Acclimation to cyclic hypoxia improves thermal tolerance and copper survival in the caridean shrimp Palaemon varians.

In response to the continuous variation of environmental parameters, species must be able to adjust their physiology to overcome stressful conditions, a process known as acclimatization. Numerous laboratory studies have been conducted to understand and describe the mechanisms of acclimation to one environmental stressor (e.g. cyclic hypoxia), but currently our understanding of how acclimation to one stressor can change tolerance to a subsequent stressor is limited. Here, in two different experiments, we used the shrimp Palaemon varians to test how, following 28-days acclimation to cyclic hypoxia (mimicking a cyclic hypoxic regime currently found in its natural habitat), critical thermal maximum (CTmax) and sensitivity to copper (Cu2+) exposure (30 mgL-1) changed in comparison to shrimp acclimated to normoxic conditions and then exposed to thermal stress or Cu2+. Acclimation to cyclic hypoxia improved both CTmax (~1 °C higher than controls) and survival to acute Cu2+ exposure (~30% higher than controls) and induced significant gene expression changes (i.e. up-regulation of heat shock protein 70 - HSP70, hypoxia inducible factor - HIF, phosphoenolpyruvate carboxykinase - PEPCK, glucose 6-P transporter - G6Pt, metallothionein - Mt, and down-regulation of hemocyanin - Hem) in animals acclimated to cyclic hypoxia. Our results demonstrate how acclimation to cyclic hypoxia improved tolerance to subsequent stressors, highlighting the complexity of predicting organismal performance in variable (i.e. where multiple parameters can simultaneously change during the day) environments.

Intraspecific plasticity and trans-generational adaptation of reproductive traits and early development in a temperate marine neogastropod.

Climate warming is altering the distribution of species, producing range shifts and promoting local extinctions. There is an urgent need to understand the underlying mechanisms that influence the persistence of populations across a species' distribution range in the face of global warming. Ocenebra erinaceus is a marine gastropod that exhibits high intraspecific variability in maternal investment and physiological capacity during early stages, which suggests local adaptation to natal environmental conditions. In this study, reproductive traits and trans-generational adaptation were measured in two subtidal populations: one from the middle (the Solent, UK) and another towards the southern end of their geographic distribution (Arcachon, France). Local adaptation was evaluated with a transfer experiment (i.e. Arcachon females transferred to Solent thermal conditions) and trans-generational adaptation was evaluated in the thermal tolerance response of embryos exposed to temperatures between 10 and 20 °C. This study shows that both populations have similar fitness; however, there are adaptive costs to live under their natal location, resulting in trade-offs between reproductive traits. Transferred females show lower reproductive output, which suggests that females are maladapted to live under a new environment. The trans-generational experiment demonstrates contrasting thermal tolerance ranges between populations. Adaptation to local thermal conditions was observed in transferred embryos, showing poor performance and high mortalities under the new environment. Our results provide a better understanding of intraspecific differences and adaptations across a species' distribution range and provide insights into how climate warming will impact encapsulated species exhibiting location-specific adaptation.

The role of temperature on the aerobic response of encapsulated embryos of Ocenebra erinaceus (Neogastropoda, Muricidae): A comparative study between two populations.

Climate warming can affect the developmental rate and embryonic survival of ectothermic species. However, it is largely unknown if the embryos of populations from different thermal regimes will respond differently to increased warming, potentially due to adaptations to natal environmental conditions. The effects of temperature on respiration rates and oxygen content of the intracapsular fluid were studied during the intracapsular development of Ocenebra erinaceus in two subtidal populations, one from the middle of their geographic distribution, the Solent, UK and another towards the southern portion: Arcachon, France. In this laboratory study, embryos were exposed to temperatures in the range of 14-20 °C. The encapsulation period for both populations was shorter at higher temperatures and intracapsular oxygen availability decreased as development progressed. However, the embryonic aerobic response differed between populations. Encapsulated embryos from the southern population (Arcachon) showed higher respiration rates and metabolic adjustment to elevated temperatures; however, encapsulated embryos from the Solent showed no metabolic adjustment, high capsular mortalities and limited acclimation to high temperatures. Our results suggest that aerobic response of encapsulated embryos is locally adapted to the temperature history of their natal environment and illustrates the importance of local environmental history in determining the fate of key life stages in response to a changing marine climate.

Evolution through cold and deep waters: the molecular phylogeny of the Lithodidae (Crustacea: Decapoda).

