Crustacean zooplankton provide the energetic link between phytoplankton and higher trophic levels in the ocean, including economically important fish species. They also affect biogeochemical cycling through production of fast sinking fecal pellets and the regeneration of nutrients. Historically, marine food-web models have assumed that zooplankton productivity is energy limited, and that productivity therefore scales directly with abundance of food in the environment. However, comparisons of the iron contents of phytoplankton and zooplankton, stoichiometric modeling and preliminary experiments all suggest that in iron-limited regions of the ocean zooplankton growth and reproduction may be limited by the supply of iron via the diet. This project will address three questions regarding the response of copepods to food containing different ratios of Fe:C. First, how the assimilation and retention of iron varies with the Fe:C ratio in food will be determined. The critical threshold Fe:C ratio in food at which copepod production is limited by iron depends on the assimilation of iron and carbon from food, retention of assimilated iron and carbon within copepod tissues and the elemental composition of copepod tissues. Under controlled conditions in the laboratory both pulse chase radioisotope experiments and stable elemental analysis will determine how these variables change with Fe:C in the diet. Second, demographic consequences of variation in Fe:C ratios in food will be assessed. Third, it will be determined whether iron limitation affects copepods indirectly by influencing other aspects of food quality. By selectively supplementing the diet of the copepods and by comparing responses to different algal species the investigators will isolate the characteristic of algal food that correlates most closely with copepod production. In all aspects of the work, a diverse set of phytoplankton will be used as composition and responses to iron limitation vary substantially among major groups. The copepod employed in these experiments will be a cultured coastal calanoid copepod, Acartia tonsa. The ability to culture this organism will allow the investigators to conduct experiments throughout the year without worrying about genotypic variability. In addition they will use copepods species collected from the California Coast which actually experience iron limitation somewhere in their range.
By building a fuller understanding of the factors controlling secondary production in the ocean, this research will be of use to fisheries scientists and managers. It will also inform policy regarding potential economic impacts of climate change and the ecological and biogeochemical consequences of anthropogenic ocean iron fertilization. A graduate and an undergraduate will be funded directly through this proposal, and more undergraduates will be involved directly in the research through alternate funding sources. The investigators will also build upon past associations with local high schools, including one with a predominantly Latino and African American student body, to involve secondary level students directly in the research. Finally, they will partner with the Center for Science and Mathematical Education at Stony Brook to engage in teacher training in global change issues and to produce and test teaching materials related to marine ecology and biogeochemistry.
We determined whether growth and reproduction of copepods, small crustaceans that support many marine fisheries, could be affected by the iron content of their food. Most fisheries models presume that growth of copepods is limited by the overall availability of their algal food, and the energy stored therein. However, in the 30-40% of the ocean in which algal growth is limited by the availability of iron, the iron content of copepod food is typically less than observed in zooplankton (Fig. 1). This mismatch raises the possibility that the growth and reproduction of copepods could be limited not simply by the amount of their food, but also by its iron content. If true, this would make food webs in regions of the ocean where algae are iron limited less efficient at converting algal biomass into fish biomass. We showed in laboratory experiments that the common estuarine copepod, Acartia tonsa, produces fewer eggs (Fig. 2) and exhibits higher larval mortality (Fig. 3) when feeding on algal food depleted in iron. For a range of algal food species, the rate of egg production by A. tonsa varied directly with the rate of iron assimilation and no other measured variable, suggesting that the assimilation of iron was limiting to reproduction in these copepods. When fed diatoms that varied in iron content, A. tonsa exhibited high egg production when iron content of food was above a critical threshold iron content, and a linear relationship with iron content of food below this threshold, again indicating that iron in the diet was the factor limiting egg production. We further showed that A. tonsa is particularly prone to iron limitation because it is not able to compensate for low iron in food by changing ingestion, assimilation or retention of iron or carbon. Both the experimental results and calculations based on physiological rates suggest that copepods must have food with iron content greater than that in their own tissues to reproduce maximally. While A. tonsa is a useful model organism, it is unlikely to experience limitation of reproduction by dietary iron in its native estuarine habitat. We therefore repeated some of these experiments with a common copepod species, Calanus pacificus, which is sometimes exposed to iron-limited algae in its native habitat off the California coast. As with A. tonsa, this species exhibited lower egg production when fed iron-depleted diatom food than when fed iron-replete food (Fig. 2). This effect was reversible; copepods previously exposed to iron-depleted food resumed producing eggs at normal rates when fed iron-replete food. As with A. tonsa, we observed no increase in ingestion rates and fecal pellet production when these organisms were fed food depleted in iron. We also tried to gather further evidence for effects of trace metal limitation of zooplankton production in nature by sampling the Costa Rica Dome, a regions in which phytoplankton are putatively limited by iron and zinc during some seasons of the year. We found that iron contents of food particles (algae and protozoans) were on average lower than measured in many zooplankton size fractions, suggesting that iron limitation of crustacean zooplankton was possible (Fig 4). Indeed, RNA:DNA ratios of zooplankton were low compared to those measured in other regions of the ocean, suggesting low growth rate (Fig. 5). However, a strong correlation between iron, titanium and aluminum in the small zooplankton also suggested that these organisms are ingesting at least some terrestrial iron, possibly by ingesting colloids containing iron oxides. Zinc concentrations in food were low compared to literature values, but generally not low enough to imply limitation of zooplankton by dietary zinc (Fig. 4). However, zinc concentrations increased noticeably with size of zooplankton, suggesting that these larger organisms may be more subject to zinc limitation, especially if they are herbivorous (Fig 6). We have also recently sampled the California current system which in some places exhibits low iron conditions during the summer upwelling season. These data will include trace metal concentrations of individual zooplankton taxa so as to assess intersepcific variation in zooplankton requirments. We expect this work will address broader impacts by contributing to the management of fisheries. Our results suggest a need to assess whether the ratio of phytoplankton production to fisheries production is reduced in iron limited regions of the ocean. Moreover, our results should provide a rational for development of fisheries models that take account of mineral limitation generally. On the educational front, this project supported the training of one graduate student, two high school students (one of which is a coauthor on a paper in Nature Geosciences) and several undergraduates (one of which is now a master student). Finally, we have begun development of active learning curricula concerning topics in oceanography, ecology and climate change that will be available to teachers training in our science and engineering education program at Stony Brook.
