Pearl Oyster Pinctada Margaritifera Research Articles

Comparison of in situ black-lipped oyster spat collection and larval dispersal modelling results in semi-closed pearl-farming lagoons of the Tuamotu Archipelago

Spat collection of the pearl oyster Pinctada margaritifera in atoll lagoons of French Polynesia is the fundamental sustain of black pearl farming. Spat collection has always yielded variable results in space and time, but obvious signs of steady decreases, even collapses, have emerged in several lagoons. Spat collection materializes the ecological connectivity pathways between wild spawning populations and the location of artificial larval settlement substrates. To assess if oyster larval dispersal modelling could capture such pathways, we compared four six-week long spat collector deployment periods with dispersal simulations in two different lagoons. Spat collectors displayed wide spatial and temporal variations. Numerical modelling and field experiments were generally not in agreement. Although both methods have limitations, they can still approximate each other. But the accuracy of model simulations cannot be ascertained with spat collection data only. Using a SWOT (Strength-Weakness-Opportunities-Threats) analysis, we emphasize the complementarity of both approaches for management decisions.

Comparative transcriptomics identifies genes underlying growth performance of the Pacific black-lipped pearl oyster Pinctada margaritifera

BackgroundIn bivalves, the rate at which organisms grow is a major functional trait underlying many aspects of their commercial production. Growth is a highly polygenic trait, which is typically regulated by many genes with small to moderate effects. Due to its complexity, growth variability in such shellfish remains poorly understood. In this study, we aimed to investigate differential gene expression among spat of the pearl oyster Pinctada margaritifera with distinct growth phenotypes.ResultsWe selected two groups of P. margaritifera spat belonging to the same F2 cohort based on their growth performance at 5.5 months old. Transcriptome profile analysis identified a total of 394 differentially expressed genes between these Fast-growing (F) and Slow-growing (S) phenotypes. According to functional enrichment analysis, S oysters overexpressed genes associated with stress-pathways and regulation of innate immune responses. In contrast, F oysters up-regulated genes associated with cytoskeleton activity, cell proliferation, and apoptosis. Analysis of genome polymorphism identified 16 single nucleotide polymorphisms (SNPs) significantly associated with the growth phenotypes. SNP effect categorization revealed one SNP identified for high effect and annotated for a stop codon gained mutation. Interestingly, this SNP is located within a gene annotated for scavenger receptor class F member 1 (SRF1), which is known to modulate apoptosis. Our analyses also revealed that all F oysters showed up-regulation for this gene and were homozygous for the stop-codon mutation. Conversely, S oysters had a heterozygous genotype and a reduced expression of this gene.ConclusionsAltogether, our findings suggest that differences in growth among the same oyster cohort may be explained by contrasted metabolic allocation between regulatory pathways for growth and the immune system. This study provides a valuable contribution towards our understanding of the molecular components associated with growth performance in the pearl oyster P. margaritifera and bivalves in general.

Biomineral photonic materials with a gradient structure: The ligament of the pearl oyster Pinctada margaritifera

The bivalve fibrous ligaments (FLs) are unusual biomineralized materials evolved to open two shell valves as needed. For a long time, the inside beautiful structural colors of the FLs have received little attention. Here, using optical microscopy, SEM, and fiber optic spectrometry combined with the image processing method and pair correlation function (Pcf) analysis, we investigate the structure and optical property of the FL of the pearl oyster Pinctada margaritifera. In this FL, we find that: (1) the aragonite fibers are uniform in diameter with an average of 98 ± 10 nm; (2) they are spatially organized with short-range order; and (3) they vary gradiently in their nearest-neighbor distance (d) from 148 nm to 103 nm along the lateral-inner direction of the FL. Therefore, this FL possesses a 2D amorphous gradient photonic structure, which results in that the FL displays extremely variable structural colors spanning from blue to yellow. In short, this work provides a new model of biological photonic structure, which may inspire the design and synthesis of novel photonic materials.

Substantial gene expression shifts during larval transitions in the pearl oyster Pinctada margaritifera.

