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Article

Feeding Physiology of Crassostrea gasar (Dillwyn, 1817) on Isochrysis galbana and Biofloc Diets

by
Thaís Brito Freire
,
Flávia Lucena Zacchi
,
João Paulo Ramos Ferreira
,
Carlos Henrique Araujo de Miranda Gomes
and
Claudio Manoel Rodrigues de Melo
*
Laboratório de Moluscos Marinhos, Departamento de Aquicultura, Universidade Federal de Santa Catarina, Florianópolis 88061-600, SC, Brazil
*
Author to whom correspondence should be addressed.
Fishes 2026, 11(4), 227; https://doi.org/10.3390/fishes11040227
Submission received: 25 February 2026 / Revised: 4 April 2026 / Accepted: 6 April 2026 / Published: 14 April 2026
(This article belongs to the Special Issue An Issue in Honor of Yoram Avnimelech: Application of Biofloc Technology (BFT))
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Abstract

Understanding the feeding physiological mechanisms of determined oyster species is fundamental for adaptation and growth stabilization, aiming for gains in aquaculture production. To assess its potential for Integrated Multi-Trophic Aquaculture (IMTA) with shrimp, we analyzed the feeding physiology of the mangrove oyster Crassostrea gasar. In this study, we determined the feeding physiology of the mangrove oyster Crassostrea gasar, a commercially important species in tropical Brazil, under two diets, live microalgae (ISO—Isochrysis galbana) and biofloc (BFT), which were tested at four concentrations (10, 20, 30, and 40 mg L−1), to establish whether this species can effectively utilize BFT as a food source. Results indicated that ISO diet promoted superior filtration, characterized by a higher proportion of feces (F), suggesting a reduced need for intensive particle selection. Both clearance (CR) and filtration (FR) rates peaked at 30 mg L−1 before declining, suggesting a physiological threshold for this diet. In contrast, the BFT diet elicited higher CR and FR values but triggered excessive pseudofeces (PF) production and low net organic selection efficiency (NOSE). This suggests high particle rejection and limited nutritional assimilation. In conclusion, while C. gasar can process BFT, it is metabolically disadvantageous as a sole food source. For an optimal performance, I. galbana concentrations should be maintained at or below 30 mg L−1.
Keywords:
bivalve mollusk; clearance rate; filtration rate; mangrove oyster; microbial flocs
Key Contribution: This study provides a detailed physiological assessment of Crassostrea gasar under controlled diets of Isochrysis galbana microalgae and biofloc, revealing that bioflocs are metabolically disadvantageous due to high particle rejection.

1. Introduction

Bivalves exhibit physiologically plastic feeding, allowing them to adapt to fluctuations in seston composition and particle load [1,2,3]. Seston, defined as the total suspended material in seawater, is commonly used as a synonym for total particulate matter (TPM), which is composed of particulate organic matter (POM) and particulate inorganic matter (PIM) [4]. POM, in turn, consists of particulate organic carbon and nitrogen and includes live microalgae, degraded cells (phytodetritus), and plant material of marine or terrestrial origin, such as that from leaching. Characterizing seston properties is essential for understanding bivalve feeding behavior, specifically organic particle ingestion, and for estimating growth patterns in relation to food quality.
To efficiently process the complex mixture of suspended particles in seawater, bivalves have developed selective feeding capabilities. This mechanism allows them to either ingest captured material, resulting in the production of feces (F), or reject it as pseudofeces (PF, captured material that is expelled without being ingested or digested) [2,5,6,7]. In oysters, this process begins as water and food enter through the incurrent aperture and are directed by the gill cilia toward the excurrent aperture. This pumping flow can be actively regulated within the mantle cavity [8].
The mechanism of pre-ingestive selection and PF formation represents a strategy for optimizing energy acquisition in bivalves [3,9,10]. This process has been widely investigated to understand which particle types (e.g., microalgae or detritus) are preferentially filtered and how this selective mechanism is regulated [3,11,12,13,14].
In their natural environment, the particulate matter retained on the gills of bivalve mollusks includes bacteria, phytoplankton, protozoa, small invertebrate larvae, and suspended detritus, all of which contribute to their diverse diet [15]. The quality and concentration of these particles strongly influence oyster feeding, shaping their physiology and energy balance. Understanding these processes provides critical insights into the ecological niche of oysters and facilitates the identification of suitable aquaculture sites for commercially important species [16,17].
Maintaining broodstock for gonad maturation or operating indoor bivalve production systems requires a steady supply of mixed microalgal diets. Isochrysis galbana (Parke, 1949) (ISO) and Chaetoceros müelleri (Lemmermann, 1898) are the most frequently employed species due to their well-established nutritional profiles [18,19]. Their quality is largely defined by their fatty acid content, specifically polyunsaturated fatty acids (PUFAs), which vary in quantity and composition across species [18,20]. Furthermore, the quality and availability of microalgae, alongside other physiological factors, significantly influence oyster growth rates [21], condition index (CI), and the rate of gametogenesis [22]. To improve the economic viability of oyster cultivation, research has focused on alternative feedstuffs to reduce or even avoid the reliance on live algae, as microalgal production can account for up to 60% of total operational costs in aquaculture systems [23].
In this context, Integrated Multi-Trophic Aquaculture (IMTA) is notable for its sustainable and ecological approach, incorporating species from different trophic levels in aquaculture production. This approach aims to maximize systemic efficiency by repurposing the metabolic waste of one species as nutrients for another. By establishing this closed-loop framework, the system significantly reduces environmental discharge while boosting overall productivity [24]. Practical applications of IMTA often feature synergistic pairings such as fish, algae, and shellfish, or integrated shrimp and shellfish cultures [25]. A common prominent system verified for shrimp production inserted in the context of IMTA applies the usage of Biofloc Technology (BFT), which promotes the continuous recycling of nutrients and water reuse throughout production cycles, improving ecological sustainability and optimizing the species production. Although, despite its sustainable dynamics, the BFT system still generates waste, such as suspended solids, that requires management. In this context, the possibility for the inclusion of oysters in this IMTA configuration emerges as an efficient alternative for utilizing the surplus solids generated by BFT.
Oysters have been evaluated as biological filters when co-cultured with the shrimp Penaeus vannamei (Boone, 1931) in both BFT and IMTA systems [26,27,28]. Optimal shrimp production in BFT requires TPM concentrations between 400 and 600 mg L−1 to facilitate nutrient recycling via bacterial activity and maximize feed efficiency [29,30,31]. In contrast, oysters are specialized for low-TPM environments (<2 mg L−1) [32], and are effective at controlling phytoplankton blooms in nutrient-enriched waters [33]. High solids concentrations (>90 mg L−1) induce reduced filtration rates and morphological alterations in oyster labial palps, with total filtration failure occurring above 200 mg L−1 [34]. These constraints highlight a fundamental physiological incompatibility between oysters and standard BFT shrimp culture. Nevertheless, the potential for using BFT as a feedstock, provided conditions are adjusted to oyster physiological limits, remains an open question, specifically regarding whether oysters derive nutritional benefit or exhibit aversive responses.
C. gasar, a mangrove oyster native from tropical Atlantic coast of South America and Africa, typically inhabits intertidal zones and brackish estuaries [35]. As a cornerstone of tropical aquaculture, its cultivation is well-established across Brazil, spanning from Pará to Santa Catarina [36], and accounts for approximately 7% of the national bivalve production [37]. While the mechanisms of particle selection in the Crassostrea genus are increasingly understood, significant knowledge gaps remain for C. gasar. Specifically, its physiological response to diverse feeding regimes, including microalgae and alternative feed sources like Biofloc Technology (BFT), requires further investigation.
The physiological efficiency of bivalves may be reflected in their biodeposition (BD), comprising feces (F) and pseudofeces (PF). The weight differential between ingested organic matter and these expelled materials ultimately dictates whether a bivalve exhibits favorable growth [38,39]. Identifying how varying concentrations of microalgae and BFT affect the interplay between BD, clearance rate (CR), filtration rate (FR), and net organic selection efficiency (NOSE) is critical to understanding the ingestion dynamics of C. gasar. This study compared the feeding physiology of C. gasar under conventional and BFT-based diets to assess the viability of microbial flocs as an alternative nutritional source.

