Lack of evidence for elevated CO2-induced bottom-up effects on marine copepods: a dinoflagellate-calanoid prey-predator pair

Rising levels of atmospheric CO2 are responsible for a change in the carbonate chemistry of seawater with associated pH drops (acidification) projected to reach 0.4 units from 1950 to 2100. We investigated possible indirect effects of seawater acidification on the feeding, fecundity, and hatching success of the calanoid copepod Acartia grani, mediated by potential CO2-induced changes in the nutritional characteristics of their prey. We used as prey the autotrophic dinoflagellate Heterocapsa sp., cultured at three distinct pH levels (control: 8.17, medium: 7.96, and low: 7.75) by bubbling pure CO2 via a computer automated system. Acartia grani adults collected from a laboratory culture were acclimatized for 3 d at food suspensions of Heterocapsa from each pH treatment (ca. 500 cells/ml; 300 ?g C/l). Feeding and egg production rates of the preconditioned females did not differ significantly among the three Heterocapsa diets. Egg hatching success, monitored once per day for the 72 h, did not reveal significant difference among treatments. These results are in agreement with the lack of difference in the cellular stoichiometry (C : N, C : P, and N : P ratios) and fatty acid concentration and composition encountered between the three tested Heterocapsa treatments. Our findings disagree with those of other studies using distinct types of prey, suggesting that this kind of indirect influence of acidification on copepods may be largely associated with interspecific differences among prey items with regard to their sensitivity to elevated CO2 levels.

Zooplankton distribution and migration in low-oxygen modewater eddies

The eastern tropical North Atlantic (ETNA) features a mesopelagic oxygen minimum zone (OMZ) at approximately 300-600 m depth. Here, oxygen concentrations rarely fall below 40 µmol O2 kg-1, but are expected to decline under future projections of global warming. The recent discovery of mesoscale eddies that harbour a shallow suboxic (<5 µmol O2 kg-1) OMZ just below the mixed layer could serve to identify zooplankton groups that may be negatively or positively affected by on-going ocean deoxygenation. In spring 2014, a detailed survey of a suboxic anticyclonic modewater eddy (ACME) was carried out near the Cape Verde Ocean Observatory (CVOO), combining acoustic and optical profiling methods with stratified multinet hauls and hydrography. The multinet data revealed that the eddy was characterized by an approximately 1.5-fold increase in total area-integrated zooplankton abundance. At nighttime, when a large proportion of acoustic scatterers is ascending into the upper 150 m, a drastic reduction in mean volume backscattering (Sv, shipboard ADCP, 75kHz) within the shallow OMZ of the eddy was evident compared to the nighttime distribution outside the eddy. Acoustic scatterers were avoiding the depth range between about 85 to 120 m, where oxygen concentrations were lower than approximately 20 µmol O2 kg-1, indicating habitat compression to the oxygenated surface layer. This observation is confirmed by time-series observations of a moored ADCP (upward looking, 300kHz) during an ACME transit at the CVOO mooring in 2010. Nevertheless, part of the diurnal vertical migration (DVM) from the surface layer to the mesopelagic continued through the shallow OMZ. Based upon vertically stratified multinet hauls, Underwater Vision Profiler (UVP5) and ADCP data, four strategies have been identified to be followed by zooplankton in response to the eddy OMZ: i) shallow OMZ avoidance and compression at the surface (e.g. most calanoid copepods, euphausiids), ii) migration to the shallow OMZ core during daytime, but paying O2 debt at the surface at nighttime (e.g. siphonophores, Oncaea spp., eucalanoid copepods), iii) residing in the shallow OMZ day and night (e.g. ostracods, polychaetes), and iv) DVM through the shallow OMZ from deeper oxygenated depths to the surface and back. For strategy i), ii) and iv), compression of the habitable volume in the surface may increase prey-predator encounter rates, rendering zooplankton and micronekton more vulnerable to predation and potentially making the eddy surface a foraging hotspot for higher trophic levels. With respect to long-term effects of ocean deoxygenation, we expect avoidance of the mesopelagic OMZ to set in if oxygen levels decline below approximately 20 µmol O2 kg-1. This may result in a positive feedback on the OMZ oxygen consumption rates, since zooplankton and micronekton respiration within the OMZ as well as active flux of dissolved and particulate organic matter into the OMZ will decline.

