended food near the seafloor correlates strongly with the abundance of benthic suspension feeders, while the deposition of food particles correlates with decreasing suspension feeder richness and more abundant deposit feeders. The modelling framework, which can be modified for other regions, has broad applications in conservation and management, as it enables spatial predictions of key components of seafloor biodiversity over vast regions around Antarctica.

Optimal scales to observe habitat dynamics: a coral reef example.

A new technique to estimate the characteristic length scales (CLSs) of real ecological systems provides an objective means to identify the optimal scale(s) of observation to best detect underlying dynamical trends. Application of the technique to natural systems has focused on identifying appropriate scales to measure the dynamics of species as descriptors of community and ecosystem dynamics. However, ecosystem monitoring is often based not on assessing single species, but on species assemblages, functional groups, or habitat types. We asked whether the concept of CLSs based on dynamic interactions among species could be extended to examine interactions among habitat types and thus to identify optimal scales for observing habitat dynamics. A time series of three spatial maps of benthic habitats on a Caribbean coral reef was constructed from aerial photographs, Compact Airborne Spectrographic Imager (CASI) images, and IKONOS satellite images, providing the short time sequence required for this technique. We estimated the CLS based on the dynamics of three distinct habitat types: dense stands of seagrass, sparse stands of seagrass, and Montastrea patch reefs. Despite notable differences in the areal extent of and relative change in these habitats over the 21-year observation period, analyses based on each habitat type indicated a similar CLS of -300 m. We interpret the consistency of CLSs among habitats to indicate that the dynamics of the three habitat types are linked. The results are encouraging, and they indicate that CLS techniques can be used to identify the appropriate scale at which to monitor ecosystem trends on the basis of the dynamics of only one of a disparate suite of habitat types.