Wave damping by giant kelp, Macrocystis pyrifera.

BACKGROUND AND AIMS: The increased likelihood and severity of storm events has brought into focus the role of coastal ecosystems in provision of shoreline protection by attenuating wave energy. Canopy-forming kelps, including giant kelp (Macrocystis pyrifera), are thought to provide this ecosystem service, but supporting data are extremely limited. Previous in situ examinations relied mostly on comparisons between nominally similar sites with and without kelp. Given that other factors (especially seafloor bathymetry and topographic features) often differ across sites, efforts to isolate the effects of kelp on wave energy propagation confront challenges. In particular, it can be difficult to distinguish wave energy dissipation attributable to kelp from frictional processes at the seabed that often covary with the presence of kelp. Here, we use an ecological transition from no kelp to a full forest, at a single site with static bathymetry, to resolve unambiguously the capacity of giant kelp to damp waves. METHODS: We measured waves within and outside rocky reef habitat, in both the absence and the presence of giant kelp, at Marguerite Reef, Palos Verdes, CA, USA. Nested within a broader kelp restoration project, this site transitioned from a bare state to one supporting a fully formed forest (density of 8 stipes m-2). We quantified, as a function of incident wave conditions, the decline in wave energy flux attributable to the presence of kelp, as waves propagated from outside and into reef habitat. KEY RESULTS: The kelp forest damped wave energy detectably, but to a modest extent. Interactions with the seabed alone reduced wave energy flux, on average, by 12 ±â€…1.4 % over 180 m of travel. The kelp forest induced an additional 7 ±â€…1.2 % decrease. Kelp-associated declines in wave energy flux were slightly greater for waves of longer periods and smaller wave heights. CONCLUSIONS: Macrocystis pyrifera forests have a limited, albeit measurable, capacity to enhance shoreline protection from nearshore waves. Expectations that giant kelp forests, whether extant or enhanced through restoration, have substantial impacts on wave-induced coastal erosion might require re-evaluation.

Biological modification of coastal pH depends on community composition and time.

Biological processes play important roles in determining how global changes manifest at local scales. Primary producers can absorb increased CO2 via daytime photosynthesis, modifying pH in aquatic ecosystems. Yet producers and consumers also increase CO2 via respiration. It is unclear whether biological modification of pH differs across the year, and, if so, what biotic and abiotic drivers underlie temporal differences. We addressed these questions using the intensive study of tide pool ecosystems in Alaska, USA, including quarterly surveys of 34 pools over 1 year and monthly surveys of five pools from spring to fall in a second year. We measured physical conditions, community composition, and changes in pH and dissolved oxygen during the day and night. We detected strong temporal patterns in pH dynamics. Our measurements indicate that pH modification varies spatially (between tide pools) and temporally (across months). This variation in pH dynamics mirrored changes in dissolved oxygen and was associated with community composition, including both relative abundance and diversity of benthic producers and consumers, whose role differed across the year, particularly at night. These results highlight the importance of the time of year when considering the ways that community composition influences pH conditions in aquatic ecosystems.

Monitoring Bivalve Behavior and Physiology in the Laboratory and Field Using Open-Source Tools.

Bivalve molluscs have been the focus of behavioral and physiological studies for over a century, due in part to the relative ease with which their traits can be observed. The author reviews historical methods for monitoring behavior and physiology in bivalves, and how modern methods with electronic sensors can allow for a number of parameters to be measured in a variety of conditions using low-cost components and open-source tools. Open-source hardware and software tools can allow researchers to design and build custom monitoring systems to sample organismal processes and the environment, systems that can be tailored to the particular needs of a research program. The ability to leverage shared hardware and software can streamline the development process, providing greater flexibility to researchers looking to expand the number of traits they can measure, the frequency and duration of sampling, and the number of replicate devices they can afford to deploy.

Detection of Damage-Activated Metacaspase Activity by Western Blot in Plants.

