Arctic copepod copper sensitivity and comparison with Antarctic and temperate copepods.

The ongoing global climate crisis increases temperatures in polar regions faster and with greater magnitude than elsewhere. The decline of Arctic sea ice opens up new passages, eventually leading to higher anthropogenic activities such as shipping, fishing, and mining. Climate change and anthropogenic activities will increase contaminant transport from temperate to Arctic regions. The shipping industry uses copper as an antifouling coating. Copper is an essential element but becomes toxic at excess concentrations, and its use may inadvertently affect non-target organisms such as copepods. Copper affects copepods by lowering reproductive output, prolonging developmental time, and causing increased mortality. As data on copper sensitivity of polar copepods at low temperatures are rare, we conducted onboard survival experiments with the Arctic region's most common copepod species (Calanus finmarchicus, C. glacialis, C. hyperboreus). Acute survival tests were done for up to 8 days on individuals in 70 ml bottles at 1 °C with nominal copper concentrations ranging from 3 to 480 µg L-1. We used a reduced General Unified Threshold model for Survival (GUTS) to analyse the data, and placed our results in the context of the few published copper sensitivity data of the Antarctic and temperate copepod species at low temperatures. The sensitivity of Cu exposure was similar between the three Calanus species. However, a model comparison suggests that the tested C. glacialis population is less sensitive than the other two species in our experiments. Compared to published data, the three Arctic species appear slightly less sensitive to copper compared to their Antarctic counterparts but more compared to their temperate ones. Our literature search revealed only a few available studies on the copper sensitivity of polar copepods. In the future, this species group will be exposed to more pollutants, which warrants more studies to predict potential risks, especially given possible interactions with environmental factors.

Drivers of copper sensitivity in copepods: A meta-analysis of LC50s.

Copper is both an essential trace element and a potent pesticide. The use of copper as an antifoulant has increased in the last decades in line with the expanding aquaculture and shipping industries. In aquatic environments, it also affects non-target taxa. One of which are copepods, which constitute the central link in the marine food web. Despite their ecological importance, there are no systematic reviews of the lethal concentration range and drivers of copper toxicity in this taxon. Here, we combined literature data from 31 peer-reviewed articles recording the Lethal Concentration 50 (LC50) for copper in copepods and the experiments' respective environmental, developmental, and taxonomic parameters. The LC50 is a traditional endpoint for toxicity testing used in standardized toxicity testing and many ecological studies. In total, we were able to extract 166 LC50 entries. The variability in the metadata allowed for a general analysis of the drivers of copper sensitivity in copepods. Using a generalized additive modeling approach, we find that temperature increases copper toxicity when above approximately 25℃. Counter to our expectations; salinity does not influence copper sensitivity across copepod species. Unsurprisingly, nauplii are more susceptible to copper exposure than adult copepods, and benthos-associated harpacticoids are less sensitive to copper than pelagic calanoids. Our final model can predict sensible specific-specific copper concentrations for future experiments, thus giving an informed analytical approach to range testing in future dose-response experiments. Our model can also potentially improve ecological risk assessment by accounting for environmental differences. The approach can be applied to other toxicants and taxa, which may reveal underlying patterns otherwise obscured by taxonomic and experimental variability.

Predation Risk Potentiates Toxicity of a Common Metal Contaminant in a Coastal Copepod.

To examine whether natural stressors like predation risk affect responses to anthropogenic contaminants, we exposed nauplii of the copepod Tigriopus brevicornis to chemical cues from fish (kairomones) and copper (Cu). We tested effects of these treatments, singly and combined, on copepod age and size at maturity, and development stage sensitivity, while controlling for effects of genetic heterogeneity (clutch identity). Predation risk, Cu and clutch identity interacted in their effect on development time. Predation risk alone had minor effects, but potentiated Cu toxicity in the combined treatment by doubling the delay in age at maturity, as compared to Cu exposure alone. This potentiating effect on developmental delay appeared already at the first copepodite stage. The specific strength of response varied among nauplii from different females' clutches. There were no differences in copepod size at maturity among treatments. We did, however, find an interaction between the effect of Cu and clutch identity on copepod growth. Our results demonstrate the importance of ecological interactions for potentiating the toxicity of environmental contaminants. We also demonstrate the need to consider genetic heterogeneity in ecotoxicology. Natural variation in stressor responses has implications for the interpretation of results from toxicological studies using single-clone or inbred culture populations.