2. Materials and Methods

2.1. Origin of Crassostrea gasar Oysters

Adult oysters produced in the Laboratory of Marine Mollusc (LMM) of the Department of Aquaculture at the Federal University of Santa Catarina (UFSC) were used for experiments. For the trial, Isochrysis galbana (ISO), and Biofloc Technology (BFT), approximately 10 oysters were used for each treatment (ISO10 no.: 9, ISO20 no.: 10, ISO30 and ISO40 no.: 11, BFT10, BFT20, BFT30, and BFT40 no.: 10), and each possessed a mean height of 63.76 ± 10.56 mm.

2.2. Experimental Diets

Experimental animals were fed once a day according to their assigned diet (ISO or BFT) and treatment concentration (10, 20, 30, or 40 mg L−1). Diets were added to reservoirs containing filtered seawater, which functioned as feeding tanks. A semi-recirculating aquaculture system (semi-RAS, Figure 1) equipped with submerged pumps (Aleas/Jeneca HM-5063, 2000 L/h—Foshan City Nanhai Jiabaolai Aquarium Equipment Co., Ltd., Foshan, China) was used to distribute the feed.

2.2.1. Isochrysis galbana (ISO)

ISO was cultured in 100 L plastic bags containing sterilized and filtered (0.5 µm) seawater enriched with F/2 medium. The cultures were maintained at 23 ± 2 °C, with a salinity of 36 ± 1 psu and under continuous (24 h) artificial fluorescent light.
Cell density was first determined by counting in a Neubauer chamber under a light microscope (Leica DM500—Leica Microsystems Shanghai, Shanghai, China). For the determination of ISO cell weight, samples of 5 mL of I. galbana were filtered using GF/C glass fiber microfilters (0.3 μm) (Whatman International Ltd., Maidstone, UK), which had been prewashed, dried, burned, and weighed in advance. After filtration, the samples were rinsed with 20 mL of ammonium formate (0.5 M) to remove seawater salts. The filters were then oven-dried at 60 °C for 24 h and weighed [40]. The feed supply was then adjusted based on the determined cell weight for ISO (3.8 × 10−8 mg cell−1), corresponding to a feeding concentration of 26.4 × 107 cell L−1 for ISO10, 52.8 × 107 cell L−1 for ISO20, 79.2 × 107 cell L−1 for ISO30, and 105.6 × 107 cell L−1 for ISO40.

2.2.2. Biofloc (BFT)

Biofloc was supplied by the Marine Shrimp Laboratory of UFSC and produced in a tank with a working volume of 50 m3, stocked with 300 shrimp m−3 in water with a stable nitrification cycle and a current nutritional profile verified in Freire [41]. The tank was initially filled with water at a salinity of 33 to 34 psu, and the photoperiod was natural. The temperature was maintained at an average of 27.5 ± 1.3 °C. Control of ammonia was performed with the daily addition of cane sugar as an organic carbon source [42]. The BFT, with a particle concentration ranging from 426 to 601 mg L−1, was sieved (200 µm mesh) to remove shrimp detritus and then diluted in seawater to achieve the desired concentrations (10, 20, 30, and 40 mg L−1).
All small particles and >80% of aggregate sizes of the current BFT after sieving were of a suitable size (<200 µm) for ingestion by adult oyster specimens [41].

