Integrating laboratory experiments and biogeographic modelling approaches to understand sensitivity to ocean warming in rare and common marine annelids.

Among ectotherms, rare species are expected to have a narrower thermal niche breadth and reduced acclimation capacity and thus be more vulnerable to global warming than their common relatives. To assess these hypotheses, we experimentally quantified the thermal sensitivity of seven common, uncommon, and rare species of temperate marine annelids of the genus Ophryotrocha to assess their vulnerability to ocean warming. We measured the upper and lower limits of physiological thermal tolerance, survival, and reproductive performance of each species along a temperature gradient (18, 24, and 30 °C). We then combined this information to produce curves of each species' fundamental thermal niche by including trait plasticity. Each thermal curve was then expressed as a habitat suitability index (HSI) and projected for the Mediterranean Sea and temperate Atlantic Ocean under a present day (1970-2000), mid- (2050-2059) and late- (2090-2099) 21st Century scenario for two climate change scenarios (RCP2.6 and RCP8.5). Rare and uncommon species showed a reduced upper thermal tolerance compared to common species, and the niche breadth and acclimation capacity were comparable among groups. The simulations predicted an overall increase in the HSI for all species and identified potential hotspots of HSI decline for uncommon and rare species along the warm boundaries of their potential distribution, though they failed to project the higher sensitivity of these species into a greater vulnerability to ocean warming. In the discussion, we provide some caveats on the implications of our results for conservation efforts.

Does plasticity in thermal tolerance trade off with inherent tolerance? The influence of setal tracheal gills on thermal tolerance and its plasticity in a group of European diving beetles.

In the face of global warming, both the absolute thermal tolerance of an ectotherm, and its ability to shift its tolerance level via acclimation, are thought to be fundamentally important. Understanding the links between tolerance and its plasticity is therefore critical to accurately predict vulnerability to warming. Previous studies in a number of ectotherm taxa suggest trade-offs in the evolution of thermal tolerance and its plasticity, something which does not, however, apply to Deronectes diving beetles, where these traits are instead positively correlated. Here we revisit the relationship between thermal tolerance and plasticity in these beetles, paying attention to a recently discovered morphological adaptation supporting under water respiration - setal tracheal gills. Hollow setae on the elytra interconnect with the beetle's tracheal system, providing a gas exchange surface that allows oxygen to be extracted directly from the water. This enables individuals to stay submerged for longer than their subelytral air stores would allow. We show that hypoxia reduced heat tolerance, especially when individuals were denied access to air, forcing them to rely solely on aquatic gas exchange. Species with higher densities of these gas-exchanging setae exhibited improved cold tolerance, but reduced heat tolerance and lower plasticity of heat tolerance. Differences in setal tracheal gill density across species were also related to habitat use: species with low gill density were found mainly in intermittent, warmer rivers, where underwater gas exchange is more problematic and risks of surfacing may be smaller. Moreover, when controlling for differences in gill density we no longer found a significant relationship between heat tolerance and its plasticity, suggesting that the previously reported positive relationship between these variables may be driven by differences in gill density. Differences in environmental conditions between the preferred habitats could simultaneously select for characteristic differences in both thermal tolerance and gill density. Such simultaneous selection may have resulted in a non-causal association between cold tolerance and gill density. For heat tolerance, the correlations with gill density could reflect a causal relationship. Species relying strongly on diffusive oxygen uptake via setal tracheal gills may have a reduced oxygen supply capacity and may be left with fewer options for matching oxygen uptake to oxygen demand during acclimation, which could explain their reduced heat tolerance and limited plasticity. Our study helps shed light on the mechanisms that underpin thermal tolerance and plasticity in diving air-breathing ectotherms, and explores how differences in thermal tolerance across species are linked to their selected habitat, morphological adaptations and evolutionary history.

Metabolic and reproductive plasticity of core and marginal populations of the eurythermic saline water bug Sigara selecta (Hemiptera: Corixidae) in a climate change context.

