Biofouling of the Mangrove Oyster (Crassostrea tulipa, Lamarck, 1819) Cultivation: The West African Perspective

Abstract

Oyster, Crassostrea tulipa cultivation in the West African subregion is largely carried out in estuarine and mangrove ecosystems on a small scale. These coastal water bodies generally present favorable biotic and abiotic conditions that impact positively oyster propagation. Some environmental factors including coastal flooding, eutrophication, and biofouling could hamper the culture of oysters in the wild. Biofouling is the attachment of organisms to the object of interest. It is also described as unwanted living things that occupy the same ecological niche as the desired species, causing harm by contesting for available food and living space, which is crucial in the culture of oysters where the biofoulers have deleterious effect on the growth and survival of oysters. The injurious impact of biofouling could result in en masse mortalities or reduced growth rate. Interventions to mitigate the effect will result in increased cost of operation, thereby making the business less profitable. However, existing studies in West Africa Indicate that fouling organisms may have no harmful impact on C. tulipa cultivation. Good water quality, a well-managed culture system, and adoption of best practices in post-harvest handling will enhance the production of oysters to provide food and nutrition security, livelihoods, and employments.

1. Introduction

Climate change; illegal, unreported, and unregulated (IUU) fishing; and the near collapse of some capture fisheries in Africa and the world at large have necessitated the need to opt for enhanced cultivation of fish to feed the teeming world population. More crucial is the case of Africa, in that, its economies largely depend on the climate; hence, variations in climatic conditions are likely to impact negatively its productivity and lead to the eventual collapse of the economies. Therefore, policymakers and resource managers in Africa are entreated to prioritize building climate-smart finfish and shellfish productions as well as aquaculture production to promote adaptation and mitigation measures toward achieving sustainable and resilient fisheries.

Shellfish production occurs globally; however, Africa has contributed little to global productivity [1]. This could be ascribed to low interest and investment on the part of African governments and private sectors as well as researchers when it comes to the development and culture of the resource, although shellfish production has great potential to contribute to food and nutritional security, livelihoods, and employments. According to a recent regional study on the evaluation of coastal shellfisheries covering eleven (11) West African countries, more than 300,000 mt of shellfish were landed annually, with an appraised value of USD 336 million [2]. With the appropriate policy and enforcement interventions from regional and national fishery bodies, the yield of these fisheries could be optimized to meet the growing demand of fish. Aquaculture has the potential to meet the high demand of fish as indicated by FAO [1].

Oysters in general inhabit coastal marine and brackish water systems, spanning from temperate, subtropics to tropical latitudes globally [3]. The West African mangrove oyster thrives in brackish water systems (i.e., estuaries and lagoons), normally with mangrove vegetations [4, 5, 6]. The organism largely filter-feeds on phytoplankton and substrate particles [7]; hence, no cost of feeding is incurred should the species be cultured in situ.

In the culture of bivalves including oysters in-situ, farmers would have to conduct an investigation as to whether biofouling would hamper their production to elicit the right management approach. Quayle and Newkirk [8] describe biofouling as the attachment of marine organisms, that is plants or animals, to the object of interest (collector, cultch, or the culture species). These fouling organisms usually occupy the same ecological niche as the culture species; hence, there is a possibility of competing for living space and available food [9]. Aside from fouling organisms, there are predators and disease-causing organisms that may be deleterious to oyster production. In addition to the aforementioned groups of organisms, it has been documented widely that the growth and survival of cultivated bivalves including oysters are influenced by environmental factors such as salinity, dissolved oxygen, temperature, turbidity, pH, and bulk density of sediments [10, 11].

Biofouling could be a severe problem in oyster cultivation in the tropics, according to Angell [12]. This position appears to be corroborated by Watson and Shumway’s [13] report, which indicates that biofouling on farmed mollusks could be severe and overwhelming. However, there are reports that describe the impact of fouling organisms as mere nuisance than a severe problem on oysters of the genus Crassostrea [14]. Moreover, it has been explained that biofoulers are generally stenohaline organisms unlike the Crassostrea species; hence, the impact of the fouling organisms will be neutralized when the organism is cultivated in an estuarine environment [8].

2. West African mangrove oyster species

Crassostrea tulipa (Lamarck, 1819) and C. gasar (Dautzenberg, 1891) are the two species referred to as the West African mangrove oyster in literature. There were concerns as to whether these species refer to the same organism or otherwise. As characteristic of oysters, morphological characteristics of individuals in a population are greatly modified by some local environmental factors despite their similar genotypic makeup [3, 8], hence making the use of morphological indices impractical to distinguish between the two species names. Lapegue et al. [15] settled the confusion with their study on the genetic analysis of the mitochondrial DNA of the two species, where it was inferred that C. tulipa and C. gasar refer to the same organism.