Instantaneous threat escape and differentiated refuge demand among zooplankton taxa.

Most animals, including aquatic crustacean zooplankton, perform strong avoidance movements when exposed to a threat, such as ultraviolet radiation (UVR). We here show that the genera Daphnia and Bosmina instantly adjust their vertical position in the water in accordance with the present UVR threat, i.e., seek refuge in deeper waters, whereas other taxa show less response to the threat. Moreover, Daphnia repeatedly respond to UVR pulses, suggesting that they spend more energy on movement than more stationary taxa, for example, during days with fluctuating cloud cover, illustrating nonlethal effects in avoiding UVR threat. Accordingly, we also show that the taxa with the most contrasting behavioral responses differ considerably in photoprotection, suggesting different morphological and behavioral strategies in handling the UVR threat. In a broader context, our studies on individual and taxa specific responses to UVR provide insights into observed spatial and temporal distribution in natural ecosystems.

Adult and offspring size in the ocean: a database of size metrics and conversion factors.

The purpose of this dataset was to compile adult and offspring size estimates for marine organisms. Adult and offspring size estimates of 408 species were compiled from the literature covering >17 orders of magnitude in body mass and including Cephalopoda (ink fish), Cnidaria ("jelly" fish), Crustaceans, Ctenophora (comb jellies), Elasmobranchii (cartilaginous fish), Mammalia (mammals), Sagittoidea (arrow worms) and Teleost (i.e., Actinopterygii, bony fish). Individual size estimates were converted to standardized size estimates (carbon weight, g) to allow for among-group comparisons. This required a number of size estimates to be converted and a compilation of conversion factors obtained from the literature are also presented.

Temporal patterns in multiple stressors shape the vulnerability of overwintering Arctic zooplankton.

The Arctic polar nights bring extreme environmental conditions characterised by cold and darkness, which challenge the survival of organisms in the Arctic. Additionally, multiple anthropogenic stressors can amplify the pressure on the fragile Arctic ecosystems during this period. Determining how multiple anthropogenic stressors may affect the survival of Arctic life is crucial for ecological risk assessments and management, but this topic is understudied. For the first time, our study investigates the complex interactions of multiple stressors, exploring stressor temporal dynamics and exposure duration on a key Arctic copepod Calanus glacialis during the polar nights. We conducted experiments with pulse (intermittent) and press (continuous) exposure scenarios, involving microplastics, pyrene and warming in a fully factorial design. We observed significant effects on copepod survival, with pronounced impacts during later stressor phases. We also detected two-way interactions between microplastics and pyrene, as well as pyrene and warming, further intensified with the presence of a third stressor. Continuous stressor exposure for 9 days (press-temporal scenario) led to greater reductions in copepod survival compared to the pulse-temporal scenario, characterised by two 3-day stressor exposure phases. Notably, the inclusion of recovery phases, free from stressor exposure, positively influenced copepod survival, highlighting the importance of temporal exposure dynamics. We did not find behaviour to be affected by the different treatments. Our findings underscore the intricate interactions amongst multiple stressors and their temporal patterns in shaping the vulnerability of overwintering Arctic copepods with crucial implications for managing Arctic aquatic ecosystems under the fastest rate of ongoing climate change on earth.

Optimal mate choice patterns in pelagic copepods.