Early development stages in marine bivalve are critical periods where larvae transition from pelagic free-life to sessile mature individuals. The successive metamorphosis requires the expression of key genes, the functions of which might be under high selective pressure, hence understanding larval development represents key knowledge for both fundamental and applied research. Phenotypic larvae development is well known, but the underlying molecular mechanisms such as associated gene expression dynamic and molecular cross-talks remains poorly described for several nonmodel species, such as P. margaritifera. We designed a whole transcriptome RNA-sequencing analysis to describe such gene expression dynamics following four larval developmental stages: d-shape, Veliger, Umbo and Eye-spot. Larval gene expression and annotated functions drastically diverge. Metabolic function (gene expression related to lipid, amino acid and carbohydrate use) is highly upregulated in the first development stages, with increasing demand from d-shape to umbo. Morphogenesis and larval transition are partly ordered by Thyroid hormones and Wnt signaling. While larvae shells show some similar characteristic to adult shells, the cause of initialization of biomineralization differ from the one found in adults. The present study provides a global overview of Pinctada margaritifera larval stages transitioning through gene expression dynamics, molecular mechanisms and ontogeny of biomineralization, immune system, and sensory perception processes.

Chemical compositions and gene expression pattern of five colored phenotypes of pearl oyster Pinctada margaritifera

Chemical compositions and gene expression pattern of five colored phenotypes of pearl oyster Pinctada margaritifera

Assessing regional connectivity patterns of bivalvia in fragmented archipelagos: Insights from biophysical modeling in French Polynesia

Larval dispersal and connectivity are key processes that drive marine metapopulation dynamics, and therefore should be well characterized when designing effective management strategies. While temperature and food availability can structure marine species connectivity patterns, their contribution has not been thoroughly investigated in highly fragmented archipelagos. We used biophysical modeling of larval dispersal to explore the connectivity patterns of species with complex life-cycles across French Polynesia (FP), a territory formed by more than a hundred small, geographically isolated islands covering an area as large as Europe. We first simulated ten years of larval dispersal to investigate the spatial and temporal (seasonal and interannual) variability in larval dispersal pathways for different hypothetical species exhibiting a range of Larval Precompetency Period (LPP) values. Then, using the black-lip pearl oyster (Pinctada margaritifera) as a model species, we accounted for variability in the LPP induced by temperature and food availability, as derived from a Dynamic Energy Budget (DEB) model. The model showed that food availability and mesoscale turbulence (eddies) in the Marquesas jointly constrained larval dispersal, reducing its potential connectivity with other archipelagos in FP. The DEB simulations also revealed seasonal and interannual variability in connectivity driven by environmental conditions. However, accounting for food and temperature effects on larval development, barely changed the connectivity pattern at regional scale due to the remoteness of this archipelago. Our study thus provides appropriate management units definition at regional scale for the species across FP.

Evidence of a Scheduled End for Prism Growth in the Shell of Pinctada margaritifera: Closure of the Calcite Biomineralization Area by a Specific Organic Membrane

The shell of the pearl oyster Pinctada margaritifera is made up of two layers: an outer layer of calcite prisms and an inner layer of aragonite tablets. Recent studies have shown that the calcite layer develops in a series of steps. We found that the end of prism growth and the start of aragonite deposition are also complex processes. Contrary to the common belief that prism growth is interrupted by the expansion of the aragonite layer, we found that a specific membrane covers the calcite surface before aragonite deposition starts. The earliest aragonite depositions occur as granular spots located only on the surfaces covered by this organic membrane This membrane appears to be the final stage of the calcite biomineralization cycle. This new understanding of calcite development has implications for shell biomineralization research and the production of pearls.

Pearl Farming Micro-Nanoplastics Affect Oyster Physiology and Pearl Quality.

Pearl farming is crucial for the economy of French Polynesia. However, rearing structures contribute significantly to plastic waste, and the widespread contamination of pearl farming lagoons by microplastics has raised concerns about risks to the pearl industry. This study aimed to evaluate the effects of micro-nanoplastics (MNPs, 0.4-200 μm) on the pearl oyster (Pinctada margaritifera) over a 5-month pearl production cycle by closely mimicking ecological scenarios. MNPs were produced from weathered plastic pearl farming gear and tested at environmentally relevant concentrations (0.025 and 1 μg L-1) to decipher biological and functional responses through integrative approaches. The significant findings highlighted the impacts of MNPs on oyster physiology and pearl quality, even at remarkably low concentrations. Exposure to MNPs induced changes in energy metabolism, predominantly driven by reduced assimilation efficiency of microalgae, leading to an alteration in gene expression patterns. A distinct gene expression module exhibited a strong correlation with physiological parameters affected by MNP conditions, identifying key genes as potential environmental indicators of nutritional-MNP stress in cultured oysters. The alteration in pearl biomineralization, evidenced by thinner aragonite crystals and the presence of abnormal biomineral concretions, known as keshi pearls, raises concerns about the potential long-term impact on the Polynesian pearl industry.

