Ocean acidification increases susceptibility to sub-zero air temperatures in ecosystem engineers and limits poleward range shifts.

Ongoing climate change has caused rapidly increasing temperatures and an unprecedented decline in seawater pH, known as ocean acidification. Increasing temperatures are redistributing species toward higher and cooler latitudes that are most affected by ocean acidification. While the persistence of intertidal species in cold environments is related to their capacity to resist sub-zero air temperatures, studies have never considered the interacting impacts of ocean acidification and freeze stress on species survival and distribution. Here, a full-factorial experiment was used to study whether ocean acidification increases mortality in subtidal Mytilus trossulus and subtidal M. galloprovincialis, and intertidal M. trossulus following sub-zero air temperature exposure. We examined physiological processes behind variation in freeze tolerance using 1H NMR metabolomics, analyses of fatty acids, and amino acid composition. We show that low pH conditions (pH = 7.5) significantly decrease freeze tolerance in both intertidal and subtidal populations of Mytilus spp. Under current day pH conditions (pH = 7.9), intertidal M. trossulus was more freeze tolerant than subtidal M. trossulus and subtidal M. galloprovincialis. Conversely, under low pH conditions, subtidal M. trossulus was more freeze tolerant than the other mussel categories. Differences in the concentration of various metabolites (cryoprotectants) or in the composition of amino acids and fatty acids could not explain the decrease in survival. These results suggest that ocean acidification can offset the poleward range expansions facilitated by warming and that reduced freeze tolerance could result in a range contraction if temperatures become lethal at the equatorward edge.

The journey of hull-fouling mobile invaders: basibionts and boldness mediate dislodgement risk during transit.

Vessel hull-fouling is responsible for most bioinvasion events in the marine environment, yet it lacks regulation in most countries. Although experts advocate a preventative approach, research efforts on pre-arrival processes are limited. The performance of mobile epifauna during vessel transport was evaluated via laboratory simulations, using the well-known invasive Japanese skeleton shrimp (Caprella mutica), and its native congener C. laeviuscula as case study. The invader did not possess any advantage in terms of inherent resistance to drag. Instead, its performance was conditioned by the complexity of secondary substrate. Dislodgement risk was significantly reduced when sessile fouling basibionts were added, which provided refugia and boosted the probability of C. mutica remaining attached from 7 to 65% in flow exposure trials. Interestingly, the invader exhibited significantly higher exploratory tendency and motility than its native congener at zero-flow conditions. Implications in terms of en-route survivorship, invasion success and macrofouling management are discussed.

Stable isotopes unravel the feeding mode-trophic position relationship in trematode parasites.

Stable isotopes have been sporadically used over the last two decades to characterise host-parasite trophic relationships. The main reason for this scarcity is the lack of an obvious pattern in the ratio of nitrogen stable isotope values (δ15 N) of parasites in comparison to their host tissues, which would be key to understand any host-parasite system dynamics. To circumvent this, we focused on a single snail host, Zeacumantus subcarinatus, and three of its trematode parasites. We used stable isotopes to investigate each host-trematode trophic relationship and shed light on the mechanisms utilised by the parasite to reroute its hosts' biomass. All our trematodes were found to be 15 N-enriched compared to their host, with their δ15 N values strongly related to their feeding behaviours: passive versus active. It was possible to 'rank' these parasite species and assess their 'relative' trophic position using δ15 N values. We also demonstrated that including a broader range of samples (e.g. host food and faeces, multiple parasite life stages) helped understand the metabolic mechanisms used by the various participants, and that using carbon stable isotope values and C:N ratios allowed to identify an important lipid requirement of these trematode parasites. Finally, we show how critical it is to not ignore parasitic infections as they can have a great influence on their host's trophic position. We have shown that by focussing on a single host species and a single taxonomic group of parasites, we can remove a certain amount of variation recorded by broader isotope studies. We hope that these data will ultimately improve our ability to place parasites in food webs, and thus improve our understanding of the connections and interactions that dictate food web dynamics.

Complex and interactive effects of ocean acidification and warming on the life span of a marine trematode parasite.