2.3. Physicochemical Parameters

Water temperature (°C) was recorded daily before feeding, one hour after feeding, and at the time of the filtration assay using a mercury thermometer. Salinity was measured once a day using a refractometer (Biobrix, Model 211—Biobrix Consultoria e Comércio Ltda., São Paulo, Brazil). The pH was measured daily at the time of the physiology assay using a benchtop pH meter (Alfakit, Model AT-350—Alfakit Indústria e Comércio de Produtos Analíticos Ltda., Florianópolis, Santa Catarina, Brazil). All parameters remained within the acceptable range for the species during the filtration assay (ISO: Temperature 23.47 ± 0.80 °C, salinity 34.75 ± 0.5 psu, and pH 7.56 ± 0.05; BFT: Temperature 23.00 ± 0.67 °C, salinity 35.25 ± 0.5 psu, and pH 7.99 ± 0.05).

2.4. Biodeposit Collection

To assess the dietary consumption of the oysters, biodeposition data were obtained using the system and a method described by Nascimento et al. [43]. Eighty oysters from each treatment of ISO (ISO10, ISO20, ISO30, ISO40 mg L−1) and of BFT (BFT10, BFT20, BFT30, BFT40 mg L−1) were acclimatized for 5 days with the test diets (20 oysters/unit, Figure 1). The acclimatization system consisted of batch-connected feed and acclimatization units (AU) with water and feed, renewed daily for each treatment. Aeration in feed tanks (Figure 1, no. 1) was carried out by compressed air distributed through a central PVC pipe (Figure 1, no. 2) to which individual silicone hoses were connected for air distribution to the tanks. The ends of the aeration hoses were connected to an air stone (Figure 1, no. 3) for improved air dispersion. The dynamics of the system operation consisted of pumping water and food from the feed tanks to AU (Figure 1, no. 4) using submerged pumps (Figure 1, no. 5). Water and food were distributed to the AU through the main distribution PVC pipe (Figure 1, no. 6), to which silicone hoses corresponding to each AU (Figure 1, no. 7) were connected. Next, by circulating through the AU, they fall by gravity into a PVC pipe (Figure 1, no. 8) and are returned to the feed tank. AU oxygenation was carried out by aeration distributed through a central PVC pipe to which silicone hoses were connected for individual air distribution in the AU (Figure 1, no. 9).
After this period, approximately 10 (see details in Section 2.1) oysters from each treatment were randomly and individually allocated to separate chambers. Each oyster was housed in an independent chamber, and the water from different chambers did not mix during the biodeposits collection. The first set of biodeposits that was produced was discarded. Subsequent biodeposits were collected individually using a 10 mL Digipet automatic pipette (Labnet International, Inc., Edison, NJ, USA) and stored in 50 mL tubes with conical bottoms (Cral Artigos para Laboratório Ltda., Cotia, São Paulo, Brazil).

2.5. Quantification of Particulate Matter

Three 500 mL samples of seawater containing feed (ISO or BFT) were collected during each trial for subsequent particulate matter analysis. The storage container was rinsed three times with sample seawater before each collection. Subsequently, the samples were filtered through pre-washed, pre-combusted (450 °C), and pre-weighed GF/C glass fiber microfilters (Whatman International Ltda, Maidstone, UK). After filtration, the filters were rinsed with 20 mL of ammonium formate (0.5 M) to remove salt [44]. The filters were dried in an oven at 60 °C for 24 h and weighed to determine the total particulate matter (TPM). The filters were then combusted in a muffle furnace at 450 °C for 4 h to remove organic matter and weighed again to determine the particulate inorganic matter (PIM). Particulate organic matter (POM) was determined as the difference between TPM and PIM. The organic content of seston (OCS) was calculated as the ratio of POM to TPM [45].

2.6. Physiological Rates

CR and FR were calculated using the biodeposit method described by Hawkins et al. [45], see Table 1. The animal tissues were dried in an oven at 60 °C for 48 h to standardize the rates per gram of animal dry weight.

2.7. Statistical Analysis

The relationship between diets (ISO10, ISO20, ISO30, ISO40, and BFT10, BFT20, BFT30, BFT40) and physiological indices (CR, FR, BD, TBDR, OBDR, and NOSE) was analyzed using generalized linear models (GLM) with the distribution families and link functions that best fitted the data. GLM selection was based on Akaike information criterion (AIC) values. Pseudo-R2 was determined by calculating D-squared (D2), as described by Guisan and Zimmerman [46]. A significance level of 5% was used for all analyses. Data analyses were implemented using RStudio® software (v.4.3.2).

3. Results

In this study, we present the physiological responses of C. gasar to Isochrysis galbana (ISO) and biofloc (BFT) diets separately, given the distinct composition of each feedstock. Notably, the BFT diet contained higher levels of particulate inorganic matter (PIM) compared to the ISO diets (Table 2). This condition substantially influenced the calculated physiological rates (Clearance rate (CR) and Filtration rate (FR)), as these parameters are derived from the amount of PIM present in feces (F) and pseudofeces (PF), as well as in the suspended diet.

