Julien Thébault

Is the meiofauna a good indicator for climate change and anthropogenic impacts

Our planet is changing, and one of the most pressing challenges facing the scientific community revolves around understanding how ecological communities respond to global changes. From coastal to deep-sea ecosystems, ecologists are exploring new areas of research to find model organisms that help predict the future of life on our planet. Among the different categories of organisms, meiofauna offer several advantages for the study of marine benthic ecosystems. This paper reviews the advances in the study of meiofauna with regard to climate change and anthropogenic impacts. Four taxonomic groups are valuable for predicting global changes: foraminifers (especially calcareous forms), nematodes, copepods and ostracods. Environmental variables are fundamental in the interpretation of meiofaunal patterns and multistressor experiments are more informative than single stressor ones, revealing complex ecological and biological interactions. Global change has a general negative effect on meiofauna, with important consequences on benthic food webs. However, some meiofaunal species can be favoured by the extreme conditions induced by global change, as they can exhibit remarkable physiological adaptations. This review highlights the need to incorporate studies on taxonomy, genetics and function of meiofaunal taxa into global change impact research.

Variation in Size and Growth of the Great Scallop Pecten maximus along a Latitudinal Gradient

Understanding the relationship between growth and temperature will aid in the evaluation of thermal stress and threats to ectotherms in the context of anticipated climate changes. Most Pecten maximus scallops living at high latitudes in the northern hemisphere have a larger maximum body size than individuals further south, a common pattern among many ectotherms. We investigated differences in daily shell growth among scallop populations along the Northeast Atlantic coast from Spain to Norway. This study design allowed us to address precisely whether the asymptotic size observed along a latitudinal gradient, mainly defined by a temperature gradient, results from differences in annual or daily growth rates, or a difference in the length of the growing season. We found that low annual growth rates in northern populations are not due to low daily growth values, but to the smaller number of days available each year to achieve growth compared to the south. We documented a decrease in the annual number of growth days with age regardless of latitude. However, despite initially lower annual growth performances in terms of growing season length and growth rate, differences in asymptotic size as a function of latitude resulted from persistent annual growth performances in the north and sharp declines in the south. Our measurements of daily growth rates throughout life in a long-lived ectothermic species provide new insight into spatio-temporal variations in growth dynamics and growing season length that cannot be accounted for by classical growth models that only address asymptotic size and annual growth rate.

Primary Production and Carrying Capacity of Former Salt Ponds After Reconnection to San Francisco Bay

Over 6,110 ha of the commercial production salt ponds surrounding South San Francisco Bay, CA, have been decommissioned and reconnected to the bay, most as part of the largest wetlands restoration program in the western United States. These open water ponds are critical habitat for millions of birds annually and restoration program managers must determine the appropriate balance between retention of ponds versus re-conversion to tidal salt marsh, knowing that both are essential ecosystems for endangered bird species. Our study describes the ecological value of the new open water pond ecosystems as feeding habitats for birds. We used the oxygen rate of change method to determine ecosystem metabolic parameters from high resolution time-series of dissolved oxygen concentration. Areal gross primary production (8.17 g O2 m−2 d−1) was roughly double the world’s most productive estuaries. High rates of phytoplankton photosynthesis were balanced by equally high rates of community respiration (8.25 g O2 m−2 d−1). Metabolic equilibrium was delicately poised: sharp irradiance and temperature shifts triggered short term photosynthesis reduction resulting in oxygen depletion. We converted net primary production (NPP) into potential carrying capacity of the forage biota that support targeted pond waterbirds. NPP was processed through both a pelagic food web, resulting in forage biota for piscivorous birds and a benthic food web, resulting in forage biota for shorebirds and diving benthivores. Both food webs included efficient algal-based and inefficient detrital trophic pathways. The result of all primary production being routed through simple food webs was high potential forage production and energy supply to waterbirds, equivalent to 11–163 million planktivorous fish or 19–78 billion small estuarine clams within the 330-ha pond between May and October. Food quantity does not necessarily equal quality and these systems have the potential to produce toxic or inedible algae. Our study provides the first measurement of primary production in the open water ponds of San Francisco Bay and presents a novel approach for transforming primary production into forage production as a metric of an ecosystem’s energetic carrying capacity.