Ongoing climate change is driving dramatic range shifts in diverse taxa worldwide, and species responses to global change are likely to be determined largely by population responses at geographical range margins. Here we investigate the metabolic and reproductive plasticity in response to water temperature and salinity variation of two populations of the eurythermic saline water bug Sigara selecta: one population located close to the northern edge of its distribution, in a relatively cold, thermally stable region (SE England - 'marginal'), and one close to the range centre, in a warmer and more thermally variable Mediterranean climate (SE Spain - 'core'). We compared metabolic and oviposition rates and egg size, following exposure to one of four different combinations of temperature (15 and 25°C) and salinity (10 and 35gL-1). Oviposition rate was significantly higher in the marginal population, although eggs laid were smaller overall. No significant differences in oxygen consumption rates were found between core and marginal populations, although the marginal population showed higher levels of plasticity in both metabolic and reproductive traits. Our results suggest that population-specific responses to environmental change are complex and may be mediated by differences in phenotypic plasticity. In S. selecta, the higher plasticity of the marginal population may facilitate both its persistence in current habitats and northward expansion with future climatic warming. The less plastic core population may be able to buffer current environmental variability with minor changes in metabolism and fecundity, but could be prone to extinction if temperature and salinity changes exceed physiological tolerance limits in the future.

Living in warmer, more acidic oceans retards physiological recovery from tidal emersion in the velvet swimming crab, Necora puber.

The distribution patterns of many species in the intertidal zone are partly determined by their ability to survive and recover from tidal emersion. During emersion, most crustaceans experience gill collapse, impairing gas exchange. Such collapse generates a state of hypoxemia and a hypercapnia-induced respiratory acidosis, leading to hyperlactaemia and metabolic acidosis. However, how such physiological responses to emersion are modified by prior exposure to elevated CO2 and temperature combinations, indicative of future climate change scenarios, is not known. We therefore investigated key physiological responses of velvet swimming crabs, Necora puber, kept for 14 days at one of four pCO2/temperature treatments (400 µatm/10°C, 1000 µatm/10°C, 400 µatm/15°C or 1000 µatm/15°C) to experimental emersion and recovery. Pre-exposure to elevated pCO2 and temperature increased pre-emersion bicarbonate ion concentrations [HCO3(-)], increasing resistance to short periods of emersion (90 min). However, there was still a significant acidosis following 180 min emersion in all treatments. The recovery of extracellular acid-base via the removal of extracellular pCO2 and lactate after emersion was significantly retarded by exposure to both elevated temperature and pCO2. If elevated environmental pCO2 and temperature lead to slower recovery after emersion, then some predominantly subtidal species that also inhabit the low to mid shore, such as N. puber, may have a reduced physiological capacity to retain their presence in the low intertidal zone, ultimately affecting their bathymetric range of distribution, as well as the structure and diversity of intertidal assemblages.

Multiple physiological responses to multiple environmental challenges: an individual approach.

The injection of anthropogenically-produced CO2 into the atmosphere will lead to an increase in temperature and a decrease in pH at the surface of the oceans by 2100. Marine intertidal organisms possess the ability to cope in the short term with environmental fluctuations exceeding predicted values. However, how they will cope with chronic exposure to elevated temperature and pCO2 is virtually unknown. In addition, individuals from the same species/population often show remarkable levels of variation in their responses to complex climatic changes: in particular, variation in metabolic rates often is linked to differences in individuals' performances and fitness. Despite its ecological and evolutionary importance, inter-individual variation has rarely been investigated within the context of climatic changes, and most investigations have typically employed orthogonal experimental designs paired to analyses of independent samples. Although this is undoubtedly a powerful and useful approach, it may not be the most appropriate for understanding all alterations of biological functions in response to environmental changes. An individual approach arguably should be favored when trying to describe organisms' responses to climatic change. Consequently, to test which approach had the greater power to discriminate the intensity and direction of an organism's response to complex climatic changes, we investigated the extracellular osmo/iono-regulatory abilities, upper thermal tolerances (UTTs), and metabolic rates of individual adults of an intertidal amphipod, Echinogammarus marinus, exposed for 15 days to combined elevated temperature and pCO2. The individual approach led to stronger and different predictions on how ectotherms will likely respond to ongoing complex climatic change, compared with the independent approaches. Consequently, this may call into question the relevance, or even the validity, of some of the predictions made to date. Finally, we argue that treating individual differences as biologically meaningful can lead to a better understanding of the physiological responses themselves and the selective processes that will occur with complex climatic changes; selection will likely play a crucial role in defining species' responses to future environmental changes. Individuals with higher metabolic rates were also characterized by greater extracellular osmo/iono-regulative abilities and higher UTTs, and thus there appeared to be no evolutionary trade-offs between these functions. However, as individuals with greater metabolic rates also have greater costs for maintenance and repair, and likely a lower fraction of energy available for growth and reproduction, trade-offs between life-history and physiological performance may still arise.