The objectives of this work are to use gene sequence data to assess the hypothesis that the Lithodinae arose from ancestors with uncalcified abdomens in shallow waters of the North-East Pacific, investigate the monophyly and interrelationships of genera within the Lithodinae and to estimate the scale and minimum number of biogeographic transitions from the shallow environment to the deep sea and vice versa. To do this, phylogenetic analysis from three mitochondrial and three nuclear markers was conducted using minimum evolution, maximum likelihood and Bayesian methods. The Lithodinae as defined to include North Pacific genus Cryptolithodes may be paraphyletic, with the Hapalogastrinae and Cryptolithodes as sister taxa. This implies that the soft-bodied abdomen of the Hapalogastrinae might not be plesiomorphic for the Lithodidae. Paralomis, Lopholithodes, Phyllolithodes, Lithodes and Neolithodes share a common ancestor, from which the North Pacific Hapalogastrinae did not descend. Lithodid ancestors are likely to have had a north Pacific, shallow water distribution and to have had planktotrophic larvae. North Pacific genus Paralithodes is paraphyletic; P. brevipes is the most basal member of the genus (as sampled) while P. camtschaticus and P. platypus are more closely related to the genera Lithodes and Neolithodes. Genera Lithodes, Neolithodes and Paralomis (as sampled) are monophyletic if Glyptolithodes is included within Paralomis. Lopholithodes is closely related to, but not included within, the Paralomis genus. Paralomis is divided into at least two major lineages: one containing South Atlantic, West African, and Indian Ocean species, and the other containing Pacific and South American species. Several species of Paralomis do not resolve consistently with any other groups sampled, implying a complex and possibly rapid global evolution early in the history of the genus. Relationships within the Lithodes genus vary between analytical methods, suggesting that conclusions may not be stable. Consistently, however, Indian Ocean and Pacific forms-L. murrayi, L. longispina and L. nintokuae form a group separated from Atlantic species such as L. santolla, L. confundens, L. maja and L. ferox.

Metabolic costs imposed by hydrostatic pressure constrain bathymetric range in the lithodid crab Lithodes maja.

The changing climate is shifting the distributions of marine species, yet the potential for shifts in depth distributions is virtually unexplored. Hydrostatic pressure is proposed to contribute to a physiological bottleneck constraining depth range extension in shallow-water taxa. However, bathymetric limitation by hydrostatic pressure remains undemonstrated, and the mechanism limiting hyperbaric tolerance remains hypothetical. Here, we assess the effects of hydrostatic pressure in the lithodid crab Lithodes maja (bathymetric range 4-790 m depth, approximately equivalent to 0.1 to 7.9 MPa hydrostatic pressure). Heart rate decreased with increasing hydrostatic pressure, and was significantly lower at ≥10.0 MPa than at 0.1 MPa. Oxygen consumption increased with increasing hydrostatic pressure to 12.5 MPa, before decreasing as hydrostatic pressure increased to 20.0 MPa; oxygen consumption was significantly higher at 7.5-17.5 MPa than at 0.1 MPa. Increases in expression of genes associated with neurotransmission, metabolism and stress were observed between 7.5 and 12.5 MPa. We suggest that hyperbaric tolerance in Lmaja may be oxygen-limited by hyperbaric effects on heart rate and metabolic rate, but that Lmaja's bathymetric range is limited by metabolic costs imposed by the effects of high hydrostatic pressure. These results advocate including hydrostatic pressure in a complex model of environmental tolerance, where energy limitation constrains biogeographic range, and facilitate the incorporation of hydrostatic pressure into the broader metabolic framework for ecology and evolution. Such an approach is crucial for accurately projecting biogeographic responses to changing climate, and for understanding the ecology and evolution of life at depth.

Hydrostatic pressure and temperature affect the tolerance of the free-living marine nematode Halomonhystera disjuncta to acute copper exposure.

Potential deep-sea mineral extraction poses new challenges for ecotoxicological research since little is known about effects of abiotic conditions present in the deep sea on the toxicity of heavy metals. Due to the difficulty of collecting and maintaining deep-sea organisms alive, a first step would be to understand the effects of high hydrostatic pressure and low temperatures on heavy metal toxicity using shallow-water relatives of deep-sea species. Here, we present the results of acute copper toxicity tests on the free-living shallow-water marine nematode Halomonhystera disjuncta, which has close phylogenetic and ecological links to the bathyal species Halomonhystera hermesi. Copper toxicity was assessed using a semi-liquid gellan gum medium at two levels of hydrostatic pressure (0.1MPa and 10MPa) and temperature (10°C and 20°C) in a fully crossed design. Mortality of nematodes in each treatment was assessed at 4 time intervals (24 and 48h for all experiments and additionally 72 and 96h for experiments run at 10°C). LC50 values ranged between 0.561 and 1.864mg Cu2+L-1 and showed a decreasing trend with incubation time. Exposure to high hydrostatic pressure significantly increased sensitivity of nematodes to copper, whereas lower temperature resulted in an apparently increased copper tolerance, possibly as a result of a slower metabolism under low temperatures. These results indicate that hydrostatic pressure and temperature significantly affect metal toxicity and therefore need to be considered in toxicity assessments for deep-sea species. Any application of pollution limits derived from studies of shallow-water species to the deep-sea mining context must be done cautiously, with consideration of the effects of both stressors.