Lagoon hydrodynamics of pearl farming atolls: the case of Raroia, Takapoto, Apataki and Takaroa (French Polynesia)

Abstract. Between 2018 and 2022, four pearl farming Tuamotu atolls of French Polynesia were monitored with autonomous oceanographic instruments to measure the hydrodynamics of atoll lagoons and the ocean–lagoon water exchanges. These surveys were conducted within the framework of the ANR-funded MANA (Management of Atolls) project and its extensions to additional sites. The overarching goal was to improve knowledge on the processes influencing the spat collection of the pearl oyster Pinctada margaritifera, the oyster species used to produce black pearls. These data sets are also critical for the calibration and validation of 3D high spatial resolution hydrodynamic models used to study oyster larval dispersal within lagoons. The observational strategies focused on the characterization of ocean–lagoon exchanges through passes and hoa (i.e., shallow reef flats), lagoon circulation, incident waves breaking on the forereef, water elevation inside the lagoon as well as spatial temperature variability. Chronologically, the investigated atolls were first Raroia Atoll with 9 months of measurements between May 2018 and March 2019 during which the MALIS1 and MALIS2 cruises on-board the R/V ALIS took place. It was followed by a 4 month deployment in Takapoto Atoll (November 2021 to March 2022). In late April 2022, Apataki Atoll was instrumented until end of July, followed by Takaroa measurements between July and October 2022. Apataki (Leg2) and Takaroa Atoll were conjointly instrumented during the MALIS 3 oceanographic cruise. Altogether, those multi-atoll data bring a worldwide unique oceanographic atoll data set that is useful for addressing local pearl farming questions but potentially beneficial for other fundamental and applied investigations. Each data set was post-processed, quality controlled and converted into NetCDF format. Files are available in open source into dedicated repositories in the SEANOE marine data platform. Links (DOI) of individual data sets are provided in Table 2.

Pearl shape classification using deep convolutional neural networks from Tahitian pearl rotation in Pinctada margaritifera

Tahitian pearls, artificially cultivated from the black-lipped pearl oyster Pinctada margaritifera, are renowned for their unique color and large size, making the pearl industry vital for the French Polynesian economy. Understanding the mechanisms of pearl formation is essential for enabling quality and sustainable production. In this paper, we explore the process of pearl formation by studying pearl rotation. Here we show, using a deep convolutional neural network, a direct link between the rotation of the pearl during its formation in the oyster and its final shape. We propose a new method for non-invasive pearl monitoring and a model for predicting the final shape of the pearl from rotation data with 81.9% accuracy. These novel resources provide a fresh perspective to study and enhance our comprehension of the overall mechanism of pearl formation, with potential long-term applications for improving pearl production and quality control in the industry.

Cryogrinding and sieving techniques as challenges towards producing controlled size range microplastics for relevant ecotoxicological tests

The impact of microplastics (MP) has attracted much attention from the scientific community and many laboratory assessments have been made of their effects on aquatic organisms. To produce MP from real environmental plastic waste, which would enable more realistic experiments, we used plastic pearl farming equipment from French Polynesian lagoons. Here, the pearl oyster Pinctada margaritifera could encounter MP coming from their breakdown in its surrounding environment. We tested an established method based on mechanical cryogenic grinding and liquid sieving. Our desired size range was 20–60 μm, corresponding to the optimal particle size ingested by P. margaritifera. The protocol was effective, generating MP particles of 20–60 μm (∼17,000–28,000 MP μg−1), but also produced too many smaller particles. The peak in the desired size range was thus flattened by the many small particles <3 μm (∼82,000–333,000 MP μg−1; 53–70% of total analysed particles), visible at the limit of Coulter counter analysis (cut-off point: 2 μm). Laser diffraction analysis (cut-off point: 0.4 μm) provided greater detail, showing that ∼80–90% of the total analysed particles were <1 μm. Diverging particle size distributions between those expected based on sieving range and those really observed, highlight the need to perform fine-scaled particle size distribution analyses to avoid underestimating the number of small micro- and nanoplastics (MNP) and to obtain an exact estimation of the fractions produced. Size and microstructure characterization by scanning electron microscopy suggested spontaneous particle self-assembly into crystal superstructures, which is the supposed cause of the divergence we observed. Overall, our results emphasize that particle self-assembly is a technical hurdle requiring further work and highlight the specific need to finely characterize the size distribution of MNP used in ecotoxicological experiments to avoid overestimating effects.

