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.

(Table A1) Annual biomass of plants and animals recorded on Bylot Island between 1993-2009

Determining the manner in which food webs will respond to environmental changes is difficult because the relative importance of top-down vs. bottom-up forces in controlling ecosystems is still debated. This is especially true in the Arctic tundra where, despite relatively simple food webs, it is still unclear which forces dominate in this ecosystem. Our primary goal was to assess the extent to which a tundra food web was dominated by plant-herbivore or predator--rey interactions. Based on a 17-year (1993-2009) study of terrestrial wildlife on Bylot Island, Nunavut, Canada, we developed trophic mass balance models to address this question. Snow Geese were the dominant herbivores in this ecosystem, followed by two sympatric lemming species (brown and collared lemmings). Arctic foxes, weasels, and several species of birds of prey were the dominant predators. Results of our trophic models encompassing 19 functional groups showed that <10% of the annual primary production was consumed by herbivores in most years despite the presence of a large Snow Goose colony, but that 20-100% of the annual herbivore production was consumed by predators. The impact of herbivores on vegetation has also weakened over time, probably due to an increase in primary production. The impact of predators was highest on lemmings, intermediate on passerines, and lowest on geese and shorebirds, but it varied with lemming abundance. Predation of collared lemmings exceeded production in most years and may explain why this species remained at low density. In contrast, the predation rate on brown lemmings varied with prey density and may have contributed to the high-amplitude, periodic fluctuations in the abundance of this species. Our analysis provided little evidence that herbivores are limited by primary production on Bylot Island. In contrast, we measured strong predator-prey interactions, which supports the hypothesis that this food web is primarily controlled by top-down forces. The presence of allochthonous resources subsidizing top predators and the absence of large herbivores may partly explain the predominant role of predation in this low-productivity ecosystem.

(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.

(Table 1) Prey species identified from the scats of Antarctic fur seals (Arctocephalus gazella) on Bouvet Island

Intraspecific differences in the diets of many species of pinnipeds are to be expected in view of the great differences in morphology, life history and foraging behaviour between the sexes of many species. We examined the diet of the Antarctic fur seal population at Bouvetøya, Southern Ocean, to assess intersexual differences. This was made possible by the analysis of prey remains extracted from scats and regurgitations collected in areas used primarily by one or the other sex. The results indicate that both males and females feed primarily on Antarctic krill Euphausia superba with several species of fish and squid being taken, likely opportunistically given their prevalence. Significant differences were identified in the frequency of occurrence of otoliths in scats and the percentage numerical abundance of the major fish prey species in the diet. Adult males ate a smaller quantity of fish overall, but ate significantly more of the larger fish species. The greater diving capabilities of males and the fact that they are not limited in the extent of their foraging area by having to return regularly to feed dependant offspring may play a role in the differences found between the diets of males and females. Additionally, females might be more selective, favouring myctophids because they are richer in energy than krill. The absence of major differences in the diet between the sexes at this location is likely due to the high overall abundance of prey at Bouvetøya.

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.

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.

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.

Plankton abundance and feeding characteristics of Thysanoessa raschii from Godthabsfjord, Greenland

Despite being a key zooplankton group, knowledge on krill biology from the Arctic is inadequate. The present study examine the functional biology and evaluate the trophic role of krill in the Godthabsfjord (64°N, 51°W) SW Greenland, through a combination of fieldwork and laboratory experiments. Krill biomass was highest in the middle fjord and inner fjord, whereas no krill was found offshore. The dominating species Thysanoessa raschii revealed a type III functional response when fed with the diatom Thalassiosira weissflogii. At food saturation, T. raschii exhibited a daily ration of 1% body C/d. Furthermore, T. raschii was capable of exploiting plankton cells from 5 to 400 µm, covering several trophic levels of the pelagic food web. The calculated grazing impact by T. raschii on the fjord plankton community was negligible. However, the schooling and migratory behaviour of krill will concentrate and elevate the grazing in specific areas of the euphotic zone.

Stomach content of ringed seals (Pusa hispida) obtained from the Northeast Greenland area

The diet of ringed seals (Pusa hispida) from coastal and offshore areas of Northeast Greenland was determined by identifying, to the lowest taxonomic limit possible, all hard-part contents from the gastrointestinal tract of 51 seals sampled (2002-2004) in spring (April to June, N = 35) and autumn (September to October, N = 16). The autumn diet was characterized by high numbers of Parathemisto libellula, and the spring diet was comprised primarily of polar cod (Boreogadus saida), with few invertebrates consumed. The coastal seal diet samples had a diverse fish prey composition (during both the spring and autumn), whereas the open water seals had eaten mostly crustaceans with P. libellula being most abundant. The sample sizes from the various locations and seasons were not large enough to explore age-class effects on diet in addition. Similar to earlier studies, this study suggests that the ringed seal is a generalist that exploits prey based on availability, with a few key species dominating the diet in an area at least on a seasonal basis.