Characteristics of digestive enzymes of calanoid copepod species from different latitudes in relation to temperature, pH and food

In calanoid copepods it is poorly understood how enzymatic activities and patterns are affected by abiotic and biotic factors. Such knowledge, however, is crucial to assess metabolic functioning and performance of organisms in different habitats. Therefore, our study focuses on digestive enzyme activities in relation to temperature, pH and food in the Arctic species Calanus glacialis and in Centropages hamatus and Temora longicornis from the North Sea. Enzyme activities were measured over a range from 0 to 70 °C (lipases/esterases, proteinases) and pH 5 to 9 (proteinases). In all species, relative proteinases activity peaked at 40/50 °C and pH 6; relative lipases/esterases activity peaked at 30 °C. Between 0 and 20 °C, lipase activity of C. glacialis was higher (40-70% of maximum) than that of the boreal copepods (25-64%), which suggests thermal adaptation of the lipid metabolism in the polar species. Incubating C. glacialis with the diatom Thalassiosira weissflogii showed (i) that enzyme activities increased especially in the alkaline range and (ii) that enzyme patterns, revealed by gel electrophoresis, differed from that of starving individuals, indicating that feeding induced enzyme expression. Such studies, linking abiotic and biotic conditions to enzyme functioning, can help elucidating the capacity of copepods to respond to environmental changes.

Energetic plasticity underlies a variable response to ocean acidification in the pteropod, Limacina helicina antarctica

Ocean acidification, caused by elevated seawater carbon dioxide levels, may have a deleterious impact on energetic processes in animals. Here we show that high PCO₂ can suppress metabolism, measured as oxygen consumption, in the pteropod, L. helicina forma antarctica, by ~20%. The rates measured at 180–380 µatm (MO₂ = 1.25 M^−0.25, p = 0.007) were significantly higher (ANCOVA, p = 0.004) than those measured at elevated target CO₂ levels in 2007 (789–1000 µatm, = 0.78 M^−0.32, p = 0.0008;). However, we further demonstrate metabolic plasticity in response to regional phytoplankton concentration and that the response to CO₂ is dependent on the baseline level of metabolism. We hypothesize that reduced regional Chl a levels in 2008 suppressed metabolism and masked the effect of ocean acidification. This effect of food limitation was not, we postulate, merely a result of gut clearance and specific dynamic action, but rather represents a sustained metabolic response to regional conditions. Thus, pteropod populations may be compromised by climate change, both directly via CO₂-induced metabolic suppression, and indirectly via quantitative and qualitative changes to the phytoplankton community. Without the context provided by long-term observations (four seasons) and a multi-faceted laboratory analysis of the parameters affecting energetics, the complex response of polar pteropods to ocean acidification may be masked or misinterpreted.

Ocean acidification induces multi-generational decline in copepod naupliar production with possible conflict for reproductive resource allocation

Climate change, including ocean acidification (OA), presents fundamental challenges to marine biodiversity and sustained ecosystem health. We determined reproductive response (measured as naupliar production), cuticle composition and stage specific growth of the copepod Tisbe battagliai over three generations at four pH conditions (pH 7.67, 7.82, 7.95, and 8.06). Naupliar production increased significantly at pH 7.95 compared with pH 8.06 followed by a decline at pH 7.82. Naupliar production at pH 7.67 was higher than pH 7.82. We attribute the increase at pH 7.95 to an initial stress response which was succeeded by a hormesis-like response at pH 7.67. A multi-generational modelling approach predicted a gradual decline in naupliar production over the next 100 years (equivalent to approximately 2430 generations). There was a significant growth reduction (mean length integrated across developmental stage) relative to controls. There was a significant increase in the proportion of carbon relative to oxygen within the cuticle as seawater pH decreased. Changes in growth, cuticle composition and naupliar production strongly suggest that copepods subjected to OA-induced stress preferentially reallocate resources towards maintaining reproductive output at the expense of somatic growth and cuticle composition. These responses may drive shifts in life history strategies that favour smaller brood sizes, females and perhaps later maturing females, with the potential to profoundly destabilise marine trophodynamics.

Ocean acidification-induced food quality deterioration constrains trophic transfer

Our present understanding of ocean acidification (OA) impacts on marine organisms caused by rapidly rising atmospheric carbon dioxide (CO2) concentration is almost entirely limited to single species responses. OA consequences for food web interactions are, however, still unknown. Indirect OA effects can be expected for consumers by changing the nutritional quality of their prey. We used a laboratory experiment to test potential OA effects on algal fatty acid (FA) composition and resulting copepod growth. We show that elevated CO2 significantly changed the FA concentration and composition of the diatom Thalassiosira pseudonana, which constrained growth and reproduction of the copepod Acartia tonsa. A significant decline in both total FAs (28.1 to 17.4 fg cell−1) and the ratio of long-chain polyunsaturated to saturated fatty acids (PUFA:SFA) of food algae cultured under elevated (750 µatm) compared to present day (380 µatm) pCO2 was directly translated to copepods. The proportion of total essential FAs declined almost tenfold in copepods and the contribution of saturated fatty acids (SFAs) tripled at high CO2. This rapid and reversible CO2-dependent shift in FA concentration and composition caused a decrease in both copepod somatic growth and egg production from 34 to 5 eggs female−1 day−1. Because the diatom-copepod link supports some of the most productive ecosystems in the world, our study demonstrates that OA can have far-reaching consequences for ocean food webs by changing the nutritional quality of essential macromolecules in primary producers that cascade up the food web.