3.1. Isochrysis galbana Diet

The values obtained from the evaluated diets (ISO10, ISO20, ISO30, and ISO40) showed distinct trends: F, biodeposition (BD), and biodeposition rate (TBDR) exhibited a parabolic trend; PF and organic biodeposition rate (OBDR) demonstrated a positive linear trend; and organic selection efficiency (NOSE) revealed a negative linear trend. The D2 values of the fitted models for the tested metrics ranged from 0.11 to 0.83 (Figure 2).
The F production of C. gasar increased as the concentration of microalgae particles increased, up to the ISO30 treatment (Figure 2a). Oysters fed with the ISO30 diet produced more F (3.40 mg g−1) compared to those fed with ISO10, ISO20, and ISO40 (2.28, 1.45, and 3.04 mg g−1, respectively), confirming the relationship between increasing microalgae levels and F production (p < 0.05; D2 = 11%) (Figure 2a; Table 3).
The PF production of the oysters (0.41, 1.35, 2.37, and 2.57 mg g−1 for ISO10, ISO20, ISO30, and ISO40, respectively) increased with the concentration of microalgae particles in the diet, showing a positive relationship (p < 0.05; D2 = 44%) between microalgae concentration and PF production (Figure 2b, Table 3).
The highest CR for C. gasar (1.01 L h−1 g−1) was found when the oysters were fed with the ISO30 diet. When subjected to the ISO40 diet, the CR decreased (0.39 L h−1 g−1) compared to the other diets, including the lower concentration diets of ISO10 (CR, 0.66 L h−1 g−1) and ISO20 (CR, 0.62 L h−1 g−1). This response indicates a potential plateau for the species processing and filtration capacity, a relationship confirmed by the model (p < 0.05; D2 = 16%) (Figure 2c, Table 3).
The oysters FR gradually increased as the concentration of available ISO in the diet increased (1.59 and 1.55 mg h−1 g−1 for ISO10 and ISO20, respectively), peaking with the ISO30 diet (2.84 mg h−1 g−1), before decreasing with the ISO40 diet (1.40 mg h−1 g−1) (p < 0.05; D2 = 18%) (Figure 2d, Table 3).
The BD (F + PF) production of C. gasar gradually increased as the microalgae concentration increased up to the ISO30 level (p < 0.05; D2 = 31%) (Figure 2e, Table 3).
A positive relationship (p < 0.05; D2 = 21%) was observed for TBDR across the evaluated diets, with values of 2.90, 3.35, 5.37, and 5.06 mg h−1 for ISO10, ISO20, ISO30, and ISO40, respectively (Figure 2f, Table 3).
Similarly, the OBDR of C. gasar increased with rising microalgae concentration, reaching 2.27, 2.56, 5.30, and 5.40 mg h−1 under ISO10, ISO20, ISO30, and ISO40, respectively (p < 0.05; D2 = 35%) (Figure 2g, Table 3).
In contrast, the NOSE fraction decreased with increasing ISO concentration in the diet, with values of 0.78, 0.08, 0.08, and 0.04 for ISO10, ISO20, ISO30, and ISO40, respectively, indicating a significant negative relationship (p < 0.05; D2 = 88%) (Figure 2h, Table 3).

3.2. Biofloc Diet

The amount of PF showed a positive linear trend. Conversely, the values for F, BD, TBDR, and OBDR showed a parabolic trend, with inflections at the highest BFT concentrations. NOSE, however, showed a negative linear trend. The D2 values of the models for the tested metrics ranged from 0.11 to 0.68 (Figure 3, Table 4).
Crassostrea gasar oysters selected, processed, and eliminated BFT as F in increasing quantities up to the BFT30 diet (1.35, 1.77, and 6.03 mg g−1). Subsequently, a decrease was observed in the amount of F produced by animals fed with BFT40 (4.45 mg g−1). This response indicates a potential plateau for the species’ acceptable limit for processing and eliminating BFT as F (p < 0.05; D2 = 48%) (Figure 3a, Table 4).
The amount of PF produced by C. gasar varied depending on BFT concentration in the diets. An increase was found in oysters fed with BFT10 (3.50 mg g−1) and BFT20 (7.50 mg g−1), followed by a slight reduction at BFT30 (7.01 mg g−1) and stabilization at BFT40 (7.21 mg g−1). The model showed a positive relationship between BFT concentration in the diet and the amount of PF rejected (p < 0.05; D2 = 11%) (Figure 3b, Table 4).
The oysters had a CR of 1.26 L h−1 g−1 when fed with BFT10 and reached maximum efficiency when exposed to BFT20 (5.09 L h−1 g−1), followed by a decline with BFT30 and BFT40 (2.66 and 2.00 L h−1 g−1, respectively). The resulting inflection point demonstrates an acceptable limit for the clearance capacity of this bivalve when exposed to BFT (p < 0.05; D2 = 31%) (Figure 3c, Table 4).
The FR of C. gasar gradually increased as the available BFT concentration in the diet increased (5.40 and 12.36 for BFT10 and BFT20, respectively), reaching maximal efficiency with the BFT30 diet (14.74 mg h−1 g−1). The rate then inflected, decreasing when exposed to the BFT40 diet (12.25 mg h−1 g−1) (p < 0.05; D2 = 32%) (Figure 3d, Table 4).
BD (F + PF) production by C. gasar was 4.86 and 9.27 mg h−1 for the BFT10 and BFT20 diets, respectively, increasing to 13.04 mg h−1 with the BFT30 diet before decreasing to 11.66 mg h−1 at the BFT40 concentration (p < 0.05; D2 = 30%) (Figure 3e, Table 4).
An increase in TBDR production was found between the BFT10 (5.16 mg h−1), BFT20 (9.76 mg h−1), and BFT30 (14.33 mg h−1) diets, followed by a reduction at BFT40 (11.38 mg h−1). This variation demonstrated a statistically significant relationship between the increasing BFT levels tested and TBDR production (p < 0.05; D2 = 41%) (Figure 3f, Table 4).
The OBDR of C. gasar increased with dietary BFT concentration up to BFT30, followed by a decrease when fed BFT40. The mean values were 3.35, 5.78, 7.82, and 7.06 mg h−1 for the BFT10, BFT20, BFT30, and BFT40 diets, respectively (p < 0.05; D2 = 29%) (Figure 3g, Table 4).
The NOSE fraction of C. gasar exhibited a progressive decline with increasing concentrations of BFT in the diet, with values of 0.35, 0.28, 0.27, and 0.24 for BFT10, BFT20, BFT30, and BFT40, respectively. This trend, confirmed by the applied model, demonstrates a significant negative relationship between the evaluated parameters (p < 0.05; D2 = 23%) (Figure 3h, Table 4).