Data compilation of dinoflagellates growth rate, grazing rate and gross gowth efficiency from field and labratory experiments

The present data compilation includes dinoflagellates growth rate, grazing rate and gross growth efficiency determined either in the field or in laboratory experiments. From the existing literature, we synthesized all data that we could find on dinoflagellates. Some sources might be missing but none were purposefully ignored. We did not include autotrophic dinoflagellates in the database, but mixotrophic organisms may have been included. This is due to the large uncertainty about which taxa are mixotrophic, heterotrophic or symbiont bearing. Field data on microzooplankton grazing are mostly comprised of grazing rate using the dilution technique with a 24h incubation period. Laboratory grazing and growth data are focused on pelagic ciliates and heterotrophic dinoflagellates. The experiment measured grazing or growth as a function of prey concentration or at saturating prey concentration (maximal grazing rate). When considering every single data point available (each measured rate for a defined predator-prey pair and a certain prey concentration) there is a total of 801 data points for the dinoflagellates, counting experiments that measured growth and grazing simultaneously as 1 data point.

Data compilation of ciliates growth rate, grazing rate and gross gowth efficiency from field and labratory experiments

The present data compilation includes ciliates growth rate, grazing rate and gross growth efficiency determined either in the field or in laboratory experiments. From the existing literature, we synthesized all data that we could find on cilliate. Some sources might be missing but none were purposefully ignored. Field data on microzooplankton grazing are mostly comprised of grazing rate using the dilution technique with a 24h incubation period. Laboratory grazing and growth data are focused on pelagic ciliates and heterotrophic dinoflagellates. The experiment measured grazing or growth as a function of prey concentration or at saturating prey concentration (maximal grazing rate). When considering every single data point available (each measured rate for a defined predator-prey pair and a certain prey concentration) there is a total of 1485 data points for the ciliates, counting experiments that measured growth and grazing simultaneously as 1 data point.

Putting prey and predator into the CO2 equation-qualitative and quantitative effects of ocean acidification on predator-prey interactions

Little is known about the impact of ocean acidification on predator-prey dynamics. Herein, we examined the effect of carbon dioxide (CO(2)) on both prey and predator by letting one predatory reef fish interact for 24 h with eight small or large juvenile damselfishes from four congeneric species. Both prey and predator were exposed to control or elevated levels of CO(2). Mortality rate and predator selectivity were compared across CO(2) treatments, prey size and species. Small juveniles of all species sustained greater mortality at high CO(2) levels, while large recruits were not affected. For large prey, the pattern of prey selectivity by predators was reversed under elevated CO(2). Our results demonstrate both quantitative and qualitative consumptive effects of CO(2) on small and larger damselfish recruits respectively, resulting from CO(2)-induced behavioural changes likely mediated by impaired neurological function. This study highlights the complexity of predicting the effects of climate change on coral reef ecosystems.

Functional consequences of prey acclimation to ocean acidification for the prey and its predator

Ocean acidification is the suite of chemical changes to the carbonate system of seawater as a consequence of anthropogenic carbon dioxide (CO2) emissions. Despite a growing body of evidences demonstrating the negative effects of ocean acidification on marine species, the consequences at the ecosystem level are still unclear. One factor limiting our ability to upscale from species to ecosystem is the poor mechanistic understanding of the functional consequences of the observed effects on organisms. This is particularly true in the context of species interactions. The aim of this work was to investigate the functional consequence of the exposure of a prey (the mussel Brachidontes pharaonis) to ocean acidification for both the prey and its predator (the crab Eriphia verrucosa). Mussels exposed to pH 7.5 for >4 weeks showed significant decreases in condition index and in mechanical properties (65% decrease in maximum breaking load) as compared with mussels acclimated to pH 8.0. This translated into negative consequences for the mussel in presence of the predator crab. The crab feeding efficiency increased through a significant 27% decrease in prey handling time when offered mussels acclimated to the lowest pH. The predator was also negatively impacted by the acclimation of the prey, probably as a consequence of a decreased food quality. When fed with prey acclimated under decreased pH for 3 months, crab assimilation efficiency significantly decreased by 30% and its growth rate was 5 times slower as compared with crab fed with mussels acclimated under high pH. Our results highlight the important to consider physiological endpoints in the context of species interactions.