Metacaspases are cysteine proteases that are present in plants, protists, fungi, and bacteria. Previously, we found that physical damage, e.g., pinching with forceps or grinding on liquid nitrogen of plant tissues, activates Arabidopsis thaliana METACASPASE 4 (AtMCA4). AtMCA4 subsequently cleaves PROPEP1, the precursor pro-protein of the plant elicitor peptide 1 (Pep1). Here, we describe a protein extraction method to detect activation of AtMCA4 by Western blot with antibodies against endogenous AtMCA4 and a PROPEP1-YFP fusion protein. It is important to (1) keep plant tissues at all times on liquid nitrogen prior to protein extraction, and (2) denature the protein lysate as fast as possible, as metacaspase activation ensues quasi immediately because of tissue damage inherent to protein extraction. In theory, this method can serve to detect damage-induced alterations of any protein-of-interest in any organism for which antibodies or fusion proteins are available, and hence, will greatly aid the study of rapid damage-activated proteolysis in the future.

Accounting for variation in temperature and oxygen availability when quantifying marine ecosystem metabolism.

It is critical to understand how human modifications of Earth's ecosystems are influencing ecosystem functioning, including net and gross community production (NCP and GCP, respectively) and community respiration (CR). These responses are often estimated by measuring oxygen production in the light (NCP) and consumption in the dark (CR), which can then be combined to estimate GCP. However, the method used to create "dark" conditions-either experimental darkening during the day or taking measurements at night-could result in different estimates of respiration and production, potentially affecting our ability to make integrative predictions. We tested this possibility by measuring oxygen concentrations under daytime ambient light conditions, in darkened tide pools during the day, and during nighttime low tides. We made measurements every 1-3 months over one year in southeastern Alaska. Daytime respiration rates were substantially higher than those measured at night, associated with higher temperature and oxygen levels during the day and leading to major differences in estimates of GCP calculated using daytime versus nighttime measurements. Our results highlight the potential importance of measuring respiration rates during both day and night to account for effects of temperature and oxygen-especially in shallow-water, constrained systems-with implications for understanding the impacts of global change on ecosystem metabolism.

Historical comparisons of body size are sensitive to data availability and ecological context.

Historical comparisons of body size often lack pertinent details, including information on the sampling protocol and relevant ecological covariates that influence body size. Moreover, historical estimates of body size that rely on museum specimens may be biased towards larger size classes because of collector preferences, and thus size thresholds have been used to focus attention on maximum body size. We tested the consequences of sampling design, ecological covariates, and size thresholds on inferences of body-size change using field-contextualized historical records, rather than museum specimens. In 2014-2015, we revisited historical (1947-1963) size-frequency distributions of three gastropods (Tegula funebralis, Lottia digitalis/L. austrodigitalis, Littorina keenae) in the context of population density and tidal height. In general, gastropods declined in size. However, our inferences regarding body-size decline were tempered when the variation between sampling units was taken into consideration, resulting in greater uncertainty around the estimate of proportional change in body size. Gastropod size was correlated with population density and tidal height, and these relationships varied over time. Finally, the magnitude and direction of body-size change varied with the amount of data available for analysis, demonstrating that the use of size thresholds can lead to incomplete conclusions.

Temperature affects susceptibility of intertidal limpets to bird predation.

High temperatures resulting in physiological stress and the reduced ability to resist predation can have life-or-death consequences for an organism. We investigated the effects of temperature on the susceptibility to predation for an ectothermic intertidal mollusc (the owl limpet, Lottia gigantea) and its predator (the black oystercatcher, Haematopus bachmani). The ability of L. gigantea to resist bird predation during low tide is determined by the tenacity of attachment to the rock. We developed a transducer to measure the force of predatory attacks on limpets by a captive black oystercatcher, and tested the hypothesis that exposure to warm temperatures during low tide emersion would affect the limpet's ability to resist dislodgement in trials with a morphometrically accurate beak mimic and a live bird. In beak mimic trials, four times as many limpets exposed to warm low tides were removed, as compared with limpets exposed to cool low tides or in 'no low tide' submerged conditions. Minimum time before limpet removal in captive bird trials was more than six times longer for limpets in cool low tide or no low tide treatments compared with limpets in the warm low tide treatment. We measured shear forces up to 36.63 N during predatory strikes. These direct measurements of the forces exerted by a living oystercatcher provide context for interactions with multiple prey species. Our data suggest that naturally occurring variation in body temperatures among individual prey items in the field could be an important driver of predator-prey interactions and subsequently community patterns.