4. Discussion

Physiological responses of the Crassostrea gasar feeding mechanism are clearly modulated by food concentrations. From patterns encountered in regressions, it is possible to infer optimal quantities to better intervals for positive energy balance of the offered suspended particles acquired from filtration rate (FR) activity [47], which promotes growth in soft tissue, shell, or gametic tissue [48]. Conversely, we also encountered patterns with increased production of pseudofeces (PF), based either on the rejection of low-quality particles [49] or saturation of the selective feeding apparatus in oysters [50], hindering possible uses of the biofloc (BFT) to feed oysters in aquaculture systems.
The adjusted regressions between parameters and feed concentration, although most linear and quadratic tendencies are significant, the biological prediction may be inaccurate for some parameters due to the high dispersion of data. This reflects high individual variability from these parameters in oysters. Studies of oyster feeding physiology involve understanding complex biological systems of pre-selection and ingestion that operate under distinct conditions related to factors such as genetics [51], individual animal weight [52], individual size [53], pallial organ plasticity [54], as well as their condition index and sexual maturity [53,55]. Even during trials, oysters may actively feed during 49—91% of the time in chambers [32], with some authors reportedly excluding oysters without any feeding activity in their analysis [56,57], thus increasing individual variability during biodeposit (BD) collection. All these aspects enhance variability among C. gasar individuals’ physiological responses to the feed mechanism.
The results of this study, comparing Isochrysis galbana (ISO) microalgae and BFT diets for the mangrove oyster C. gasar, underscore the critical role of food quality in bivalve feeding responses. Food quality is fundamentally defined by the biochemical nature of particulate organic matter (POM), its proportion relative to total particulate matter (TPM), and the physical particle size [10,55]. The specific physiological responses elicited by these factors are examined individually in the following sections.

4.1. Microalgae Feeding Behavior

The feeding behavior of bivalve mollusks is influenced by both the concentration of suspended particles in the water and their nutritional properties. In this study, feeding rates followed a curvilinear pattern, increasing with particle concentration up to an optimal threshold (ISO20 or ISO30) before declining at higher levels. Similar responses have been documented in other marine mollusk species, including Cerastoderma edule [3], C. gigas [58,59], and Ostrea edulis [60].
The clearance rate (CR) of C. gasar increased to a maximum of 1.01 L h−1 g−1 at ISO30. At ISO40, there was a clear shift in feeding behavior towards lower activity, which may be related to valve closure mechanisms when particle concentrations exceed optimal conditions [61,62].
Furthermore, the CRs observed for C. gasar were lower than those found by other researchers for other ostreids. The CR of C. gasar fed with the ISO30 concentration was similar only to that observed for O. edulis, which had a CR of 0.8 L h−1 g−1 when fed with diets containing Phaeodactylum tricornotum and Chroomonas salina [7]. However, contrasting results exist for O. edulis, for which a CR of 6.5 L h−1 g−1 (at 20 °C, 808 cells mL−1) was observed when fed with I. galbana [63]. These CR values are more than double those observed in the present study using the same microalgal species (I. galbana). Additionally, CR values higher than those in our study have also been reported for C. gigas when feeding on seston in a natural environment average of 10.18 ± 7.47 L h−1 in [59], 6.8–16.7 L h−1 g−1 at 25 °C, 2.9 cells mL−1 in [64], or even when fed with only I. galbana in the laboratory (4.8 L h−1 g−1 in [65]). The differences in feeding and processing responses observed among experiments can be attributed to different temperatures, methodologies, and ISO concentrations compared to our study.
The FR and deposition rates of most oyster species are plastic and can exhibit wide variations both regionally and seasonally [66]. Similar to CR, the physiological trends in FR were non-linear across the tested diets, increasing to a maximum value of 2.84 mg h−1 g−1 at the ISO30 concentration, followed by an inflection and a decrease in activity at ISO40. This is directly related to the selective feeding capacity of bivalves. Oysters have several mechanisms to maximize the organic-to-inorganic ratio of ingested particles [2,3,45,67], including the rejection of excess material as PF through pre-ingestive selection [10,45,68]. Pre-ingestive selection is particularly beneficial under conditions of high TPM [45], and evidence indicates that oysters may be more effective at this selection mechanism compared to other bivalves [69]. C. gasar oysters fed with microalgae behaved as observed in other studies: as TPM increased, PF production also increased, suggesting efficient pre-ingestive selection [66,69].
The deposition capacity of C. gasar in its natural environment is considered low compared to other species in Brazil, with an average biodeposition rate slightly above 20 mg h−1 g−1 while removing particulate matter from the water column during feeding [43]. The even lower values found in the present study for the microalgae experiments (2.69 to 5.77 mg h−1 g−1) do not indicate an inefficient filtration and biodeposition process for food preferred by oysters (ISO); instead, they reflect the limitations of the equations used to calculate bivalve FRs when the POM of the food source exceeds 75% of its total composition (Table 2).
In marine environments, the proportion of particulate inorganic matter (PIM) is commonly higher than that of POM [70], with PIM levels often being three to four times higher than POM levels [71]. This is different from the scenario tested in the present study with the ISO diet. The specific condition of a high organic particle concentration alters the magnitude of FR and CR calculations, tending to reflect an underestimated physiological state. This is particularly evident in the reduced requirement for net organic selection efficiency (NOSE) as the concentration of ISO supplied to C. gasar increases. With organic particles readily available in this proportion, there may be a reduced effort to selectively sort them (Figure 2h).