The Effects of Temperature and Hydrostatic Pressure on Metal Toxicity: Insights into Toxicity in the Deep Sea.

Mineral prospecting in the deep sea is increasing, promoting concern regarding potential ecotoxicological impacts on deep-sea fauna. Technological difficulties in assessing toxicity in deep-sea species has promoted interest in developing shallow-water ecotoxicological proxy species. However, it is unclear how the low temperature and high hydrostatic pressure prevalent in the deep sea affect toxicity, and whether adaptation to deep-sea environmental conditions moderates any effects of these factors. To address these uncertainties we assessed the effects of temperature and hydrostatic pressure on lethal and sublethal (respiration rate, antioxidant enzyme activity) toxicity in acute (96 h) copper and cadmium exposures, using the shallow-water ecophysiological model organism Palaemon varians. Low temperature reduced toxicity in both metals, but reduced cadmium toxicity significantly more. In contrast, elevated hydrostatic pressure increased copper toxicity, but did not affect cadmium toxicity. The synergistic interaction between copper and cadmium was not affected by low temperature, but high hydrostatic pressure significantly enhanced the synergism. Differential environmental effects on toxicity suggest different mechanisms of action for copper and cadmium, and highlight that mechanistic understanding of toxicity is fundamental to predicting environmental effects on toxicity. Although results infer that sensitivity to toxicants differs across biogeographic ranges, shallow-water species may be suitable ecotoxicological proxies for deep-sea species, dependent on adaptation to habitats with similar environmental variability.

Respiratory response to temperature of three populations of Aurelia aurita polyps in northern Europe.

The benthic life stage (polyp or scyphistoma) of the bloom-forming jellyfish, Aurelia aurita (Linnaeus, 1759), also known as the moon jellyfish, contributes to the seasonal occurrence and abundance of medusa blooms via asexual reproduction. A. aurita is widely distributed in coastal areas in northern Europe, and one of the most studied jellyfish species. While the physiology of the visible medusa is largely understood, understanding of the physiology of the perennial benthic life-stage is scarce. To measure the physiological tolerance of A. aurita, the scyphistoma's temperature sensitivity across its distributional range was investigated. Respiration rates of polyps from three northern European locations exposed to 11 temperatures between 2 and 22°C were measured. There was a significant difference in respiration rate among the three polyp populations, which may reflect on differences in their thermal tolerance window. A critical temperature was reached at 14°C with the metabolic rate decreasing below and above that temperature. This pattern was less pronounced in the Norwegian population but polyps were able to survive, at least temporarily, those temperatures exceeding their natural range. While polyps collected from northern Norway, with a narrow environmental thermal window, displayed a low baseline metabolism with a Q10 value of 1.2, polyps from southern England and Scotland had Q10 values of 1.6 and 2.5, respectively. Differences in polyps' respiration rates across their distributional range suggest that populations have evolved adaptations to local environmental thermal conditions.

The effect of temperature on the evolution of per offspring investment in a globally distributed family of marine invertebrates (Crustacea: Decapoda: Lithodidae).

Within the marine environment, per offspring investment (POI) is associated with modes in larval development; an increase in POI has often been described with a decrease in temperature, as evidenced along latitudinal clines. However, the environmental drivers of POI remain largely hypothetical and have not yet been tested within an evolutionary context. Here, we test the hypothesis that developmental temperature is linked to POI within a globally distributed and diverse family of benthic crustaceans, the Lithodidae, also known as stone or king crab. To do this, we examine variations in egg diameter-a proven corollary of POI-within the Lithodidae. Based on a rare case of well-construed phylogeny, we test the relationship between egg diameter and two aspects of the maternal physical environment: water depth and temperature. We observe a significant relationship between decreasing environmental temperature and an increase in POI within genera of lithodid crabs, and independent of depth. There is a clear correlation of high levels in POI with a decrease in temperature in lithodid crab genera currently inhabiting the deep sea, all of which follow a food-independent (lecithotrophic) mode of larval development. In contrast, lithodid genera thriving in the warmer waters of shallow (continental shelf) seas follow a feeding (planktotrophic) mode in larval development. We conclude that temperature is an important factor governing POI, and discuss its importance in the evolution of larval lecithotrophy in marine invertebrates.