The importance of sexual selection for the evolution, dynamics and adaptation of organisms is well known for many species. However, the topic is rarely studied in marine plankton, the basis of the marine food web. Copepods show behaviors that suggest the existence of sexually selected traits, and recent laboratory experiments identified some selected morphological traits. Here, we use a 'life history-based' model of sex roles to determine the optimal choosiness behavior of male and female copepods for important copepod traits. Copepod females are predicted to be choosy at population densities typically occurring during the main breeding season, whereas males are not. The main drivers of this pattern are population density and the difference in non-receptive periods between males and females. This suggests that male reproductive traits have evolved mainly due to mate competition. The model can easily be parameterized for other planktonic organisms, and be used to plan experiments about sexual selection.

Zoobooth: A portable, open-source and affordable approach for repeated size measurements of live individual zooplankton.

Repeated size measurements of individual animals are valuable data for many research questions, but it is often hard to obtain without causing stress or damage to the animal. We developed a video-based approach called Zoobooth to size individual zooplankton, which involves a low risk of handling accidents and stress. Here we describe the process of assembling the instrument we used to acquire video recordings of single zooplankton and the procedure to obtain size estimates from the recorded videos. Our setup produces accurate size estimates for Daphnia magna (correlation to manual measurements = 0.97), and was also tested with other zooplankton species. Zoobooth is especially advantageous when one needs size measurements of live, individual mesozooplankton. The device is small, portable, and comprised of very affordable and readily available components. It can easily be modified for other purposes, such as studies of coloration or behavior of micro-and macro-plankton. We share all the files to build and use Zoobooth.

Coordinated gas release among the physostomous fish sprat (Sprattus sprattus).

Previous experimental studies suggest that the production of sound associated with expelling gas from an open swimbladder may play a role in communication. This would suggest non-random gas release. We used deployed echosounders to study patterns of gas release among a fjord population of sprat (Sprattus sprattus). The echosounder records concurrently revealed individual fish and their release of gas. The gas release primarily occurred at night, partly following recurrent temporal patterns, but also varying between nights. In testing for non-randomness, we formulated a data-driven simulation approach. Non-random gas release scaled with the length of the analyzed time intervals from 1 min to 6 h, and above 30 min the release events in more than 50% of the intervals were significantly connected.

Density-Dependent Metabolic Costs of Copper Exposure in a Coastal Copepod.

Traditional ecotoxicology methods involving copepods have focused on exposure of pooled individuals and averaged responses, but there is increasing awareness of the importance of individual variation. Many biological traits are density dependent, and decisions to use single-individual or pooled exposure may affect responses to anthropogenic stressors. We investigated how conspecific density as a biotic stressor affects behavioral and respiratory responses to copper (Cu) exposure in the coastal copepod Tigriopus brevicornis. Adults were incubated at densities of 1, 2, or 4 individuals per replicate in 3.2 mL of exposure medium (23 µg Cu L-1 or control). Our results show an interaction of Cu exposure and density on respiration. The Cu exposure increased respiration, but this effect diminished with increasing density. We also found reduced swimming activity with increasing density. We propose 2 nonexclusive alternative explanations for the density-dependent respiratory increase of Cu exposure: 1) a behavioral stress response to low conspecific density, or 2) increased Cu exposure due to increased swimming activity. We emphasize the importance of considering density-dependency in responses when designing and interpreting ecotoxicology studies. Environ Toxicol Chem 2021;40:2538-2546. © 2021 The Authors. Environmental Toxicology and Chemistry published by Wiley Periodicals LLC on behalf of SETAC.

The Hidden Dimension: Context-Dependent Expression of Repeatable Behavior in Copepods.

In ecotoxicology and aquatic ecology, we often ignore responses of individuals and focus on average responses. However, both terrestrial and aquatic animals display consistent behavioral differences between individuals. The distribution of behavioral differences within a population contains vital information for predicting population responses to novel environmental challenges. Currently, individual data for behavioral and physiological traits of small marine invertebrates are few, partly because such variation is lost within published group means and assumed normality. We tested the combined effects of an inorganic contaminant (copper) and a biological stressor (i.e., chemical cues of a fish predator) on activity in a marine copepod. Although direct stress effects were weak, individuals behaved consistently differently, depending on the context. Individual differences in behavior were only expressed under the influence of kairomones, but not by copper exposure alone. This finding indicates that copepods express repeatable and context-dependent behavior. We also demonstrate how large variations in behavioral data can hide consistent differences between individuals. Environ Toxicol Chem 2020;39:1017-1026. © 2020 The Authors. Environmental Toxicology and Chemistry published by Wiley Periodicals, Inc. on behalf of SETAC.