4.2. Biofloc Feeding Behavior

The feeding behavior of bivalve mollusks when offered unconventional feeds such as BFT is directly related to the total particle load available in the water column. Oysters, in turn, homeostatically adjust their shell gape to preserve the integrity of the physiological mechanisms associated with the ciliary pump [72]. The finding that oysters can process BFT demonstrates that alterations in their feeding physiology are influenced by variations in particle availability and quality [34,73], which in turn modulate the production of F and PF, as well as other physiological rates.
PF production exceeding F production indicates poor utilization of available food. This can be explained by the preference of bivalves to ingest and absorb chlorophyll-rich substrates instead of more refractory organic materials such as prokaryotes, colloids, or detritus [74,75,76], elements commonly found in BFT.
The physiological responses of C. gasar within the tested BFT experimental ranges exhibited a clear inflection point for both CR and FR, indicating a non-linear relationship between these rates (Figure 3c,d). In general, FR decreases with increasing cell concentrations, indicating that bivalves regulate the amount of water cleared of particles in relation to food concentration [77]. Another response that helps explain this mechanism is NOSE, which decreased as concentration increased (Figure 3h). This supports the idea that bivalves regulate their feeding physiology rates in response to the quantity and concentration of food in their environment.
Filtration activity showed that exposing C. gasar oysters to BFT in certain concentration ranges (10–40 mg L−1) significantly altered their CR and FR. BD and organic biodeposition rate (OBDR) production by the oysters increased exponentially up to the BFT30 diet, followed by a decline at BFT40. This suggests that when these bivalves are exposed to concentrations above their optimal limit, they reduce their physiological activity (Figure 3e,g).
C. gasar are known to survive in BFT-fed systems for up to 14 days without visible morphoanatomical changes at particle concentrations up to 200 mg L−1. However, at higher concentrations or with longer BFT exposure times, changes such as gill cell hyperplasia and increased valve occlusion time have been observed [78]. Similarly, our study observed that BFT, even at concentrations acceptable for oyster survival, can induce physiological stress responses, leading to significant modifications, including changes in the morphology of F and PF.
When fed with ISO, the F tended to be more compact and homogeneous, with a dark color and a well-defined structure. This indicates more efficient digestion and better utilization of nutrients in the diet. PF were less frequent, indicating that the oyster could filter and utilize most of the ingested material. Conversely, when subjected to the BFT diet, the F had a more irregular and fragmented morphology, with variations in color and texture. PF were more abundant, indicating that the oysters rejected a larger quantity of unusable particles. This strengthens the idea that microbial flocs are not an ideal diet for C. gasar, as they require greater effort for the selection and elimination of unwanted material. This difference in BD morphology directly reflects the filtration efficiency and the diet’s impact on the oysters’ physiology.

5. Conclusions

The comprehension of the feeding mechanisms in C. gasar gives us insights into possible trends involving the utilization of this species in Multi-Trophic Aquaculture (IMTA) systems. Clearance rate (CR) and filtration rate (FR) adjusted regression of C. gasar feed with Isochrysis galbana (ISO), achieving maximum clearance and filtration efficiency on the ISO30 diet (1.01 L h−1 g−1 and 2.84 mg h−1 g−1, respectively), with a decrease in performance under the past ISO40 diet and higher density concentrations (0.39 L h−1 g−1 and 1.40 mg h−1 g−1, respectively). The concentrations of ISO in diets have a direct relation with physiological rates, implicating higher biodeposits (BDs), total biodeposition rate (TBDR), and organic biodeposition rate (OBDR).
When fed with BFT, pseudofeces (PF) production exceeded feces (F) production, indicating that this diet is unsuitable for C. gasar growth objectives in IMTA, despite higher CR and FR values with inflection points at BFT20 (5.09 L h−1 g−1) and BFT30 (14.74 mg h−1 g−1), respectively. Although no mortality was evinced on C. gasar fed with BFT, concentrations superior to BFT30 decrease the clearance of particles in the water, which may indicate that oysters prefer to diminish the feeding activity instead of dealing with low-nutritional particles. This pattern either hinders or severely limits the usage of C. gasar in IMTA systems using BFT as a sole feeding source.

Author Contributions

T.B.F., methodology, data collection, formal analysis, investigation, writing of original draft. F.L.Z., methodology, manuscript review and editing. J.P.R.F., data collection, methodology, manuscript review and editing. C.H.A.d.M.G., methodology, data collection. C.M.R.d.M., conceptualization, methodology, resources, supervision, funding acquisition, manuscript review and editing, project administration. All authors have read and agreed to the published version of the manuscript.

Funding

This study was financed by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superiror—Brazil (CAPES)—Finance Code 001 and by the Universidade Federal de Santa Catarina (249/2016). The authors also thank the Conselho Nacional de Desenvolvimento Científico e Tecnológico—Brazil (CNPq), who provided a scholarship to C. M. R. De Melo.

Institutional Review Board Statement

This study involved bivalves; studies involving invertebrate animals do not need ethical approval.

Informed Consent Statement

Not applicable.

Data Availability Statement

The datasets generated or analyzed during the current study are available from the corresponding author on reasonable request.

Acknowledgments

The authors thank the Marine Shrimp Laboratory at the Federal University of Santa Catarina for providing the conditions for the development of the current study.