No barrier to emergence of bathyal king crabs on the Antarctic shelf.

Cold-water conditions have excluded durophagous (skeleton-breaking) predators from the Antarctic seafloor for millions of years. Rapidly warming seas off the western Antarctic Peninsula could now facilitate their return to the continental shelf, with profound consequences for the endemic fauna. Among the likely first arrivals are king crabs (Lithodidae), which were discovered recently on the adjacent continental slope. During the austral summer of 2010 ‒ 2011, we used underwater imagery to survey a slope-dwelling population of the lithodid Paralomis birsteini off Marguerite Bay, western Antarctic Peninsula for environmental or trophic impediments to shoreward expansion. The population density averaged ∼ 4.5 individuals × 1,000 m(-2) within a depth range of 1,100 ‒ 1,500 m (overall observed depth range 841-2,266 m). Images of juveniles, discarded molts, and precopulatory behavior, as well as gravid females in a trapping study, suggested a reproductively viable population on the slope. At the time of the survey, there was no thermal barrier to prevent the lithodids from expanding upward and emerging on the outer shelf (400- to 550-m depth); however, near-surface temperatures remained too cold for them to survive in inner-shelf and coastal environments (<200 m). Ambient salinity, composition of the substrate, and the depth distribution of potential predators likewise indicated no barriers to expansion of lithodids onto the outer shelf. Primary food resources for lithodids--echinoderms and mollusks--were abundant on the upper slope (550-800 m) and outer shelf. As sea temperatures continue to rise, lithodids will likely play an increasingly important role in the trophic structure of subtidal communities closer to shore.

Characterising multi-level effects of acute pressure exposure on a shallow-water invertebrate: insights into the kinetics and hierarchy of the stress response.

Hydrostatic pressure is an important, ubiquitous, environmental variable of particular relevance in the marine environment. However, it is widely overlooked despite recent evidence that some marine ectotherms may be demonstrating climate-driven bathymetric range shifts. Wide-ranging effects of increased hydrostatic pressure have been observed from the molecular through to the behavioural level. Still, no study has simultaneously examined these multiple levels of organisation in a single experiment in order to understand the kinetics, hierarchy and interconnected nature of such responses during an acute exposure, and over a subsequent recovery period. Here, we quantify the transcription of a set of previously characterised genes during and after acute pressure exposure in adults of the shrimp Palaemonetes varians. Further, we perform respiratory rate and behavioural analysis over the same period. Increases in expression of genes associated with stress and metabolism were observed during and after high-pressure exposure. Respiratory rate increased during exposure and into the recovery period. Finally, differential behaviour was observed under elevated hydrostatic pressure in comparison to ambient pressure. Characterising generalised responses to acute elevated pressure is a vital precursor to longer-term, acclimation-based pressure studies. Results provide a novel insight into what we term the overall stress response (OSR) to elevated pressure; a concept that we suggest to be applicable to other environmental stressors. We highlight the importance of considering more than a single component of the stress response in physiological studies, particularly in an era where environmental multi-stressor studies are proliferating.

Adaptations to Hydrothermal Vent Life in Kiwa tyleri, a New Species of Yeti Crab from the East Scotia Ridge, Antarctica.

Hydrothermal vents in the Southern Ocean are the physiologically most isolated chemosynthetic environments known. Here, we describe Kiwa tyleri sp. nov., the first species of yeti crab known from the Southern Ocean. Kiwa tyleri belongs to the family Kiwaidae and is the visually dominant macrofauna of two known vent sites situated on the northern and southern segments of the East Scotia Ridge (ESR). The species is known to depend on primary productivity by chemosynthetic bacteria and resides at the warm-eurythermal vent environment for most of its life; its short-range distribution away from vents (few metres) is physiologically constrained by the stable, cold waters of the surrounding Southern Ocean. Kiwa tylerihas been shown to present differential life history adaptations in response to this contrasting thermal environment. Morphological adaptations specific to life in warm-eurythermal waters, as found on - or in close proximity of - vent chimneys, are discussed in comparison with adaptations seen in the other two known members of the family (K. hirsuta, K. puravida), which show a preference for low temperature chemosynthetic environments.