Human activities have caused an increase in atmospheric CO2 over the last 250 years, leading to unprecedented rates of change in seawater pH and temperature. These global scale processes are now commonly referred to as ocean acidification and warming, and have the potential to substantially alter the physiological performance of many marine organisms. It is vital that the effects of ocean acidification and warming on marine organisms are explored so that we can predict how marine communities may change in future. In particular, the effect of ocean acidification and warming on host-parasite dynamics is poorly understood, despite the ecological importance of these relationships. Here, we explore the response of one himasthlid trematode, Himasthla sp., an abundant and broadly distributed species of marine parasite, to combinations of elevated temperature and pCO2 that represent physiological extremes, pre-industrial conditions, and end of century predictions. Specifically, we quantified the life span of the free-living cercarial stage under elevated temperature and pCO2, focussing our research on functional life span (the time cercariae spend actively swimming) and absolute life span (the period before death). We found that the effects of temperature and pCO2 were complex and interactive. Overall, increased temperature negatively affected functional and absolute life span, e.g. across all pCO2 treatments the average time to 50% cessation of active swimming was approximately 8 h at 5 °C, 6 h at 15 °C, 4 h at 25 °C, and 2 h at 40 °C. The effect of pCO2, which significantly affected absolute life span, was highly variable across temperature treatments. These results strongly suggest that ocean acidification and warming may alter the transmission success of trematode cercariae, and potentially reduce the input of cercariae to marine zooplankton. Either outcome could substantially alter the community structure of coastal marine systems.

Caste ratio adjustments in response to perceived and realised competition in parasites with division of labour.

Colonial organisms with division of labour are assumed to achieve increased colony-level efficiency in task performance through functional specialisation of individuals into distinct castes. In social insects, ratios of individuals in different castes can adjust adaptively in response to external threats. However, whether flexibility in caste ratio also occurs in other social organisms with division of labour remains unclear. Some parasitic trematodes, in which clonal colonies within the snail intermediate host comprise a reproductive caste and a soldier caste, offer good systems to test the general nature of adaptive caste ratio adjustments. Using the trematode Philophthalmus sp. as model, we test whether trematode colonies shift their composition towards more soldiers when exposed to a sustained risk of invasion by a competitor parasite species, and/or when experiencing sustained, active competition. We also quantify the colony-level fitness impact of caste ratio adjustments, measured as the colony's output of larval infective stages. We conducted two long-term laboratory experiments on within-snail trematode colonies. First, snails harbouring Philophthalmus colonies were exposed to different levels of invasion risk by another trematode species, Maritrema novaezealandense. Second, the structure of Philophthalmus colonies was quantified after a year-long period of within-snail competition with the other trematode species. When facing the risk of invasion by a competitor, independently of the level of risk, Philophthalmus colonies showed a significant shift towards producing more soldiers, resulting in altered caste ratio. Similarly, when experiencing actual competition by another trematode established in the same snail, Philophthalmus colonies also adjusted by producing significantly more soldiers. Greater investments in defense via more soldiers had negative impacts on the establishment and size of the competitor's colonies. Nevertheless, the presence of the competitor reduced the fitness (output of infective stages) of Philophthalmus colonies, although the production of more soldiers mitigated that effect. Our findings demonstrate that trematode colonies with division of labour are capable of adaptive caste ratio adjustments in response to both the perceived threat of competition and actual competition, with trade-offs against reproductive success only apparent when soldier numbers are very high. Combined with results on social insects, our study suggests parallel adaptations of colonial organisms in phylogenetically disparate organisms.

Parasitic infection: a buffer against ocean acidification?

Recently, there has been a concerted research effort by marine scientists to quantify the sensitivity of marine organisms to ocean acidification (OA). Empirical data generated by this research have been used to predict changes to marine ecosystem health, biodiversity and productivity that will be caused by continued acidification. These studies have also found that the effects of OA on marine organisms can be significantly modified by additional abiotic stressors (e.g. temperature or oxygen) and biotic interactions (e.g. competition or predation). To date, however, the effects of parasitic infection on the sensitivity of marine organisms to OA have been largely ignored. We show that parasitic infection significantly altered the response of a marine gastropod to simulated OA conditions by reducing the mortality of infected individuals relative to uninfected conspecifics. Without the inclusion of infection data, our analysis would not have detected the significant effect of pH on host mortality. These results strongly suggest that parasitic infection may be an important confounding factor in OA research and must be taken into consideration when assessing the response of marine species to OA.

Predicting population-level risk effects of predation from the responses of individuals.

Fear of predation produces large effects on prey population dynamics through indirect risk effects that can cause even greater impacts than direct predation mortality. As yet, there is no general theoretical framework for predicting when and how these population risk effects will arise in specific prey populations, meaning that there is often little consideration given to the key role predator risk effects can play in understanding conservation and wildlife management challenges. Here, we propose that population predator risk effects can be predicted through an extension of individual risk trade-off theory and show for the first time that this is the case in a wild vertebrate system. Specifically, we demonstrate that the timing (in specific months of the year), occurrence (at low food availability), cause (reduction in individual energy reserves), and type (starvation mortality) of a population-level predator risk effect can be successfully predicted from individual responses using a widely applicable theoretical framework (individual-based risk trade-off theory). Our results suggest that individual-based risk trade-off frameworks could allow a wide range of population-level predator risk effects to be predicted from existing ecological theory, which would enable risk effects to be more routinely integrated into consideration of population processes and in applied situations such as conservation.