Conflicts of Interest

The authors declare that they have no conflicts of interest to disclose.

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Figure 1. Overview of the acclimatization system used to develop the experiment. (1) Feed tanks; (2) feed tank aeration tubes; (3) air stone (AS15S/14LPM) of feed tanks; (4) acclimatization units (AUs); (5) submerged pumps (Aleas/Jeneca HM-5063 2000 L/H); (6) distribution PVC pipe (Ø 25 mm) of the water and feed pumped from the feed tanks; (7) silicone hoses (Ø 1.50 mm) connecting and inputting water and feed in AUs; (8) output collector PVC pipe (Ø 75 mm) of water and feed after its circulation in AU; (9) AU’s aeration hose connected to porous stone (Boyu A001).
Figure 1. Overview of the acclimatization system used to develop the experiment. (1) Feed tanks; (2) feed tank aeration tubes; (3) air stone (AS15S/14LPM) of feed tanks; (4) acclimatization units (AUs); (5) submerged pumps (Aleas/Jeneca HM-5063 2000 L/H); (6) distribution PVC pipe (Ø 25 mm) of the water and feed pumped from the feed tanks; (7) silicone hoses (Ø 1.50 mm) connecting and inputting water and feed in AUs; (8) output collector PVC pipe (Ø 75 mm) of water and feed after its circulation in AU; (9) AU’s aeration hose connected to porous stone (Boyu A001).
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Figure 2. Particle processing by Crassostrea gasar subjected to diets with increasing concentrations of Isochrysis galbana (ISO) in the laboratory. Relationship between ISO concentration and mean production of feces (F) (a), pseudofeces (PF) (b), clearance rate (CR) (c), filtration rate (FR) (d), biodeposits (BDs) (e), total biodeposition rate (TBDR) (f), organic biodeposition rate (OBDR) (g), and net organic selection efficiency (NOSE) (h). Straight lines and parabolas represent the relationships between diets and parameters. The shadow in the graph represents the 95% probability confidence interval.
Figure 2. Particle processing by Crassostrea gasar subjected to diets with increasing concentrations of Isochrysis galbana (ISO) in the laboratory. Relationship between ISO concentration and mean production of feces (F) (a), pseudofeces (PF) (b), clearance rate (CR) (c), filtration rate (FR) (d), biodeposits (BDs) (e), total biodeposition rate (TBDR) (f), organic biodeposition rate (OBDR) (g), and net organic selection efficiency (NOSE) (h). Straight lines and parabolas represent the relationships between diets and parameters. The shadow in the graph represents the 95% probability confidence interval.
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Figure 3. Particle processing by Crassostrea gasar subjected to diets with increasing concentrations of biofloc (BFT) in the laboratory. Responses include mean production of feces (F) (a), pseudofeces (PF) (b), clearance rate (CR) (c), filtration rate (FR) (d), biodeposits (BDs) (e), total biodeposition rate (TBDR) (f), organic biodeposition rate (OBDR) (g), and net organic selection efficiency (NOSE) (h). Straight lines and parabolas represent the relationships between diets and parameters. The shadow in the graph represents the 95% probability confidence interval.
Figure 3. Particle processing by Crassostrea gasar subjected to diets with increasing concentrations of biofloc (BFT) in the laboratory. Responses include mean production of feces (F) (a), pseudofeces (PF) (b), clearance rate (CR) (c), filtration rate (FR) (d), biodeposits (BDs) (e), total biodeposition rate (TBDR) (f), organic biodeposition rate (OBDR) (g), and net organic selection efficiency (NOSE) (h). Straight lines and parabolas represent the relationships between diets and parameters. The shadow in the graph represents the 95% probability confidence interval.
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Table 1. Metrics and formulae used to evaluate biodeposit production and physiological rates of Crassostrea gasar fed with Isochrysis galbana and biofloc, as determined by the biodeposition method (adapted from Gray and Langdon [38]). CR and FR were standardized to L cleared per hour per gram of dry weight (L h−1 g−1).
Table 1. Metrics and formulae used to evaluate biodeposit production and physiological rates of Crassostrea gasar fed with Isochrysis galbana and biofloc, as determined by the biodeposition method (adapted from Gray and Langdon [38]). CR and FR were standardized to L cleared per hour per gram of dry weight (L h−1 g−1).
ParameterAcronymFormula
Clearance rate (L h−1 g−1)CR(mg inorganic matter egested (feces and pseudofeces) h−1)/(mg inorganic matter concentration L−1 in seawater)
Filtration rate (total mg h−1 g−1)FR(mg inorganic matter egested (feces and pseudofeces) h−1) × [(mg total particle L−1 seawater)/(mg inorganic matter L−1 seawater)]
Feces (total mg h−1)Fmg total feces egested h−1
Pseudofeces (total mg h−1)PFmg total pseudofeces egested h−1
Organic selection efficiency (fraction)NOSE[1 − (organic fraction in pseudofeces)/(organic fraction within total particulates available in seawater)]
Biodeposition (total mg h−1) BD(total feces egested h−1) + (mg total pseudofeces h−1)
Biodeposition rate (total mg h−1 g−1) TBDR(total feces egested h−1) + (mg total pseudofeces h−1)]/(g animal dry weight)
Organic biodeposition rate (total mg h−1)OBDR(mg total feces egested h−1 × organic fraction of feces) + (mg total pseudofeces h−1 × organic fraction of pseudofeces)
Table 2. Percentage of particulate inorganic matter (PIM) and particulate organic matter (POM) from the total particulate matter (TPM) suspended in seawater for the diets used in biodeposit collection assays. no. = number of samples, s.d. = standard deviation for both PIM and POM.
Table 2. Percentage of particulate inorganic matter (PIM) and particulate organic matter (POM) from the total particulate matter (TPM) suspended in seawater for the diets used in biodeposit collection assays. no. = number of samples, s.d. = standard deviation for both PIM and POM.
DietISO10 §ISO20ISO30ISO40BFT10BFT20BFT30BFT40
PIM25%16%17.85%13.88%27.91%35.09%35.92%38.52%
POM75%84%82.15%86.11%72.09%64.91%64.08%61.48%
s.d.10.6%2.38%2.03%1.42%4.25%8.31%1.5%0.83%
no.32333233
§ Diets evaluated in experiments: ISO10 = 10 mg L−1 of I. galbana; ISO20 = 20 mg L−1 of I. galbana; ISO30 = 30 mg L−1 of I. galbana; ISO40 = 40 mg L−1 of I. galbana; BFT10 = 10 mg L−1 of biofloc; BFT20 = 20 mg L−1 of biofloc; BFT30 = 30 mg L−1 of biofloc; BFT40 = 40 mg L−1 of biofloc.
Table 3. Statistics of the equations fitted to the calculated metrics for mangrove oysters (Crassostrea gasar) subjected to diets with increasing concentrations of Isochrysis galbana (ISO). Family distribution; canonical link; a, b, and c: equation parameters; AIC: Akaike information criterion; and D2: pseudo-R2.
Table 3. Statistics of the equations fitted to the calculated metrics for mangrove oysters (Crassostrea gasar) subjected to diets with increasing concentrations of Isochrysis galbana (ISO). Family distribution; canonical link; a, b, and c: equation parameters; AIC: Akaike information criterion; and D2: pseudo-R2.
ParametricFamilyCanonical
Link		 a b c AICD2
Feces (F)GammaInverse0.57660 ***−0.00677 *-138.400.11
Pseudofeces (PF)GammaLog−2.61100 ***0.20022 ***−0.00278 **107.840.44
Clearance rate (CR)GammaIdentity0.012030.07749 *−0.00169 **38.8740.16
Filtration rate (FR)GaussianInverse1.91264 **−0.10823 **0.00190 *123.390.18
Biodeposits (BD)GammaInverse0.42741 ***−0.00672 ***-168.020.31
Total biodeposition rate (TBDR)GammaIdentity2.065280.08454-170.070.21
Organic biodeposition rate (OBDR)GammaInverse0.49423 ***−0.00825 ***-161.480.35
Net organic selection efficiency (NOSE)GaussianIdentity1.60905 ***−0.10327 ***0.00162 ***−58.9190.88
* p < 0.05; ** p < 0.01; *** p < 0.001.
Table 4. Statistical summary of parameters for mangrove oysters (Crassostrea gasar) subjected to diets with increasing concentrations of biofloc (BFT). Family distribution; canonical link; a, b, and c: equation parameters; AIC: Akaike information criterion; and D2: pseudo-R2.
Table 4. Statistical summary of parameters for mangrove oysters (Crassostrea gasar) subjected to diets with increasing concentrations of biofloc (BFT). Family distribution; canonical link; a, b, and c: equation parameters; AIC: Akaike information criterion; and D2: pseudo-R2.
ParameterFamilyCanonical Link a b c AICD2
Feces (F)GammaInverse1.61052 ***−0.08512 ***0.00125 ***153.260.48
Pseudofeces (PF)GammaIdentity2.71371 *0.14608 **-214.560.11
Clearance rate (CR)GammaIdentity−3.55163 *0.60305 ***−0.01167 ***146.700.31
Filtration rate (FR)GaussianIdentity−6.354731.41021 **−0.02362 **251.350.32
Biodeposits (BD)GaussianIdentity3.66075 *0.24178 ***-231.10.30
Total biodeposition rate (TBDR)GammaInverse0.33411 ***−0.01689 ***0.00026 **228.890.41
Organic biodeposition rate (OBDR)GaussianIdentity2.706250.13183-187.070.29
Net organic selection efficiency (NOSE)GammaInverse2.50422 ***0.04235 ***-−94.4770.23
* p < 0.05; ** p < 0.01; *** p < 0.001.
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MDPI and ACS Style

