Pelagic stocks and carbon and nitrogen uptake in a pearl farming atoll (Ahe, French Polynesia)

Highlights

• Study reports nitrogen uptake and primary production data in a pearl farming lagoon.

• Nitrate and ammonium uptake data suggested a fast turn-over of N-nutrients.

• Regenerated nitrogen provided a large part of phytoplankton nitrogen demand.

• A spatial pattern of nitrogen uptake distribution was evidenced at the lagoon-scale.

• High regeneration conditions favored high nanophytoplankton production.

Abstract

This study reports the first measurements of nitrogen uptake and new data on carbon fixation (¹⁵N/¹³C incorporation) for two size-fractionated phytoplankton (<2 μm and >2 μm), on organic matter, and phytoplankton stocks in Ahe lagoon. Data were collected between November and December 2017, during the hot season with prevailing trade winds. Ammonium and nitrate uptake data (7.58 to 39.81 and 1.80 to 21.43 μmol N m⁻³ h⁻¹, respectively) suggest a rapid turn-over of N-nutrients in the water column and show that primary production was largely sustained by recycled nitrogen providing 68% of the pelagic N demand. These results highlight the spatial heterogeneity of the measured processes linked to the local hydrodynamics, exhibiting higher regenerated production in the more exploited southwestern part of the lagoon and a higher proportion of new production in the north. Intense nutrient recycling appears to promote nanophytoplankton production which is critical for pearl oyster growth.

Introduction

Atoll lagoons are generally highly productive ecosystems compared to the surrounding oligotrophic ocean (Hatcher, 1997). They support fisheries and aquaculture production that can make significant contributions to the economic development of many Pacific island countries. There are 84 atolls in French Polynesia, 77 of which belong to the Tuamotu Archipelago, a highly productive black pearl oyster (Pinctada margaritifera) farming site. Black pearl production currently ranks second only to tourism among the sources of income in French Polynesia. However, over the two past decades, this sector has declined and many farms had to close with major consequences for the local population. This decline has several reasons, including high stocking densities of pearl oysters potentially coupled with environmental changes causing algal blooms and massive mortalities as well as poor management of regional and international trade (Andréfouët et al., 2012). In this context, several research programs were launched to learn more about the biological processes related to pearl oyster farming and possible interactions with the environment (Andréfouët et al., 2012; Gueguen et al., 2016). These programs were to provide appropriate management recommendations and develop models and new tools specifically designed to achieve a sustainable use of atoll resources.

Atoll lagoons are isolated marine ecosystems and their remoteness and poor accessibility often make it difficult to carry out field studies. Modelling can therefore be a cost-effective way to help understand the often complex ecosystem dynamics and assess the importance of the various physico-biogeochemical processes, particularly with regard to the oyster food web (Duarte et al., 2003; Webster and Harris, 2004). In the past decade, several numerical models have been developed and implemented for the Ahe atoll (Tuamotu Archipelago) which hosts an important pearl oyster farming industry. One of those models is a 3D biophysical model based on the MARS3D hydrodynamic model (Dumas et al., 2012), which was extended by adding a larval transport model (Thomas et al., 2014). In parallel, a Dynamic Energy Budget (DEB) model of the larval stage was developed considering the eco-physiology of P. margaritifera (Sangare et al., 2020; Thomas et al., 2011) and coupled with the 3D physical model (Thomas et al., 2016). The coupling of such a DEB model with a physico-biogeochemical model that can simulate the variability of food sources in time and space represents a significant advancement compared to the traditional approach using temporal and spatial interpolations of sparse in situ measurements.

The success of black pearl aquaculture strongly depends on environmental parameters and pelagic food sources that can affect larval development and settlement as well as adult development and reproduction of P. margaritifera (Fournier et al., 2012b; Pouvreau et al., 2000; Thomas et al., 2016). While this species is benthic in the wild, when farmed, it is suspended on vertical lines in water-column and is therefore highly dependent on the availability of plankton for feeding. Thus, while pearl oyster culture negatively affect phytoplankton abundance and primary production through grazing, it may also stimulate phytoplankton development by supplying the water column with nutrients through regeneration (Lacoste and Gaertner-Mazouni, 2016). The development of a new biogeochemical model should therefore consider the pelagic food web and be able to account for the effects of oysters on lower trophic levels such as phytoplankton. This model is currently in its first phase of development for the Ahe lagoon (ECO3M-Atoll model configuration) and uses the environmental and planktonic data collected over 10 years to constrain the model parameters. This dataset includes chlorophyll a (Chla), phytoplankton size structure and composition (Charpy et al., 2012; Thomas et al., 2010), prokaryotic diversity and dynamics (Bouvy et al., 2012; Michotey et al., 2012), zooplankton biomass and composition (Pagano et al., 2012, Pagano et al., 2017) and grazing by oysters (Dupuy et al., 2009; Fournier et al., 2012a), primary production and photosynthetic parameters (Lefebvre et al., 2012), as well as nutrient fluxes at the sediment-water interface or produced in the water column by the cultured pearl oysters and their associated epibionts and biofouling (Lacoste and Gaertner-Mazouni, 2016, and references herein). However, several characteristics of the Ahe lagoon remain less well documented such as the taxonomic composition of nano- and microphytoplankton (Fournier et al., 2012a) and the C, N and P content of organic matter. Finally, no information exists on the in situ N uptake by phytoplankton at Ahe and at the entire Tuamotu Archipelago, with the exception of some preliminary data on N₂ fixation (Charpy-Roubaud et al., 2001). The only information on nitrogen utilization by phytoplankton in Tuamotu atoll lagoons was collected in bioassay experiments to investigate nutrient limitation (Dufour and Berland, 1999; Ferrier-Pagès and Furla, 2001; Sakka et al., 1999), although without discriminating between the different chemical forms of nitrogen.

In November and December 2017, a field campaign was conducted in Ahe lagoon as part of the MANA (MANagement of Atoll) project. The main objectives included the provision of new insights into the ecosystem dynamics and functioning in Ahe lagoon by acquiring new and innovative pelagic data to calibrate a new ecosystem model. Measurements included hydrological parameters, particulate and dissolved matter (C, N, P), chlorophyll, nano- and microphytoplankton taxonomy, and phytoplankton C and N uptake. For the first time, in situ data on nitrogen uptake for two phytoplankton size fractions (<2 μm and >2 μm) could be collected and combined with carbon fixation and other environmental and phytoplankton data. Here, we used the dual ¹⁵N/¹³C isotopic method to measure nitrate, ammonium, and carbon uptake rates and estimate the amount of production that is sustained by new and regenerated nitrogen. In addition to the usual nutrient measurements, these nitrogen uptake data are essential to determine the effective trophic status of the lagoon and to better understand the nitrogen cycling and the ability of planktonic food-webs to sustain intense pearl farming. More generally, these data are useful to improve our understanding of lagoon ecosystem functioning and ecosystem-level effects of pearl farming, and to develop realistic biophysical models.