Improved ocean-based nursery culture of blacklip pearl oyster (Pinctada margaritifera) juveniles in mesh baskets using cyanoacrylate adhesive

The blacklip pearl oyster, Pinctada margaritifera, supports well-established cultured pearl industries throughout the Pacific with various nursery culture methods used to on-grow juvenile oysters to a size suitable for pearl production. Locally-available plastic baskets are commonly used to rear juvenile oysters, but they do not prevent oysters from aggregating, which negatively impacts production. To develop an understanding of how basket-based nursery culture might best be adapted for rearing juvenile P. margaritifera, this study examined growth and survival of juveniles of varying sizes and stocked at varying densities in mesh baskets when using a cyanoacrylate adhesive to prevent aggregation. During a 3.5-month ocean-based nursery culture period, stocking density was shown to have a significant effect on growth (F = 11.53, p < 0.001), yet a minimal influence on oyster survival (χ2 = 5.05, p = 0.28). By contrast, stocking size influenced survival (χ2 = 7.17, p = 0.03), but had minimal impact on growth (F = 3.24, p = 0.08). Given that mean ( ± SD) survival of juveniles ranged from 65.0 ± 14.4% to 94.0 ± 8.2% and dorsoventral shell growth ranged from 13.9 ± 6.2 mm to 19.7 ± 6.3 mm, depending on stocking density and stocking size, these factors clearly merit consideration before fixing juvenile oysters to baskets with an adhesive. Such results broaden our knowledge of nursery culture methods for P. margaritifera and improve options for small-scale pearl farmers in the Pacific.

Natural stocks of Pinctada margaritifera pearl oysters in Tuamotu and Gambier lagoons: New assessments, temporal evolutions, and consequences for the French Polynesia pearl farming industry.

Knowledge of the status of the black-lipped pearl oyster Pinctada margaritifera populations is critical for the sustainability of the French Polynesia black pearl farming industry. Indeed, this activity relies on collection of spat settling out of the water column, which is inherently related to the abundance of in situ benthic stocks and their reproductive capacities. From surveys performed between 2016 and 2021, we present new stock assessments of natural wild oyster populations from four contrasted pearl farming lagoons (Gambier, Takapoto, Raroia, Takume). Also using Ahe atoll historical data, we first highlight how results vary with the methods (Direct, Zonal and Cokriging) used to scale in situ density measurements to lagoon-scale stocks. Takapoto and Gambier populations were also previously surveyed at least twice since the 1980s, allowing to demonstrate with field data clear changes in stock distributions and population structures. The consequences of our findings are discussed to provide recommendations for stock monitoring and management in the future.

Identifying genes associated with genetic control of color polymorphism in the pearl oyster Pinctada margaritifera var. cumingii (Linnaeus 1758) using a comparative whole genome pool-sequencing approach.

For hundreds of years, the color diversity of Mollusca shells has been a topic of interest for humanity. However, the genetic control underlying color expression is still poorly understood in mollusks. The pearl oyster Pinctada margaritifera is increasingly becoming a biological model to study this process due to its ability to produce a large range of colors. Previous breeding experiments demonstrated that color phenotypes were partly under genetic control, and while a few genes were found in comparative transcriptomics and epigenetic experiments, genetic variants associated with the phenotypes have not yet been investigated. Here, we used a pooled-sequencing approach on 172 individuals to investigate color-associated variants on three color phenotypes of economic interest for pearl farming, in three wild and one hatchery populations. While our results uncovered SNPs targeting pigment-related genes already identified in previous studies, such as PBGD, tyrosinases, GST, or FECH, we also identified new color-related genes occurring in the same pathways, like CYP4F8, CYP3A4, and CYP2R1. Moreover, we identified new genes involved in novel pathways unknown to be involved in shell coloration for P.margaritifera, like the carotenoid pathway, BCO1. These findings are essential to possibly implement future breeding programs focused on individual selection for specific color production in pearl oysters and improve the footprint of perliculture on the Polynesian lagoon by producing less but with a better quality.