Interactive effects of ocean acidification and rising sea temperatures alter predation rate and predator selectivity in reef fish communities

Ocean warming and acidification are serious threats to marine life. While each stressor alone has been studied in detail, their combined effects on the outcome of ecological interactions are poorly understood. We measured predation rates and predator selectivity of two closely related species of damselfish exposed to a predatory dottyback. We found temperature and CO2 interacted synergistically on overall predation rate, but antagonistically on predator selectivity. Notably, elevated CO2 or temperature alone reversed predator selectivity, but the interaction between the two stressors cancelled selectivity. Routine metabolic rates of the two prey showed strong species differences in tolerance to CO2 and not temperature, but these differences did not correlate with recorded mortality. This highlights the difficulty of linking species-level physiological tolerance to resulting ecological outcomes. This study is the first to document both synergistic and antagonistic effects of elevated CO2 and temperature on a crucial ecological process like predator-prey dynamics.

Elevated CO2 affects predator-prey interactions through altered performance

Recent research has shown that exposure to elevated carbon dioxide (CO2) affects how fishes perceive their environment, affecting behavioral and cognitive processes leading to increased prey mortality. However, it is unclear if increased mortality results from changes in the dynamics of predator-prey interactions or due to prey increasing activity levels. Here we demonstrate that ocean pCO2 projected to occur by 2100 significantly effects the interactions of a predator-prey pair of common reef fish: the planktivorous damselfish Pomacentrus amboinensis and the piscivorous dottyback Pseudochromis fuscus. Prey exposed to elevated CO2 (880 µatm) or a present-day control (440 µatm) interacted with similarly exposed predators in a cross-factored design. Predators had the lowest capture success when exposed to elevated CO2 and interacting with prey exposed to present-day CO2. Prey exposed to elevated CO2 had reduced escape distances and longer reaction distances compared to prey exposed to present-day CO2 conditions, but this was dependent on whether the prey was paired with a CO2 exposed predator or not. This suggests that the dynamics of predator-prey interactions under future CO2 environments will depend on the extent to which the interacting species are affected and can adapt to the adverse effects of elevated CO2.

Predator nonconsumptive effects on prey recruitment weaken with recruit density, supplementary material

We investigated the nonconsumptive effects (NCEs) of predatory dogwhelks (Nucella lapillus) on intertidal barnacle (Semibalanus balanoides) recruitment through field experiments on the Gulf of St. Lawrence coast and the Atlantic coast of Nova Scotia, Canada. We studied the recruitment seasons (May-June) of 2011 and 2013. In 2011, the Gulf coast had five times more nearshore phytoplankton (food for barnacle larvae and recruits) during the recruitment season and yielded a 58% higher barnacle recruit density than the Atlantic coast at the end of the recruitment season. In 2013, phytoplankton levels and barnacle recruit density were similar on both coasts and also lower than for the Gulf coast in 2011. Using the comparative-experimental method, the manipulation of dogwhelk presence (without allowing physical contact with prey) revealed that dogwhelk cues limited barnacle recruitment under moderate recruit densities (Atlantic 2011/2013 and Gulf 2013) but had no effect under a high recruit density (Gulf 2011). Barnacle recruits attract settling larvae through chemical cues. Thus, the highest recruit density appears to have neutralized dogwhelk effects. This study suggests that the predation risk perceived by settling larvae may decrease with increasing recruit density and that prey food supply may indirectly influence predator NCEs on prey recruitment.

(Table 1) Stable carbon and nitrogen isotopic ratios of potential prey species of bearded seals (Erignathus barbatus), Svalbard