A marine secondary producer respires and feeds more in a high CO2 ocean

Climate change mediates marine chemical and physical environments and therefore influences marine organisms. While increasing atmospheric CO₂ level and associated ocean acidification has been predicted to stimulate marine primary productivity and may affect community structure, the processes that impact food chain and biological CO₂ pump are less documented. We hypothesized that copepods, as the secondary marine producer, may respond to future changes in seawater carbonate chemistry associated with ocean acidification due to increasing atmospheric CO₂ concentration. Here, we show that the copepod, Centropages tenuiremis, was able to perceive the chemical changes in seawater induced under elevated CO₂ concentration (>1700 μatm, pH < 7.60) with avoidance strategy. The copepod’s respiration increased at the elevated CO₂ (1000 μatm), associated acidity (pH 7.83) and its feeding rates also increased correspondingly, except for the initial acclimating period, when it fed less. Our results imply that marine secondary producers increase their respiration and feeding rate in response to ocean acidification to balance the energy cost against increased acidity and CO₂ concentration.

Description and quantification of pteropod shell dissolution: A sensitive bioindicator of ocean acidification

Anthropogenic ocean acidification is likely to have negative effects on marine calcifying organisms, such as shelled pteropods, by promoting dissolution of aragonite shells. Study of shell dissolution requires an accurate and sensitive method for assessing shell damage. Shell dissolution was induced through incubations in CO₂ enriched seawater for between 4 and 14 days. We describe a procedure that allows the level of dissolution to be assessed and classified into three main types: Type I with partial dissolution of the prismatic layer; Type II with exposure of underlying crossed-lamellar layer, and Type III, where crossed-lamellar layer shows signs of dissolution. Levels of dissolution showed a good correspondence to the incubation conditions, with the most severe damage found in specimens held for 14 d in undersaturated condition (Ω ~ 0.8). This methodology enables the response of small pelagic calcifiers to acidified conditions to be detected at an early stage, thus making pteropods a valuable bioindicator of future ocean acidification.

Biochemical responses of the copepod Centropages tenuiremis to CO2-driven acidified seawater

An ecophysiological experiment was conducted to examine the biochemical effects of acidified seawater containing elevated concentration of CO₂ (C_CO2 0.08, 0.20, 0.50 and 1.00%) on the copepod Centropages tenuiremis. AchE, ATPase, SOD, GPx, GST, GSH level and GSH/GSSG ratio of the copepod were analyzed. The results showed that elevated C_CO2 and the duration of culture time significantly influenced several biochemical indices in C. tenuiremis (ATPase, GPx, GST, GSH and SOD). Furthermore, the principal component analysis results indicated that 72.32% of the overall variance was explained by the first three principal components (GPx, SOD and GSH). Changes in GPx and GSH levels may play a significant role in the antioxidant defense of copepods against seawater acidification. The long-term response of copepods to seawater acidification and the synergistic effects of acidification with other environmental factors, such as temperature, salinity and trace metal need further investigation.

End of century ocean warming and acidification effects on reproductive success in a temperate marine copepod

We examined how predicted end of century ocean warming and acidification scenarios affected the incidence of apoptosis in the eggs and nauplii of the copepod Calanus helgolandicus. Offspring viability was not affected by 1000 ppm CO₂-acidified seawater, whereas the effects of 2 and 4°C warming were dependent upon the batch of eggs used; warming increased viability in the second batch. This context-dependency highlights the need for cautious interpretation and application of data from individual climate-change studies.

Pteropods from the Caribbean Sea: variations in calcification as an indicator of past ocean carbonate saturation (update)

The aragonite shell-bearing thecosome pteropods are an important component of the oceanic plankton. However, with increasing pCO₂ and the associated reduction in oceanic pH (ocean acidification), thecosome pteropods are thought to be particularly vulnerable to shell dissolution. The distribution and preservation of pteropods over the last 250 000 years have been investigated in marine sediment cores from the Caribbean Sea close to the island of Montserrat. Using the Limacina Dissolution Index (LDX), fluctuations in pteropod calcification through the most recent glacial/interglacial cycles are documented. By comparison to the oxygen isotope record (global ice volume), we show that pteropod calcification is closely linked to global changes in pCO₂ and pH and is, therefore, a global signal. These data are in agreement with the findings of experiments upon living pteropods, which show that variations in pH can greatly affect aragonitic shells. The results of this study provide information which may be useful in the prediction of future changes to the pteropod assemblage caused by ocean acidification.

Impacts of CO2-driven seawater acidification on survival, egg production rate and hatching success of four marine copepods

Ecological experiments were conducted to examine the effects of seawater containing elevated partial pressure of carbon dioxide (pCO2 800×10⁻⁶, 2 000×10⁻⁶, 5 000×10⁻⁶ and 10 000×10⁻⁶) on the survival and reproduction of female Acartia pacifica, Acartia spinicauda, Calanus sinicus and Centropages tenuiremis, which are the dominant copepods in the southern coastal waters of China. The results show that the effects of elevated pCO2 on the survival rates of copepods were speciesspecific. C. sinicus, which was a macro-copepod, had a higher survival rate (62.01%–71.96%) than the other three species (5.00%–26.67%) during the eight day exposure. The egg production rates of C. sinicus, A. spinicauda and C. tenuiremis were significantly inhibited by the increased pCO₂ and the exposure time duration. There were significantly negative impacts on the egg hatching success of A. spinicauda and C. tenuiremis in the pCO2 2 000×10⁻⁶ and 10 000×10⁻⁶ groups, and, in addition, the exposure time had noticeably impacts on these rates too. This study indicates that the reproductive performances of copepods were sensitive to elevated pCO2, and that the response of different copepod species to acidified seawater was different. Furthermore, the synergistic effects of seawater acidification and climate change or other pollutant stresses on organisms should be given more attention.