Distribution of sea urchins living near shallow water CO2 vents is dependent upon species acid-base and ion-regulatory abilities.

To reduce the negative effect of climate change on Biodiversity, the use of geological CO2 sequestration has been proposed; however leakage from underwater storages may represent a risk to marine life. As extracellular homeostasis is important in determining species' ability to cope with elevated CO2, we investigated the acid-base and ion regulatory responses, as well as the density, of sea urchins living around CO2 vents at Vulcano, Italy. We conducted in situ transplantation and field-based laboratory exposures to different pCO2/pH regimes. Our results confirm that sea urchins have some ability to regulate their extracellular fluid under elevated pCO2. Furthermore, we show that even in closely-related taxa divergent physiological capabilities underlie differences in taxa distribution around the CO2 vent. It is concluded that species distribution under the sort of elevated CO2 conditions occurring with leakages from geological storages and future ocean acidification scenarios, may partly be determined by quite subtle physiological differentiation.

The comparative biology of diving in two genera of European Dytiscidae (Coleoptera).

Surfacing behaviour is fundamental in the ecology of aquatic air-breathing organisms; however, it is only in vertebrates that the evolutionary ecology of diving has been well characterized. Here, we explore the diving behaviour of dytiscid beetles, a key group of surface-exchanging freshwater invertebrates, by comparing the dive responses of 25 taxa (Deronectes and Ilybius spp.) acclimated at two temperatures. The allometric slopes of dive responses in these dytiscids appear similar to those of vertebrate ectotherms, supporting the notion that metabolic mode shapes the evolution of diving performance. In both genera, beetles spend more time submerged than on the surface, and surface time does not vary with the temperature of acclimation. However, presumably in order to meet increased oxygen demand at higher temperatures, Deronectes species increase surfacing frequency, whereas Ilybius species decrease dive time, an example of 'multiple solutions.' Finally, widespread northern species appear to possess higher diving performances than their geographically restricted southern relatives, something which may have contributed to their range expansion ability.

The sandhopper Talitrus saltator (Crustacea: Amphipoda) as a biomonitor of trace metal bioavailabilities in European coastal waters.

The amphipod crustacean Talitrus saltator is an established, easily accessible, biomonitor of trace metal bioavailabilities in coastal waters. We have carried out a geographically widespread collection of T. saltator from European shores, stretching from the north-west Atlantic through the Baltic to the Mediterranean. A primary aim of the work was to establish a database of accumulated trace metal concentrations (Cd, Cr, Cu, Fe, Mn and Zn) in this biomonitor. Statistical analysis has shown significant geographical differences in the bioavailabilities of all the metals, the most distinct being copper, iron and manganese. It has proved possible to identify unusually high accumulated concentrations of Cd, Cr, Cu, Fe, Mn and Zn in this biomonitor, indicative of high metal bioavailability at a particular site. These may serve as reference points for future biomonitoring programmes seeking to identify metal contamination in coastal waters.

Mediterranean Talitrus saltator (Crustacea, Amphipoda) as a biomonitor of heavy metals contamination.

The use of sandhoppers and beachfleas as biomonitors of heavy metals contamination is relatively recent. Using adult individuals of Talitrus saltator from nine localities on the northern Mediterranean Sea, we studied the concentrations of eight trace elements: Al, Cd, Cr, Fe, Hg, Pb, Cu, Zn, both in the substratum and in the individuals. We also carried out a preliminary investigation of the correspondence between the sandhoppers' genetic variability and heavy metal contamination at the sampling sites. T. saltator accumulated Cd, Cu, Zn and Hg (at higher concentrations than in the sand) and also Al and Fe (at lower concentrations than in the sand). It seems that Mediterranean sandhoppers do not accumulate Pb and Cr. An intraspecific comparison between northern European (Baltic) and Mediterranean populations of T. saltator was made. Finally, we observed a tendency to a positive correlation between the sandhoppers' genetic variability and heavy metals contamination.