Changing patterns of sea-ice distribution and extent have measurable effects on polar marine systems. Beyond the obvious impacts of key-habitat loss, it is unclear how such changes will influence ice-associated marine mammals in part because of the logistical difficulties of studying foraging behaviour or other aspects of the ecology of large, mobile animals at sea during the polar winter. This study investigated the diet of pregnant bearded seals (Erignathus barbatus) during three spring breeding periods (2005, 2006 and 2007) with markedly contrasting ice conditions in Svalbard using stable isotopes (d13C and d15N) measured in whiskers collected from their newborn pups. The d15N values in the whiskers of individual seals ranged from 11.95 to 17.45 per mil, spanning almost 2 full trophic levels. Some seals were clearly dietary specialists, despite the species being characterised overall as a generalist predator. This may buffer bearded seal populations from the changes in prey distributions lower in the marine food web which seems to accompany continued changes in temperature and ice cover. Comparisons with isotopic signatures of known prey, suggested that benthic gastropods and decapods were the most common prey. Bayesian isotopic mixing models indicated that diet varied considerably among years. In the year with most fast-ice (2005), the seals had the greatest proportion of pelagic fish and lowest benthic invertebrate content, and during the year with the least ice (2006), the seals ate more benthic invertebrates and less pelagic fish. This suggests that the seals fed further offshore in years with greater ice cover, but moved in to the fjords when ice-cover was minimal, giving them access to different types of prey. Long-term trends of sea ice decline, earlier ice melt, and increased water temperatures in the Arctic are likely to have ecosystem-wide effects, including impacts on the forage bases of pagophilic seals.

The California current predator diet database: synthesis of common forage species

Characterization of the diets of upper-trophic predators is a key ingredient in management including the development of ecosystem-based fishery management plans, conservation efforts for top predators, and ecological and economic modeling of predator prey interactions. The California Current Predator Diet Database (CCPDD) synthesizes data from published records of predator food habits over the past century. The database includes diet information for 100+ upper-trophic level predator species, based on over 200 published citations from the California Current region of the Pacific Ocean, ranging from Baja, Mexico to Vancouver Island, Canada. We include diet data for all predators that consume forage species: seabirds, cetaceans, pinnipeds, bony and cartilaginous fishes, and a predatory invertebrate; data represent seven discrete geographic regions within the CCS (Canada, WA, OR, CA-n, CA-c, CA-s, Mexico). The database is organized around predator-prey links that represent an occurrence of a predator eating a prey or group of prey items. Here we present synthesized data for the occurrence of 32 forage species (see Table 2 in the affiliated paper) in the diet of pelagic predators (currently submitted to Ecological Informatics). Future versions of the shared-data will include diet information for all prey items consumed, not just the forage species of interest.

(Table 1) Nesting characteristics of greater snow geese (Chen caerulescens atlanticus) on Bylot Island between 1995-2005

1. Habitat heterogeneity and predator behaviour can strongly affect predator-prey interactions but these factors are rarely considered simultaneously, especially when systems encompass multiple predators and prey. 2. In the Arctic, greater snow geese Anser caerulescens atlanticus L. nest in two structurally different habitats: wetlands that form intricate networks of water channels, and mesic tundra where such obstacles are absent. In this heterogeneous environment, goose eggs are exposed to two types of predators: the arctic fox Vulpes lagopus L. and a diversity of avian predators. We hypothesized that, contrary to birds, the hunting ability of foxes would be impaired by the structurally complex wetland habitat, resulting in a lower predation risk for goose eggs. 3. In addition, lemmings, the main prey of foxes, show strong population cycles. We thus further examined how their fluctuations influenced the interaction between habitat heterogeneity and fox predation on goose eggs. 4. An experimental approach with artificial nests suggested that foxes were faster than avian predators to find unattended goose nests in mesic tundra whereas the reverse was true in wetlands. Foxes spent 3-5 times more time between consecutive attacks on real goose nests in wetlands than in mesic tundra. Their attacks on goose nests were also half as successful in wetlands than in mesic tundra whereas no difference was found for avian predators. 5. Nesting success in wetlands (65%) was higher than in mesic tundra (56%) but the difference between habitats increased during lemming crashes (15%) compared to other phases of the cycle (5%). Nests located at the edge of wetland patches were also less successful than central ones, suggesting a gradient in accessibility of goose nests in wetlands for foxes. 6. Our study shows that the structural complexity of wetlands decreases predation risk from foxes but not avian predators in arctic-nesting birds. Our results also demonstrate that cyclic lemming populations indirectly alter the spatial distribution of productive nests due to a complex interaction between habitat structure, prey-switching and foraging success of foxes.