Growth and Survival of Black-lip Pearl Oyster Pinctada margaritifera (Linnaeus, 1758) in Bamboo and Metal-framed Pocket Net Baskets Subjected to Cleaning and Without Cleaning Conditions

The farming of black-lip pearl oyster Pinctada margaritifera (Linnaeus, 1758) has been a viable industry for small and large-scale farmers in the South Pacific, but not in the Philippines, where it is monopolized by large-scale farms primarily based on the gold-lip pearl oyster Pinctada maxima. To promote the industry among small-scale players, we simplified the culture method by using bamboo slats as frame materials and compared them to the common material used in pearl oyster culture, metal rods. A total of 400 individuals seven-month-old hatchery-produced P. margaritifera were used as experimental animals, distributed in the following treatments with five replications: T1 (metal-framed pocket net basket with monthly cleaning), T2 (metal-framed pocket net basket without monthly cleaning), T3 (bamboo-framed pocket net basket with monthly cleaning), and T4 (bamboo-framed pocket net basket without monthly cleaning). Growth was fast in the first four months and slowed down after that. Two-way analysis of variance found no significant differences between the average anteroposterior shell (APS) length increments of pearl oysters between two types of frame, and between two cleaning conditions. Survival rates did not significantly differ between types of basket frame, and between cleaning conditions. Parameters of the “Typical” von Bertalanffy growth model (L∞ = 118.41 mm, K = 1.03 year-1, and t0 = 0.12) suggested that oyster would take about 23.16 months to reach 100 mm APS length, a size suitable for nucleus implantation. The life span of bamboo slats as basket frame was half of the metal frame, and the absence of cleaning has reduced the operational cost by up to 82.08%.

GROWTH PATTERNS OF THE PEARL OYSTER Pinctada margaritifera IN NORTH SULAWESI WATERS

The pearl oyster Pinctada margaritifera (Linnaeus, 1758) or black lip pearl oyster is a marinebivalves with important economic value. This Indo-Pacific species is found in abundance in the waters of North Sulawesi, but cultivation activities have not been optimized. Growth information is important for aquaculture activities because it is a useful indicator to determine the health of pearl oysters and environmental suitability (Moussa, 2013). The purpose of this study was to determine the growth pattern of P. margaritifera pearl shells in the waters of North Sulawesi. Species P. margaritifera were collected at a depth of 2-20 m in the waters of North Minahasa Bahoi, Arakan waters South Minahasa and Talengen waters Sangihe Islands, North Sulawesi Province. The morphometric parameters observed included shell length (PC), shell height (TC), shell thickness (tC), and total weight (BT). The relationship between length, height, shell thickness and total weight was analyzed by regression equation. Morphometric measurements of P. margaritifera showed average shell length (PC) of 95.26 mm (Arakan waters), 81.15 mm (Talengen waters) and 70.19 mm (Bahoi waters). The growth pattern of P. margaritifera in the waters of Bahoi, Arakan and Talengen, North Sulawesi Province was allometric negative. This means that the increase in length, height and thickness of the shell is faster than the total weight.

Different food particle sources in the pearl oyster Pinctada margaritifera and its epibionts

Suspended bivalve culture (e.g. longlines) transfers benthic biomass - including bivalves and various epibionts - toward the water column, creating strong trophic interactions with the planktonic compartment. Trophic interactions are of central interest for ecologists, yet not well understood in coastal lagoon food webs, especially in tropical areas. Using stable isotope (SI) analyses, this study explored the trophic relationships between marine particulate organic matter (POM), pearl oysters and epibionts, in two contrasted production areas in French Polynesia. Different size classes of POM (0.7–2 µm, 2–20 µm, 20–80 µm, 80–250 µm and >250 µm) were well discriminated both by their δ13C and δ15N signature and results showed a low dietary overlap between pearl oysters and epibionts, likely due to assimilation of large particles in greater proportion by pearl oysters. Pearl oyster diet may vary in time in relation with variations of the basal trophic resource and selective feeding, such that their isotopic signature is more variable compared with that of epibionts. Pearl oysters and epibionts might alter nutrient cycling in a different way as reflected by their different tissue C:N.

