Influence of the trophic environment and individual metabolism on the dynamics of stable isotopes in the Pacific oyster (Crassostrea gigas): modeling and experimental approaches

Emmery, A., 2012 Influence of the trophic environment and metabolism on the dynamics of stable isotopes in the Pacific oyster (Crassostrea gigas): modeling and experimental approaches.
PhD-thesis, Cean University and VU-University Amsterdam, to appear.


The general aim of this doctorate work was to understand how the trophic environment, i.e. amount and diversity of food, and the metabolism influence the dynamics of stable isotopes 13C and 15N in the tissues of the Pacific oyster (Crassostrea gigas). I combined both experimental (under natural and controlled conditions) and dynamic energy budget modelling (DEB) approaches to decipher the role of oyster metabolism and trophic resource relatively to stable isotopes discrimination.

Trophic resource is frequently characterized thanks to stable isotopic ratios, i.e. delta-13C and delta-15N. Natural stable isotopes are forms of the same element that differ in the number of neutrons in the nucleus. Isotopes with extra neutron are qualified as `heavy isotopes'. The delta notation (promille) stands for the difference in the ratio of heavy isotopes over the light ones relative to a standard. The enrichment in heavy isotopes of a predator relative to its prey is classically called the trophic fractionation (i.e. Delta = delta_predator - delta_consumer, promille). At first approximation, Delta has been frequently considered constant across trophic levels, with an average enrichment of about 1% and 3.4% for Delta-13C and Delta-15N respectively. However, the increasing bulk of results from experimental and modelling approaches shown that Delta depends on numerous environmental (e.g. diversity and quality of food source(s)) and physiological (e.g. growth) factors.

In the first part of this doctorate work (chapter 2), I carried out an in situ survey of oysters growth and isotopic composition (delta-13C and delta-15N) over one year in two different ecosystems, the Bay of Veys (BDV) and the Brest Harbor (BH). The BDV was characterized by an higher amount of food and a higher diversity of food source(s) compared to BH. I expected that the amount of food was the main factor accounting for the spatial differences in stable isotopic composition of oysters. In BDV, oysters exhibited higher growth and CN ratios for both whole soft body tissues (Wd) and organs (gills, Gi, muscle adductor, Mu, and remaining tissues, Re). However, the isotopic ratios of the whole soft body tissues (delta-Wd ) exhibited opposite patterns between the two sites with, on average, a higher delta-13C_Wd and a lower delta-15N_Wd in BH compared to BDV. The interplay of both growth and temporal variations of the trophic resource certainly accounted for these spatial differences in delta_Wd. The dynamics of stable isotopes in organs were similar, i.e. with delta_Mu > delta_Gi > delta_Re regardless of the studied area and season. I thus concluded that the metabolism and the temporal variations of the trophic resource (amount and diversity) had to be considered together to explain the stable isotopes trajectories. However, I could not quantify the impact of metabolism on the dynamics of stable isotopes yet. I thus concluded on the necessity to select an appropriate bioenergetic model i) to understand how oysters discriminate stable isotopes of their food sourcesand ii) to consider the variations of Delta values according to both environmental and physiological factors.

The theoretical study I carried out in the chapter 3 allowed me to better understand how both the amount of food consumed and the metabolism impacted the dynamics of delta-13C_Wd and delta-15N_Wd in the soft tissues of C. gigas. I used a dynamic energy budget model (DEB) combined with a dynamic isotope budget model (DIB) (i.e. from the DEB theory Kooijman, 2010), calibrated and parametrized thanks to data from literature. Based on physical and chemical rules, the DEB model quantifies the state of the individual under varying food and temperature regimes. It delineates catabolic and anabolic aspects of assimilation, maintenance and growth. It makes explicit use of balances of the chemical elements C, H, O and N, as well as the mixing and fractionation of stable isotopes. The results demonstrate that the higher the feeding level, the lower delta_ Wd and Delta_Wd. The mass effect on delta_Wd was not sufficient to explain trophic enrichment classically observed in field. The separation of anabolic and catabolic pathways is key to fractionation. Moreover, the Delta values are dynamically calculated by the IsoDEB model (DEB and DIB models) according to both environmental and metabolism effect.

To test consistency of the model's predictions, I carried out a fractionation experiment under controlled conditions (chapter 4). First, the oysters spat was fed at two different feeding levels (high food, HF; low food, LF) with a single type of food depleted in 13C and 15N, and then starved. The oysters reared at HF level had i) an higher growth and C/N ratios and ii) lower delta-13C_Wd and delta-15N_Wd compared to those reared at LF. The same pattern also occurred for Gi, Mu and Re. As observed during the in situ monitoring, delta_Mu was heavier than delta_Gi and delta_Re regardless of the feeding level. The differences between delta-13C_WdHF and delta-13C_WdLF were more important compared to the trends simulated by the model (chapter 3). The comparison with literature results led me conclude on a potential effect of the diet isotopic ratios (delta_X) on the Delta value. During the starvation the whole soft body tissues and organs were enriched in heavy isotopes. This enrichment was due to the maintenance of the body. Experimental results also revealed that diet isotopic ratios can exhibited strong temporal variations with consequences on Delta values. The next step was thus to apply the model under varying conditions of food.

To this end, the set of parameters for the DEB model has been improved by using a wide variety of data i) to characterize the full life cycle of C. gigas from birth to adult stage (including development acceleration process and metamorphosis) and ii) to take into account the large physiological plasticity of this species. With a single set of parameters, the model successfully fitted all the data for the di erent life stages (embryo, juvenile, adult). Based on this set of parameters, the effect of the ingestion rate on the growth and delta_Wd was successfully described by the IsoDEB model. During the starvation phase, the model also correctly described the enrichment in heavy isotopes due to the maintenance of the body. However, model simulations were less accurate during strong variations of delta_X for both carbon and nitrogen isotopes. This deviation might link to an inaccurate estimation of the elemental composition of reserve and structure. It might also be that fast changes can only be captured accurately with much more complex models.

According to the results of this doctorate work, both the metabolism and the amount of the trophic resource influence the dynamics of stable isotopes in the soft tissues of the Pacific oyster C. gigas. The results also revealed that an accurate quantification of the metabolism (from a modelling point of view) is of primary importance to accurately describe the dynamics of delta-13C_Wd and delta-15N_Wd. The consideration of the (temporal) fluctuations of the environment (food quantity, temperature, diet isotopic ratios) by the IsoDEB model also considerably helped to understand variations of the trophic fractionation. The DEB theory constitutes a promising and innovating ecophysiological tool to understand stable isotope trajectories among living organisms. However, I did not investigate yet the effect of the diversity of the trophic resource on growth and its consequences on the dynamics of stable isotopes in oyster tissues. The coupling of DEB modelling with e.g. mixing models could be the next step.

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