Contrasting Effects of Predation Risk and Copper on Copepod Respiration Rates.

Natural biotic and anthropogenic stressors can interact to alter contaminant toxicity. Energetic restrictions are potential mechanisms causing this pattern. To identify processes underlying observed effects of predation risk and copper (Cu) on delayed copepod age at maturity, we examined how these 2 stressors affect respiration rates. We tested 2 very different copepod species: the large, pelagic calanoid Calanus finmarchicus and the small, semibenthic harpacticoid Tigriopus brevicornis. Adult individuals were exposed for 12 h to the treatments: predation risk, Cu (23 µg L-1 ), combined predation risk and Cu (23 µg L-1 ), or control. Oxygen concentrations were monitored continuously. The 2 species differed in their responses. We found no clear effects of either stressor in C. finmarchicus. In T. brevicornis, predation risk increased respiration rates, whereas Cu alone had little impact. In contrast, combined exposure to predation risk and Cu interacted to reduce respiration rates to less than expected. We further observed an effect of sex because female-biased T. brevicornis replicates were more sensitive to both predation risk (increased respiration rates) and Cu exposure (reduced respiration rates). The present study provides further evidence that predation risk can interact with copepod responses toward Cu exposure. Interactive effects of biotic stressors ought to be considered to improve future marine environmental monitoring. Environ Toxicol Chem 2020;39:1765-1773. © 2020 The Authors. Environmental Toxicology and Chemistry published by Wiley Periodicals LLC on behalf of SETAC.

An affordable and automated imaging approach to acquire highly resolved individual data-an example of copepod growth in response to multiple stressors.

Individual trait variation is essential for populations to cope with multiple stressors and continuously changing environments. The immense number of possible stressor combinations and the influence of phenotypic variation makes experimental testing for effects on organisms challenging. The acquisition of such data requires many replicates and is notoriously laborious. It is further complicated when responses occur over short time periods. To overcome such challenges, we developed an automated imaging platform to acquire temporally highly resolved individual data. We tested this platform by exposing copepods to a combination of a biotic stressor (predator cues) and a toxicant (copper) and measured the growth response of individual copepods. We tested the automatically acquired data against published manually acquired data with much lower temporal resolution. We find the same general potentiating effects of predator cues on the adverse effects of copper, and the influence of an individual's clutch identity on its ability to resist stress, between the data obtained from low and high temporal resolution. However, when using the high temporal resolution, we also uncovered effects of clutch ID on the timing and duration of stage transitions, which highlights the importance of considering phenotypic variation in ecotoxicological testing. Phenotypic variation is usually not acknowledged in ecotoxicological testing. Our approach is scalable, affordable, and adjustable to accommodate both aquatic and terrestrial organisms, and a wide range of visually detectable endpoints. We discuss future extensions that would further widen its applicability.

Genotoxic Response and Mortality in 3 Marine Copepods Exposed to Waterborne Copper.