Repeatable patterns of small-scale spatial variation in intertidal mussel beds and their implications for responses to climate change.

The interaction of ocean conditions and weather with small-scale physical features of a habitat can have profound effects on the experiences of individual organisms. On topographically complex shorelines, and particularly within dense aggregations of organisms such as mussel beds, a mosaic of environmental conditions can develop, and the resulting variation in conditions within the aggregation could drastically alter the performance of neighboring individuals. Using a suite of sensors mounted to individual Mytilus californianus mussels over two summer field deployments, we have characterized the temperature variation and valve gaping behavior differences found at two spatial scales: within a group separated by centimeters, and between groups of mussels located at the upper and lower extents of the natural mussel zone separated by meters. While temperature conditions near the lower edge of the mussel bed were generally more benign, temperature extremes were similar at both heights in the bed, and variation in body temperature among neighbors increased as the daily mean temperature increased. These patterns were similar across years despite a 3.8 °C difference in mean air and seawater temperatures between years. Gaping behavior was also highly variable among individuals, though that variability diminished at the high end of the mussel bed where the total time mussels spent submerged was much more constrained. These data indicate that an individual mussel's physiological status and past history can be drastically different than those of its nearby neighbors, complicating our ability to characterize representative conditions within a habitat. These observations also provide for the possibility that the impacts of future climate change will be highly specific to certain individuals based on their relative exposure or protection within the mosaic. To address such possibilities, future work must examine the correlation between genotypic and physiological traits that determine performance and individuals' unique experiences in their disparate micro-environments.

Thermal history and gape of individual Mytilus californianus correlate with oxidative damage and thermoprotective osmolytes.

The ability of animals to cope with environmental stress depends - in part - on past experience, yet knowledge of the factors influencing an individual's physiology in nature remains underdeveloped. We used an individual monitoring system to record body temperature and valve gaping behavior of rocky intertidal zone mussels (Mytilus californianus). Thirty individuals were selected from two mussel beds (wave-exposed and wave-protected) that differ in thermal regime. Instrumented mussels were deployed at two intertidal heights (near the lower and upper edges of the mussel zone) and in a continuously submerged tidepool. Following a 23-day monitoring period, measures of oxidative damage to DNA and lipids, antioxidant capacities (catalase activity and peroxyl radical scavenging) and tissue contents of organic osmolytes were obtained from gill tissue of each individual. Univariate and multivariate analyses indicated that inter-individual variation in cumulative thermal stress is a predominant driver of physiological variation. Thermal history over the outplant period was positively correlated with oxidative DNA damage. Thermal history was also positively correlated with tissue contents of taurine, a thermoprotectant osmolyte, and with activity of the antioxidant enzyme catalase. Origin site differences, possibly indicative of developmental plasticity, were only significant for catalase activity. Gaping behavior was positively correlated with tissue contents of two osmolytes. Overall, these results are some of the first to clearly demonstrate relationships between inter-individual variation in recent experience in the field and inter-individual physiological variation, in this case within mussel beds. Such micro-scale, environmentally mediated physiological differences should be considered in attempts to forecast biological responses to a changing environment.

Multimodal in situ datalogging quantifies inter-individual variation in thermal experience and persistent origin effects on gaping behavior among intertidal mussels (Mytilus californianus).

