Direct and indirect effects of elevated CO2 are revealed through shifts in phytoplankton, copepod development, and fatty acid accumulation.

Change in the nutritional quality of phytoplankton is a key mechanism through which ocean acidification can affect the function of marine ecosystems. Copepods play an important role transferring energy from phytoplankton to higher trophic levels, including fatty acids (FA)-essential macronutrients synthesized by primary producers that can limit zooplankton and fisheries production. We investigated the direct effects of pCO2 on phytoplankton and copepods in the laboratory, as well as the trophic transfer of effects of pCO2 on food quality. The marine cryptophyte Rhodomonas salina was cultured at 400, 800, and 1200 µatm pCO2 and fed to adult Acartia hudsonica acclimated to the same pCO2 levels. We examined changes in phytoplankton growth rate, cell size, carbon content, and FA content, and copepod FA content, grazing, respiration, egg production, hatching, and naupliar development. This single-factor experiment was repeated at 12°C and at 17°C. At 17°C, the FA content of R. salina responded non-linearly to elevated pCO2 with the greatest FA content at intermediate levels, which was mirrored in A. hudsonica; however, differences in ingestion rate indicate that copepods accumulated FA less efficiently at elevated pCO2. A. hudsonica nauplii developed faster at elevated pCO2 at 12°C in the absence of strong food quality effects, but not at 17°C when food quality varied among treatments. Our results demonstrate that changes to the nutritional quality of phytoplankton are not directly translated to their grazers, and that studies that include trophic links are key to unraveling how ocean acidification will drive changes in marine food webs.

Temperature-driven changes in the diet preference of omnivorous copepods: no more meat when it's hot? A response to Winder et al.

The study of environmental impact on feeding preferences of omnivores is a rapidly growing field. Here, we show that the criticism put forward in a comment on our original study is largely unfounded.

Temperature driven changes in the diet preference of omnivorous copepods: no more meat when it's hot?

Herbivory is more prevalent in the tropics than at higher latitudes. If differences in ambient temperature are the direct cause for this phenomenon, then the same pattern should be visible in a seasonal gradient, as well as in experiments manipulating temperature. Using (15)N stable isotope analyses of natural populations of the copepod Temora longicornis we indeed observed seasonal differences in the trophic level of the copepod and a decrease in trophic level with increasing temperature. In a grazing experiment, with a mixed diet of the cryptophyte Rhodomonas salina and the heterotrophic dinoflagellate Oxyrrhis marina, T. longicornis preferred the cryptophyte at higher temperatures, whereas at lower temperatures it preferred the non-autotrophic prey. We explain these results by the higher relative carbon content of primary producers compared to consumers, in combination with the higher demand for metabolic carbon at higher temperatures. Thus, currently increasing temperatures may cause changes in dietary preferences of many consumers.

The reaction of European lobster larvae (Homarus gammarus) to different quality food: effects of ontogenetic shifts and pre-feeding history.

Young larval stages of many organisms represent bottlenecks in the life-history of many species. The high mortality commonly observed in, for example, decapod larvae has often been linked to poor nutrition, with most studies focussing on food quantity. Here, we focus instead on the effects of quality and have investigated its effects on the nutritional condition of lobster larvae. We established a tri-trophic food chain consisting of the cryptophyte Rhodomonas salina, the calanoid copepod Acartia tonsa and larvae of the European lobster Homarus gammarus. In a set of experiments, we manipulated the C:N:P stoichiometry of the primary producers, and accordingly those of the primary consumer. In a first experiment, R. salina was grown under N- and P-limitation and the nutrient content of the algae was manipulated by addition of the limiting nutrient to create a food quality gradient. In a second experiment, the effect on lobster larvae of long- and short-term exposure to food of varying quality during ontogenetic development was investigated. The condition of the lobster larvae was negatively affected even by subtle N- and P-nutrient limitations of the algae. Furthermore, younger lobster larvae were more vulnerable to nutrient limitation than older ones, suggesting an ontogenetic shift in the capacity of lobster larvae to cope with low quality food. The results presented here might have substantial consequences for the survival of lobster larvae in the field, as, in the light of future climate change and re-oligotrophication of the North Sea, lobster larvae might face marked changes in temperature and nutrient conditions, thus significantly altering their condition and growth.

Food quality affects secondary consumers even at low quantities: an experimental test with larval European lobster.

The issues of food quality and food quantity are crucial for trophic interactions. Although most research has focussed on the primary producer-herbivore link, recent studies have shown that quality effects at the bottom of the food web propagate to higher trophic levels. Negative effects of poor food quality have almost exclusively been demonstrated at higher food quantities. Whether these negative effects have the same impact at low food availability in situations where the majority if not all of the resources are channelled into routine metabolism, is under debate. In this study a tri-trophic food chain was designed, consisting of the algae Rhodomonas salina, the copepod Acartia tonsa and freshly hatched larvae of the European lobster Homarus gammarus. The lobster larvae were presented with food of two different qualities (C:P ratios) and four different quantities to investigate the combined effects of food quality and quantity. Our results show that the quality of food has an impact on the condition of lobster larvae even at very low food quantities. Food with a lower C:P content resulted in higher condition of the lobster larvae regardless of the quantity of food. These interacting effects of food quality and food quantity can have far reaching consequences for ecosystem productivity.

Differential effects of nutrient-limited primary production on primary, secondary or tertiary consumers.

Nutritional imbalances between predator and prey are the rule rather than the exception at the lower end of food webs. We investigated the role of different grazers in the propagation of nutritionally imbalanced primary production by using the same primary producers in a three-trophic-level food chain and a four-trophic-level food chain experimental setup. The three-trophic-level food chain consisted of a classic single-cell primary producer (Rhodomonas salina), a metazoan grazer (the copepod Acartia tonsa) and a top predator (the jellyfish Gonionemus vertens), while we added a protozoan grazer (Oxyrrhis marina) as primary consumer to the food chain to establish the four-trophic-level food chain. This setup allowed us to investigate how nutrient-limitation effects change from one trophic level to another, and to investigate the performance of two components of our experimental food chains in different trophic positions. Stoichiometry and fatty acid profiles of the algae showed significant differences between the nutrient-depleted [no N and no P addition (-P), respectively] and the nutrient-replete (f/2) treatments. The differences in stoichiometry could be traced when O. marina was the first consumer. Copepods feeding on these flagellates were not affected by the nutritional imbalance of their prey in their stoichiometry, their respiration rates nor in their developmental rates. In contrast, when copepods were the primary consumer, those reared on the -P algae showed significantly higher respiration rates along with significantly lower developmental rates. In neither of our two experimental food chains did the signals from the base of the food chains travel up to jelly fish, our top predator.