Copper (Cu) is an essential trace metal, but may also be toxic to aquatic organisms. Although many studies have investigated the cytotoxicity of Cu, little is known about the in vivo genotoxic potential of Cu in marine invertebrates. We investigated the genotoxicity of Cu in 2 pelagic calanoid copepods, Acartia tonsa and Temora longicornis, and the intertidal harpacticoid copepod Tigriopus brevicornis by exposing them for 6 and 72 h to waterborne Cu (0, 6, and 60 µg Cu/L). A subsequent 24-h period in filtered seawater was used to investigate delayed effects or recovery. Genotoxicity was evaluated as DNA strand breaks in individual copepods using the comet assay. Copper did not increase DNA strand breaks in any of the species at any concentration or time point. The treatment did, however, cause 100% mortality in A. tonsa following exposure to 60 µg Cu/L. Acartia tonsa and T. longicornis were more susceptible to Cu-induced mortality than the benthic harpacticoid T. brevicornis, which appeared to be unaffected by the treatments. The results show major differences in Cu susceptibility among the 3 copepods and also that acute toxicity of Cu to A. tonsa is not directly associated with genotoxicity. We also show that the comet assay can be used to quantify genotoxicity in individual copepods. Environ Toxicol Chem 2019;38:2224-2232. © 2019 SETAC.

Selective silicate-directed motility in diatoms.

Diatoms are highly abundant unicellular algae that often dominate pelagic as well as benthic primary production in the oceans and inland waters. Being strictly dependent on silica to build their biomineralized cell walls, marine diatoms precipitate 240 × 10(12) mol Si per year, which makes them the major sink in the global Si cycle. Dissolved silicic acid (dSi) availability frequently limits diatom productivity and influences species composition of communities. We show that benthic diatoms selectively perceive and behaviourally react to gradients of dSi. Cell speed increases under dSi-limited conditions in a chemokinetic response and, if gradients of this resource are present, increased directionality of cell movement promotes chemotaxis. The ability to exploit local and short-lived dSi hotspots using a specific search behaviour likely contributes to micro-scale patch dynamics in biofilm communities. On a global scale this behaviour might affect sediment-water dSi fluxes and biogeochemical cycling.

Solid phase extraction and metabolic profiling of exudates from living copepods.

Copepods are ubiquitous in aquatic habitats. They exude bioactive compounds that mediate mate finding or induce defensive traits in prey organisms. However, little is known about the chemical nature of the copepod exometabolome that contributes to the chemical landscape in pelagic habitats. Here we describe the development of a closed loop solid phase extraction setup that allows for extraction of exuded metabolites from live copepods. We captured exudates from male and female Temora longicornis and analyzed the content with high resolution LC-MS. Chemometric methods revealed 87 compounds that constitute a specific chemical pattern either qualitatively or quantitatively indicating copepod presence. The majority of the compounds were present in both female and male exudates, but nine compounds were mainly or exclusively present in female exudates and hence potential pheromone candidates. Copepodamide G, known to induce defensive responses in phytoplankton, was among the ten compounds of highest relative abundance in both male and female extracts. The presence of copepodamide G shows that the method can be used to capture and analyze chemical signals from living source organisms. We conclude that solid phase extraction in combination with metabolic profiling of exudates is a useful tool to develop our understanding of the chemical interplay between pelagic organisms.

Is sexual selection beneficial during adaptation to environmental change?

The role of sexual selection in adaptation is disputed. A balance between sexual and viability selection can be achieved in stable environments, but environmental perturbations could change the costs and benefits arising from sexual selection and influence the rate of adaptation. Here we synthesise theoretical and empirical work on the role of sexual selection in adaptation to changed conditions. Contrasting results have been gained, but the majority of studies suggest that sexual selection has no significant effect or a negative effect on the rate of adaptation. However, once sexually selected traits start to evolve, sexual selection can accelerate adaptation. The role of sexual selection in extinction appears to be minor, but the results could be skewed.

An increase in pH boosts olfactory communication in sticklebacks.

Human-induced eutrophication is a serious environmental problem that constrains visual communication and influences the mate choice process in fishes. Eutrophication also changes the chemical environment and the pH of the water, which could influence the use of olfactory cues in mate choice. Here, we show that an increase in pH enhances the use of male olfactory cues in mate choice in three-spined sticklebacks, Gasterosteus aculeatus. In a laboratory choice experiment, gravid females were more attracted to male olfactory cues when pH was raised. This could compensate for impaired visual communication in eutrophied waters and facilitate adaptive mate choice.