In complex habitats, environmental variation over small spatial scales can equal or exceed larger-scale gradients. This small-scale variation may allow motile organisms to mitigate stressful conditions by choosing benign microhabitats, whereas sessile organisms may rely on other behaviors to cope with environmental stresses in these variable environments. We developed a monitoring system to track body temperature, valve gaping behavior and posture of individual mussels (Mytilus californianus) in field conditions in the rocky intertidal zone. Neighboring mussels' body temperatures varied by up to 14°C during low tides. Valve gaping during low tide and postural adjustments, which could theoretically lower body temperature, were not commonly observed. Rather, gaping behavior followed a tidal rhythm at a warm, high intertidal site; this rhythm shifted to a circadian period at a low intertidal site and for mussels continuously submerged in a tidepool. However, individuals within a site varied considerably in time spent gaping when submerged. This behavioral variation could be attributed in part to persistent effects of the mussels' developmental environment. Mussels originating from a wave-protected, warm site gaped more widely, and remained open for longer periods during high tide than mussels from a wave-exposed, cool site. Variation in behavior was modulated further by recent wave heights and body temperatures during the preceding low tide. These large ranges in body temperatures and durations of valve closure events - which coincide with anaerobic metabolism - support the conclusion that individuals experience 'homogeneous' aggregations such as mussel beds in dramatically different fashion, ultimately contributing to physiological variation among neighbors.

Long-term, high frequency in situ measurements of intertidal mussel bed temperatures using biomimetic sensors.

At a proximal level, the physiological impacts of global climate change on ectothermic organisms are manifest as changes in body temperatures. Especially for plants and animals exposed to direct solar radiation, body temperatures can be substantially different from air temperatures. We deployed biomimetic sensors that approximate the thermal characteristics of intertidal mussels at 71 sites worldwide, from 1998-present. Loggers recorded temperatures at 10-30 min intervals nearly continuously at multiple intertidal elevations. Comparisons against direct measurements of mussel tissue temperature indicated errors of ~2.0-2.5 °C, during daily fluctuations that often exceeded 15°-20 °C. Geographic patterns in thermal stress based on biomimetic logger measurements were generally far more complex than anticipated based only on 'habitat-level' measurements of air or sea surface temperature. This unique data set provides an opportunity to link physiological measurements with spatially- and temporally-explicit field observations of body temperature.

Global threats from invasive alien species in the twenty-first century and national response capacities.

Invasive alien species (IAS) threaten human livelihoods and biodiversity globally. Increasing globalization facilitates IAS arrival, and environmental changes, including climate change, facilitate IAS establishment. Here we provide the first global, spatial analysis of the terrestrial threat from IAS in light of twenty-first century globalization and environmental change, and evaluate national capacities to prevent and manage species invasions. We find that one-sixth of the global land surface is highly vulnerable to invasion, including substantial areas in developing economies and biodiversity hotspots. The dominant invasion vectors differ between high-income countries (imports, particularly of plants and pets) and low-income countries (air travel). Uniting data on the causes of introduction and establishment can improve early-warning and eradication schemes. Most countries have limited capacity to act against invasions. In particular, we reveal a clear need for proactive invasion strategies in areas with high poverty levels, high biodiversity and low historical levels of invasion.

A tide prediction and tide height control system for laboratory mesocosms.

Experimental mesocosm studies of rocky shore and estuarine intertidal systems may benefit from the application of natural tide cycles to better replicate variation in immersion time, water depth, and attendant fluctuations in abiotic and edaphic conditions. Here we describe a stand-alone microcontroller tide prediction open-source software program, coupled with a mechanical tidal elevation control system, which allows continuous adjustment of aquarium water depths in synchrony with local tide cycles. We used this system to monitor the growth of Spartina foliosa marsh cordgrass and scale insect herbivores at three simulated shore elevations in laboratory mesocosms. Plant growth decreased with increasing shore elevation, while scale insect population growth on the plants was not strongly affected by immersion time. This system shows promise for a range of laboratory mesocosm studies where natural tide cycling could impact organism performance or behavior, while the tide prediction system could additionally be utilized in field experiments where treatments need to be applied at certain stages of the tide cycle.

Thermal stress and predation risk trigger distinct transcriptomic responses in the intertidal snail Nucella lapillus.