9-28 d of exposure to elevated pCO2 reduces avoidance of predator odour but had no effect on behavioural lateralization or swimming activity in a temperate wrasse(Ctenolabrus rupestris)

Most studies on the impact of near-future levels of carbon dioxide on fish behaviour report behavioural alterations, wherefore abnormal behaviour has been suggested to be a potential consequence of future ocean acidification and therefore a threat to ocean ecosystems. However, an increasing number of studies show tolerance of fish to increased levels of carbon dioxide. This variation among studies in susceptibility highlights the importance of continued investigation of the possible effects of elevated pCO2. Here, we investigated the impacts of increased levels of carbon dioxide on behaviour using the goldsinny wrasse (Ctenolabrus rupestris), which is a common species in European coastal waters and widely used as cleaner fish to control sea lice infestation in commercial fish farming in Europe. The wrasses were exposed to control water conditions (370 µatm) or elevated pCO2 (995 µatm) for 1 month, during which time behavioural trials were performed. We investigated the possible effects of CO2 on behavioural lateralization, swimming activity, and prey and predator olfactory preferences, all behaviours where disturbances have previously been reported in other fish species after exposure to elevated CO2. Interestingly, we failed to detect effects of carbon dioxide for most behaviours investigated, excluding predator olfactory cue avoidance, where control fish initially avoided predator cue while the high CO2 group was indifferent. The present study therefore shows behavioural tolerance to increased levels of carbon dioxide in the goldsinny wrasse. We also highlight that individual fish can show disturbance in specific behaviours while being apparently unaffected by elevated pCO2 in other behavioural tests. However, using experiments with exposure times measured in weeks to predict possible effects of long-term drivers, such as ocean acidification, has limitations, and the behavioural effects from elevated pCO2 in this experiment cannot be viewed as proof that these fish would show the same reaction after decades of evolution.

Populations of Pacific Oysters Crassostrea gigas Respond Variably to Elevated CO2 and Predation by Morula marginalba

Ocean acidification is anticipated to decrease calcification and increase dissolution of shelled molluscs. Molluscs with thinner and weaker shells may be more susceptible to predation, but not all studies have measured negative responses of molluscs to elevated pCO2. Recent studies measuring the response of molluscs have found greater variability at the population level than first expected. Here we investigate the impact of acidification on the predatory whelk Morula marginalba and genetically distinct subpopulations of the Pacific oyster Crassostrea gigas. Whelks and eight family lines of C. gigas were separately exposed to ambient (385 ppm) and elevated (1000 ppm) pCO2 for 6 weeks. Following this period, individuals of M. marginalba were transferred into tanks with oysters at ambient and elevated pCO2 for 17 days. The increase in shell height of the oysters was on average 63% less at elevated compared to ambient pCO2. There were differences in shell compression strength, thickness, and mass among family lines of C. gigas, with sometimes an interaction between pCO2 and family line. Against expectations, this study found increased shell strength in the prey and reduced shell strength in the predator at elevated compared to ambient pCO2. After 10 days, the whelks consumed significantly more oysters regardless of whether C. gigas had been exposed to ambient or elevated CO2, but this was not dependent on the family line and the effect was not significant after 17 days. Our study found an increase in predation after exposure of the predator to predicted near-future levels of estuarine pCO2.

Data base on pelagic ciliates grazing and growth rate as a function of size, prey size and type compiled from the literature

Microzooplankton (the 20 to 200 µm size class of zooplankton) is recognised as an important part of marine pelagic ecosystems. In terms of biomass and abundance pelagic ciliates are one of the important groups of organism in microzooplankton. However, their rates - grazing and growth - , feeding behaviour and prey preferences are poorly known and understood. A set of data was assembled in order to derive a better understanding of pelagic ciliates rates, in response to parameters such as prey concentration, prey type (size and species), temperature and their own size. With these objectives, literature was searched for laboratory experiments with information on one or more of these parameters effect studied. The criteria for selection and inclusion in the database included: (i) controlled laboratory experiment with a known ciliates feeding on a known prey; (ii) presence of ancillary information about experimental conditions, used organisms - cell volume, cell dimensions, and carbon content. Rates and ancillary information were measured in units that meet the experimenter need, creating a need to harmonize the data units after collection. In addition different units can link to different mechanisms (carbon to nutritive quality of the prey, volume to size limits). As a result, grazing rates are thus available as pg C/(ciliate*h), µm**3/(ciliate*h) and prey cell/(ciliate*h); clearance rate was calculated if not given and growth rate is expressed as the growth rate per day.