Freire, T.B.; Zacchi, F.L.; Ferreira, J.P.R.; Gomes, C.H.A.d.M.; de Melo, C.M.R. Feeding Physiology of Crassostrea gasar (Dillwyn, 1817) on Isochrysis galbana and Biofloc Diets. Fishes 2026, 11, 227. https://doi.org/10.3390/fishes11040227

AMA Style

Freire TB, Zacchi FL, Ferreira JPR, Gomes CHAdM, de Melo CMR. Feeding Physiology of Crassostrea gasar (Dillwyn, 1817) on Isochrysis galbana and Biofloc Diets. Fishes. 2026; 11(4):227. https://doi.org/10.3390/fishes11040227

Chicago/Turabian Style

Freire, Thaís Brito, Flávia Lucena Zacchi, João Paulo Ramos Ferreira, Carlos Henrique Araujo de Miranda Gomes, and Claudio Manoel Rodrigues de Melo. 2026. "Feeding Physiology of Crassostrea gasar (Dillwyn, 1817) on Isochrysis galbana and Biofloc Diets" Fishes 11, no. 4: 227. https://doi.org/10.3390/fishes11040227

APA Style

Freire, T. B., Zacchi, F. L., Ferreira, J. P. R., Gomes, C. H. A. d. M., & de Melo, C. M. R. (2026). Feeding Physiology of Crassostrea gasar (Dillwyn, 1817) on Isochrysis galbana and Biofloc Diets. Fishes, 11(4), 227. https://doi.org/10.3390/fishes11040227

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