Specific pathways for the incorporation of dissolved barium and molybdenum into the bivalve shell: An isotopic tracer approach in the juvenile Great Scallop (Pecten maximus)

Dissolved barium and molybdenum incorporation in the calcite shell was investigated in the Great Scallop Pecten maximus. Sixty six individuals were exposed for 16 days to two successive dissolved Ba and Mo concentrations accurately differentiated by two different isotopic enrichments (⁹⁷Mo, ⁹⁵Mo; ¹³⁵Ba, ¹³⁷Ba). Soft tissue and shell isotopic composition were determined respectively by quantitative ICP-MS (Inductively Coupled Plasma Mass Spectrometer) and laser ablation--ICP-MS. Results from Ba enrichment indicate the direct incorporation of dissolved Ba into the shell in proportion to the levels in the water in which they grew with a 6-8 day delay. The low spike contributions and the low partition coefficient (D(Mo) = 0.0049 ± 0.0013), show that neither the soft tissue nor the shell were significantly sensitive to Mo enrichment. These results eliminate direct Mo shell enrichment by the dissolved phase, and favour a trophic uptake that will be investigated using the successive isotopic enrichment approach developed in this study.

Responses of Two Scleractinian Corals to Cobalt Pollution and Ocean Acidification

The effects of ocean acidification alone or in combination with warming on coral metabolism have been extensively investigated, whereas none of these studies consider that most coral reefs near shore are already impacted by other natural anthropogenic inputs such as metal pollution. It is likely that projected ocean acidification levels will aggravate coral reef health. We first investigated how ocean acidification interacts with one near shore locally abundant metal on the physiology of two major reef-building corals: Stylophora pistillata and Acropora muricata. Two pH levels (pHT 8.02; pCO2 366 μatm and pHT 7.75; pCO2 1140 μatm) and two cobalt concentrations (natural, 0.03 μg L-1 and polluted, 0.2 μg L-1) were tested during five weeks in aquaria. We found that, for both species, cobalt input decreased significantly their growth rates by 28% while it stimulated their photosystem II, with higher values of rETRmax (relative Electron Transport Rate). Elevated pCO2 levels acted differently on the coral rETRmax values and did not affect their growth rates. No consistent interaction was found between pCO2 levels and cobalt concentrations. We also measured in situ the effect of higher cobalt concentrations (1.06 ± 0.16 μg L-1) on A. muricata using benthic chamber experiments. At this elevated concentration, cobalt decreased simultaneously coral growth and photosynthetic rates, indicating that the toxic threshold for this pollutant has been reached for both host cells and zooxanthellae. Our results from both aquaria and in situ experiments, suggest that these coral species are not particularly sensitive to high pCO2 conditions but they are to ecologically relevant cobalt concentrations. Our study reveals that some reefs may be yet subjected to deleterious pollution levels, and even if no interaction between pCO2 levels and cobalt concentration has been found, it is likely that coral metabolism will be weakened if they are subjected to additional threats such as temperature increase, other heavy metals, and eutrophication.

Drivers of shell growth of the bivalve, Callista chione (L. 1758) – Combined environmental and biological factors

Seasonal shell growth patterns were analyzed using the stable oxygen and carbon isotope values of live-collected specimens of the bivalve Callista chione from two sites in the Adriatic Sea (Pag and Cetina, Croatia). Micromilling was performed on the shell surface of three shells per site and shell oxygen isotopes of the powder samples were measured. The timing and rate of seasonal shell growth was determined by aligning the δ18Oshell-derived temperatures so that the best fit was achieved with the instrumental temperature curve. According to the data, shells grew only at very low rates or not at all during the winter months, i.e., between January and March. Shell growth slowdown/shutdown temperatures varied among sites, i.e., 13.6 °C at Pag and 16.6 °C at Cetina, indicating that temperature was not the only driver of shell growth. Likely, seasonal differences in seawater temperature and food supply were the major component explaining contrasting growth rates of C. chione at two study sites. Decreasing shell growth rates were also associated with the onset of gametogenesis suggesting a major energy reallocation toward reproduction rather than growth. These results highlight the need to combine sclerochronological analyses with ecological studies to understand life history traits of bivalves as archives of environmental variables.

Influence of riverine input on the growth of Glycymeris glycymeris in the Bay of Brest, North-West France

A crossdated, replicated, chronology of 114 years (1901–2014) was developed from internal growth increments in the shells of Glycymeris glycymeris samples collected monthly from the Bay of Brest, France. Bivalve sampling was undertaken between 2014 and 2015 using a dredge. In total 401 live specimens and 243 articulated paired valves from dead specimens were collected, of which 38 individuals were used to build the chronology. Chronology strength, assessed as the Expressed Population Signal, was above 0.7 throughout, falling below the generally accepted threshold of 0.85 before 1975 because of reduced sample depth. Significant positive correlations were identified between the shell growth and the annual averages of rainfall (1975–2008; r = 0.34) and inflow from the river Elorn (1989–2009; r = 0.60). A significant negative correlation was identified between shell growth and the annual average salinity (1998–2014; r = -0.62). Analysis of the monthly averages indicates that these correlations are associated with the winter months (November–February) preceding the G. glycymeris growth season suggesting that winter conditions predispose the benthic environment for later shell growth. Concentration of suspended particulate matter within the river in February is also positively correlated with shell growth, leading to the conclusion that food availability is also important to the growth of G. glycymeris in the Bay of Brest. With the addition of principle components analysis, we were able to determine that inflow from the River Elorn, nitrite levels and salinity were the fundamental drivers of G. glycymeris growth and that these environmental parameters were all linked.