Karakteristik morfometrik kerang mutiara Pinctada margaritifera di Perairan Arakan, Mantehage Bango dan Talengen Provinsi Sulawesi Utara untuk kelayakan budidaya

The purpose of this study were (1) to determine the morphometric characteristic of pearl oyster Pinctada margaritifera in Arakan, Mantehage Bango, and Talengen waters of North Sulawesi Province, (2) to determine the ideal location for the feasibility of pearl oyster culture. Determination of the sampling location is done by purposive sampling. The shell morphometric dimensions measured were shell length, shell height, hinge length, shell thickness and shell weight. The measured water quality were temperature, salinity, dissolved oxygen, pH, and depth. The morphometric characteristic of P. margaritifera oyster in Arakan waters have shell length (PC) ranging from 44,25 – 169,77 mm with an average of 86,50 mm, Mantehage Bango waters have PC ranged from 38,73 – 106,09 mm with an average of 80,31 mm, and Talengen waters have PC ranged from 25,89 mm to 105,34 mm with an average of 68,97 mm. Arakan waters are dominated by medium size P. margaritifera (53,78%), it is suspected that Arakan waters have pearl oyster stocks in nature for aquaculture activities. Evaluation of the suitability of waters for pearl oyster culture P. margaritifera in Arakan waters scored 77,7% categorized as suitable (S2), the location of Mantehage Bango waters scored 80% categorized as suitable (S2) and the location of Talengen waters 68,8% categorized as conditional (S3).

Assessment of an alternative Pinctada margaritifera spat collector in French Polynesia

Plastic waste in the oceans is a growing concern due to its size diversity, its ubiquitous nature and its impact on both marine organisms and ecosystems. While threatened by this marine plastic litter, the aquaculture industries also represent one of its major sources. In French Polynesia, black-lip pearl oyster (Pinctada margaritifera) farming is no exception. Wild spat collection has been described as a source of pollution because of the numerous particularly fragile and brittle shade-mesh plastic collectors used locally and often mismanaged when no longer usable. Thus, with the aim of helping to reduce this pollution, the present study is focused on the assessment of reusable plate collector as a potential alternative. We tested, using an in situ approach, the influence of the collecting surface position (i.e. horizontal vs vertical), plate color (i.e. black vs orange) and density (i.e. 25 plates vs 50 plates) on Pinctada margaritifera and Pinctada maculata spat settlement. Our results showed that 50-plates collectors, whatever their color and position, were more efficient to collect both kinds of spat than shade-mesh collectors (P < 0.0001). They also induced a higher number of Pinctada margaritifera spat than on the 25-plates collection device although there was no significant difference in numbers of Pinctada maculata spat (P < 0.0001). However, every type of plate collector presented a decreased mean length of the spat collected (P < 0.0001) compared to the shade-mesh collector. Furthermore, horizontal positioning of the collecting surface greatly improved the spat numbers on plate collectors (P < 0.0001) although there was no effect on shade-mesh collectors (P > 0.05). Finally, our results indicated that, among all the devices tested, the black horizontal 50-plates collector was the most efficient to collect spat and particularly Pinctada margaritifera. These first findings thus tend to suggest that these black re-usable plate collectors could be an efficient alternative to the currently used shade-mesh collectors.

Dynamic Energy Budget model suggests feeding constraints and physiological stress in black-lip pearl oysters, 5 years post mass-mortality event

Mass-mortality events of marine species can disturb the structure of communities. While identifying the causes of mass-mortality events is crucial for implementing recovery strategies, monitoring is challenging in remote locations. Black-lip pearl oysters (Pinctada margaritifera) are farmed for producing black pearls within remote atolls of French Polynesia. Previous mass-mortality events have resulted in the collapse of oysters and other species; however, the causes and conditions that favour recovery are unclear. We investigated the potential for oyster population recovery 5 years after a mortality event at Takaroa Atoll (Tuamotu Archipelago). Temperature, food availability (total chlorophyll-a), growth and reproduction were monitored. Growth was also simulated using a Dynamic Energy Budget model. Despite favourable conditions, reduced growth and reproduction signalled an energetic deficit. The model overpredicted growth, and supported the hypotheses that individuals are unable to profit from the phytoplankton available and maintenance costs are high in Takaroa, ultimately explaining their poor physiological condition.