Thermal stress and predation risk have profound effects on rocky shore organisms, triggering changes in their feeding behaviour, morphology and metabolism. Studies of thermal stress have shown that underpinning such changes in several intertidal species are specific shifts in gene and protein expression (e.g. upregulation of heat-shock proteins). But relatively few studies have examined genetic responses to predation risk. Here, we use next-generation RNA sequencing (RNA-seq) to examine the transcriptomic (mRNA) response of the snail Nucella lapillus to thermal stress and predation risk. We found that like other intertidal species, N. lapillus displays a pronounced genetic response to thermal stress by upregulating many heat-shock proteins and other molecular chaperones. In contrast, the presence of a crab predator (Carcinus maenas) triggered few significant changes in gene expression in our experiment, and this response showed no significant overlap with the snail's response to thermal stress. These different gene expression profiles suggest that thermal stress and predation risk could pose distinct and potentially additive challenges for N. lapillus and that genetic responses to biotic stresses such as predation risk might be more complex and less uniform across species than genetic responses to abiotic stresses such as thermal stress.

Climate change enhances the negative effects of predation risk on an intermediate consumer.

Predators are a major source of stress in natural systems because their prey must balance the benefits of feeding with the risk of being eaten. Although this 'fear' of being eaten often drives the organization and dynamics of many natural systems, we know little about how such risk effects will be altered by climate change. Here, we examined the interactive consequences of predator avoidance and projected climate warming in a three-level rocky intertidal food chain. We found that both predation risk and increased air and sea temperatures suppressed the foraging of prey in the middle trophic level, suggesting that warming may further enhance the top-down control of predators on communities. Prey growth efficiency, which measures the efficiency of energy transfer between trophic levels, became negative when prey were subjected to predation risk and warming. Thus, the combined effects of these stressors may represent an important tipping point for individual fitness and the efficiency of energy transfer in natural food chains. In contrast, we detected no adverse effects of warming on the top predator and the basal resources. Hence, the consequences of projected warming may be particularly challenging for intermediate consumers residing in food chains where risk dominates predator-prey interactions.

Integrated assessment of biological invasions.

As the main witnesses of the ecological and economic impacts of invasions on ecosystems around the world, ecologists seek to provide the relevant science that informs managers about the potential for invasion of specific organisms in their region(s) of interest. Yet, the assorted literature that could inform such forecasts is rarely integrated to do so, and further, the diverse nature of the data available complicates synthesis and quantitative prediction. Here we present a set of analytical tools for synthesizing different levels of distributional and/or demographic data to produce meaningful assessments of invasion potential that can guide management at multiple phases of ongoing invasions, from dispersal to colonization to proliferation. We illustrate the utility of data-synthesis and data-model assimilation approaches with case studies of three well-known invasive species--a vine, a marine mussel, and a freshwater crayfish--under current and projected future climatic conditions. Results from the integrated assessments reflect the complexity of the invasion process and show that the most relevant climatic variables can have contrasting effects or operate at different intensities across habitat types. As a consequence, for two of the study species climate trends will increase the likelihood of invasion in some habitats and decrease it in others. Our results identified and quantified both bottlenecks and windows of opportunity for invasion, mainly related to the role of human uses of the landscape or to disruption of the flow of resources. The approach we describe has a high potential to enhance model realism, explanatory insight, and predictive capability, generating information that can inform management decisions and optimize phase-specific prevention and control efforts for a wide range of biological invasions.

Poised to prosper? A cross-system comparison of climate change effects on native and non-native species performance.

Climate change and biological invasions are primary threats to global biodiversity that may interact in the future. To date, the hypothesis that climate change will favour non-native species has been examined exclusively through local comparisons of single or few species. Here, we take a meta-analytical approach to broadly evaluate whether non-native species are poised to respond more positively than native species to future climatic conditions. We compiled a database of studies in aquatic and terrestrial ecosystems that reported performance measures of non-native (157 species) and co-occurring native species (204 species) under different temperature, CO(2) and precipitation conditions. Our analyses revealed that in terrestrial (primarily plant) systems, native and non-native species responded similarly to environmental changes. By contrast, in aquatic (primarily animal) systems, increases in temperature and CO(2) largely inhibited native species. There was a general trend towards stronger responses among non-native species, including enhanced positive responses to more favourable conditions and stronger negative responses to less favourable conditions. As climate change proceeds, aquatic systems may be particularly vulnerable to invasion. Across systems, there could be a higher risk of invasion at sites becoming more climatically hospitable, whereas sites shifting towards harsher conditions may become more resistant to invasions.