Transcriptomic responses of the endangered freshwater mussel Margaritifera margaritifera to trace metal contamination in the Dronne River, France

The freshwater pearl mussel Margaritifera margaritifera is one of the most threatened freshwater bivalves worldwide. In this study, we aimed (i) to study the processes by which water quality might affect freshwater mussels in situ and (ii) to provide insights into the ecotoxicological significance of water pollution to natural populations in order to provide necessary information to enhance conservation strategies. M. margaritifera specimens were sampled in two close sites located upstream or downstream from an illegal dumping site. The renal transcriptome of these animals was assembled and gene transcription determined by RNA-seq. Correlations between transcription levels of each single transcript and the bioaccumulation of nine trace metals, age (estimated by sclerochronology), and condition index were determined in order to identify genes likely to respond to a specific factor. Amongst the studied metals, Cr, Zn, Cd, and Ni were the main factors correlated with transcription levels, with effects on translation, apoptosis, immune response, response to stimulus, and transport pathways. However, the main factor explaining changes in gene transcription appeared to be the age of individuals with a negative correlation with the transcription of retrotransposon-related genes. To investigate this effect further, mussels were classified into three age classes. In young, middle-aged and old animals, transcription levels were mainly explained by Cu, Zn and age, respectively. This suggests differences in the molecular responses of this species to metals during its lifetime that must be better assessed in future ecotoxicology studies.

Combined Use of Morphological and Molecular Tools to Resolve Species Mis-Identifications in the Bivalvia The Case of Glycymeris glycymeris and G. pilosa.

Morphological and molecular tools were combined to resolve the misidentification between Glycymeris glycymeris and Glycymeris pilosa from Atlantic and Mediterranean populations. The ambiguous literature on the taxonomic status of these species requires this confirmation as a baseline to studies on their ecology and sclerochronology. We used classical and landmark-based morphometric approaches and performed bivariate and multivariate analyses to test for shell character interactions at the individual and population level. Both approaches generated complementary information. The former showed the shell width to length ratio and the valve asymmetry to be the main discriminant characters between Atlantic and Mediterranean populations. Additionally, the external microsculpture of additional and finer secondary ribs in G. glycymeris discriminates it from G. pilosa. Likewise, landmark-based geometric morphometrics revealed a stronger opisthogyrate beak and prosodetic ligament in G. pilosa than G. glycymeris. Our Bayesian and maximum likelihood phylogenetic analyses based on COI and ITS2 genes identified that G. glycymeris and G. pilosa form two separate monophyletic clades with mean interspecific divergence of 11% and 0.9% for COI and ITS2, respectively. The congruent patterns of morphometric analysis together with mitochondrial and nuclear phylogenetic reconstructions indicated the separation of the two coexisting species. The intraspecific divergence occurred during the Eocene and accelerated during the late Pliocene and Pleistocene. Glycymeris pilosa showed a high level of genetic diversity, appearing as a more robust species whose tolerance of environmental conditions allowed its expansion throughout the Mediterranean.

Bivalve trophic ecology in the Mediterranean: Spatio-temporal variations and feeding behavior

The trophic ecology of two bivalves, the clam Callista chione and the cockle Glycymeris bimaculata was studied using environmental and biochemical variables of the suspended particulate matter and the sediment. Samples were collected from two shallow sites, Pag and Cetina, in the coastal oligotrophic Mediterranean Sea, during a 17 month period. The temporal variation of the particulate matter reflected a mixture between marine and terrestrial sources throughout the year, with a clear marine influence during summer and fall, and predominance of terrestrial inputs during spring and winter. The digestive gland was a useful rapid turnover tissue, where the carbon isotope signal was species-specific and the nitrogen isotope one was site-specific. FA markers in the digestive gland revealed a mixed diet where Callista chione fed more upon fresh material than G. bimaculata which relied largely on bacteria-derived detritus. Overall, little feeding niche overlap was observed between the two species during the year, indicating resource partitioning, expected for a food-limited system. The present trophic ecology study in co-occurring species allowed identifying species-specific feeding adaptations to environmental variability.