Cultural transmission of tool use by Indo-Pacific bottlenose dolphins (Tursiops sp.) provides access to a novel foraging niche.

Culturally transmitted tool use has important ecological and evolutionary consequences and has been proposed as a significant driver of human evolution. Such evidence is still scarce in other animals. In cetaceans, tool use has been inferred using indirect evidence in one population of Indo-Pacific bottlenose dolphins (Tursiops sp.), where particular dolphins ('spongers') use marine sponges during foraging. To date, evidence of whether this foraging tactic actually provides access to novel food items is lacking. We used fatty acid (FA) signature analysis to identify dietary differences between spongers and non-spongers, analysing data from 11 spongers and 27 non-spongers from two different study sites. Both univariate and multivariate analyses revealed significant differences in FA profiles between spongers and non-spongers between and within study sites. Moreover, FA profiles differed significantly between spongers and non-spongers foraging within the same deep channel habitat, whereas the profiles of non-spongers from deep channel and shallow habitats at this site could not be distinguished. Our results indicate that sponge use by bottlenose dolphins is linked to significant differences in diet. It appears that cultural transmission of tool use in dolphins, as in humans, allows the exploitation of an otherwise unused niche.

Cetacean range and climate in the eastern North Atlantic: future predictions and implications for conservation.

There is increasing evidence that the distributions of a large number of species are shifting with global climate change as they track changing surface temperatures that define their thermal niche. Modelling efforts to predict species distributions under future climates have increased with concern about the overall impact of these distribution shifts on species ecology, and especially where barriers to dispersal exist. Here we apply a bio-climatic envelope modelling technique to investigate the impacts of climate change on the geographic range of ten cetacean species in the eastern North Atlantic and to assess how such modelling can be used to inform conservation and management. The modelling process integrates elements of a species' habitat and thermal niche, and employs "hindcasting" of historical distribution changes in order to verify the accuracy of the modelled relationship between temperature and species range. If this ability is not verified, there is a risk that inappropriate or inaccurate models will be used to make future predictions of species distributions. Of the ten species investigated, we found that while the models for nine could successfully explain current spatial distribution, only four had a good ability to predict distribution changes over time in response to changes in water temperature. Applied to future climate scenarios, the four species-specific models with good predictive abilities indicated range expansion in one species and range contraction in three others, including the potential loss of up to 80% of suitable white-beaked dolphin habitat. Model predictions allow identification of affected areas and the likely time-scales over which impacts will occur. Thus, this work provides important information on both our ability to predict how individual species will respond to future climate change and the applicability of predictive distribution models as a tool to help construct viable conservation and management strategies.

Host-parasite interactions: a litmus test for ocean acidification?

The effects of ocean acidification (OA) on marine species and ecosystems have received significant scientific attention in the past 10 years. However, to date, the effects of OA on host-parasite interactions have been largely ignored. As parasites play a multidimensional role in the regulation of marine population, community, and ecosystem dynamics, this knowledge gap may result in an incomplete understanding of the consequences of OA. In addition, the impact of stressors associated with OA on host-parasite interactions may serve as an indicator of future changes to the biodiversity of marine systems. This opinion article discusses the potential effects of OA on host and parasite species and proposes the use of parasites as bioindicators of OA disturbance.

Linking sandeel consumption and the likelihood of starvation in harbour porpoises in the Scottish North Sea: could climate change mean more starving porpoises?

Sandeels are known to be negatively affected by climate change in a number of ways. This study investigated whether these changes are affecting the harbour porpoise (Phocoena phocoena), a species which consumes sandeels. Porpoise diet was examined in spring (March-May), a critical time of year for survival when sandeels are important prey, from 1993 to 2001 to provide baseline information on the proportion of sandeels consumed. When data from spring 2002 and 2003 were compared to these baseline data, the diet was found to be substantially different, with a significant and substantially smaller proportion of sandeels being consumed in March and May. There were also differences in the number of porpoises starving between the two time periods (33% in spring 2002 and 2003 died of starvation, but only 5% in the baseline period). This suggests that a lower proportion of sandeels in the diet of porpoises in spring increases the likelihood of starvation. Therefore, we suggest that the negative effects of climate change on sandeel availability may have serious negative effects on harbour porpoise populations in the North Sea by increasing the likelihood of starvation in spring.