Importance of behavior and morphological traits for controlling body temperature in littorinid snails.

For organisms living in the intertidal zone, temperature is an important selective agent that can shape species distributions and drive phenotypic variation among populations. Littorinid snails, which occupy the upper limits of rocky shores and estuaries worldwide, often experience extreme high temperatures and prolonged aerial emersion during low tides, yet their robust physiology--coupled with morphological and behavioral traits--permits these gastropods to persist and exert strong grazing control over algal communities. We use a mechanistic heat-budget model to compare the effects of behavioral and morphological traits on the body temperatures of five species of littorinid snails under natural weather conditions. Model predictions and field experiments indicate that, for all five species, the relative contribution of shell color or sculpturing to temperature regulation is small, on the order of 0.2-2 °C, while behavioral choices such as removing the foot from the substratum or reorienting the shell can lower body temperatures by 2-4 °C on average. Temperatures in central California rarely exceeded the thermal tolerance limits of the local littorinid species during the study period, but at sites where snails are regularly exposed to extreme high temperatures, the functional significance of the tested traits may be important. The mechanistic approach used here provides the ability to gauge the importance of behavioral and morphological traits for controlling body temperature as species approach their physiological thresholds.

Heat-shock protein 70 (Hsp70) expression in four limpets of the genus Lottia: interspecific variation in constitutive and inducible synthesis correlates with in situ exposure to heat stress.

Limpets of the genus Lottia occupy a broad vertical distribution on wave-exposed rocky shores, a range that encompasses gradients in the frequency and severity of thermal and desiccation stress brought on by aerial emersion. Using western blot analysis of levels of heat-shock protein 70 (Hsp70), we examined the heat-shock responses of four Lottia congeners: Lottia scabra and L. austrodigitalis, which occur in the high-intertidal zone, and L. pelta and L. scutum, which are restricted to the low- and mid-intertidal zones. Our results suggest distinct strategies of Hsp70 expression in limpets occupying different heights and orientations in the rocky intertidal zone. In freshly field-collected animals and in specimens acclimated at ambient temperature ( approximately 14 degrees C) for 14 days, the two high-intertidal species had higher constitutive levels of Hsp70 than the low- and mid-intertidal species. During aerial exposure to high temperatures, the two low-shore species and L. austrodigitalis exhibited an onset of Hsp70 expression at 28 degrees C; no induction of Hsp70 occurred in L. scabra. Our findings suggest that high-intertidal congeners of Lottia employ a "preparative defense" strategy involving maintenance of high constitutive levels of Hsp70 in their cells as a mechanism for protection against periods of extreme and unpredictable heat stress.

Thermal stress on intertidal limpets: long-term hindcasts and lethal limits.

When coupled with long-term meteorological records, a heat-budget model for the limpet, Lottia gigantea, provides a wealth of information regarding environmental and topographic controls of body temperature in this ecologically important species. (1) The maximum body temperature predicted for any site (37.5 degrees C) is insufficient to kill all limpets, suggesting that acute thermal stress does not set an absolute upper limit to the elevation of L. gigantea on the shore. Therefore, the upper limit must be set by behavioral responses, sublethal effects or ecological interactions. (2) Temperatures sufficient to kill limpets are reached at only a small fraction of substratum orientations and elevations and on only three occasions in 5 years. These rare predicted lethal temperatures could easily be missed in field measurements, thereby influencing the interpretation of thermal stress. (3) Body temperature is typically higher than air temperature, but maximum air temperature can nonetheless be used as an accurate predictor of maximum body temperature. Warmer air temperatures in the future may thus cause increased mortality in this intertidal species. Interpretation of the ecological effects of elevated body temperature depends strongly on laboratory measurements of thermal stress, highlighting the need for additional research on the temporal and spatial variability of thermal limits and sublethal stress. The lengthy time series of body temperatures calculated from the heat-budget model provides insight into how these physiological measurements should be conducted.