Moreover, on the decision of which specific name to adopt upon realization that the two species refer to the West African mangrove oyster, C. tulipa is chosen over C. gasar owing to the precedence of the former to the latter in the literature. Yankson [16] agreed with the above position by reporting a comprehensive discussion on the matter, thereby recommending the use of C. tulipa as the West African mangrove oyster. In that respect, C. tulipa will be used throughout this document as the species name of the mangrove oyster found in the West African coastal waters.

3. Biofouling

3.1 Description and types of biofoulers

Biofouling studies carried out in West Africa have identified tube-dwelling polychaetes, mussels, barnacles, sea anemones, hydroids, and tunicates as the main fouling organisms [5, 17, 18, 19]. In a recent publication [10], the following species were observed in an experimental culture of oysters in the Densu Delta, Ghana: Fistubalanus pallidus (barnacle), Chaetomorpha antennina (green alga), Ficopomatus sp. (tube-dwelling worm), and Brachidontes sp. (mussel); see Figure 1. F. pallidus was the dominant sedentary fouling organism. To the oyster farmer, the attachment of biofoulers to cultches or substrates and the cultured oysters may be of concern.

Figure 1.

A photograph of biofoulers on (a) an oyster shell cultch: alga, barnacle, tubeworm, sea anemone and (b) cultured oyster: mussel (Source: [10]).

3.2 Spatial and seasonal variations in fouling organisms

The biofoulers of C. tulipa are largely marine in nature. This is because the oysters inhabit brackish water systems with measurable freshwater influx, optimally with a salinity range between 35 and 5‰ [10]. In view of this, the fouling organisms tend to exhibit high abundance toward the saline end of the estuarine ecosystems. Furthermore, the biofoulers tend to thrive during the dry season when there is low rainfall or inundation at the coastal areas and vice versa.

3.3 Effect of biofoulers on cultured oysters from the African perspective

The aforementioned fouling organisms are filter-feeders, suggesting the potential of competing with oysters for food resources, except for the green alga (C. antennina), which is an autotroph. Competition is highly probable if there is no food resource partitioning, that is, difference in food particle size selection and feeding efficiency, among the epibionts. On the other hand, green algae reduce the setting surface of oyster spat, which is a huge challenge in collecting oyster seeds for stocking as well as obstructing the flow water into and out of the cultured oysters leading to low growth rate or mortality could lead to low growth rate or mortality. Studies carried out elsewhere reported some adverse impacts of the observed biofoulers on oyster cultivation. These include mortality, physical interruption to opening and closure of shells, and reduction in growth rate [14, 20]. The most lethal observed sedentary fouling organism was the tubeworm (Ficopomatus sp), which could burrow into the oyster shell.

3.4 Growth and survival of oysters on the convex and concave surfaces as well as on the top-2-collectors and bottom-2-collectors of biofouled and cleaned coconut and oyster shell cultches

Osei et al. [10] published their findings on the growth and survival of oysters on the convex and concave surfaces of biofouled and cleaned coconut shell and oyster shell cultches, where it was inferred that biofouling had no harmful effect on the growth and survival of oysters in the Densu Delta. In that study, oysters cultivated on the biofouled cultches appeared to exhibit faster mean growth rate than their counterparts on clean cultches. Nonetheless, the treatments were not significantly different except for oysters cultivated on the concave surface/underside of oyster shell cultches.

Moreover, in concurrence with the above experiment, a similar experiment to the biofouling research [10] was done on the growth and survival of oysters cultured on the top- and bottom-2-collectors of two different collectors at the Densu Delta (see the aforementioned paper for the methodology). Generally, the growth of biofouled and cleaned oysters followed a similar pattern. Panel (a) of Figure 2 presents the growth of oysters cultured on the top-2-collectors of biofouled and cleaned coconut-shell cultches. Oysters on biofouled and cleaned cultches grew up to 4.93 ± 0.11 cm SH (shell height) and 4.79 ± 0.13 cm SH with mean growth rates of 0.77 ± 0.20 cm/month and 0.74 ± 0.21 cm/month, respectively. The treatments were not statistically significant (F = 1.74, df = 4, p = 0.15).

Figure 2.

Growth of Crassostrea tulipa cultured on the top- and bottom-2-collectors of biofouled and cleaned coconut-shell and oyster-shell cultches using the suspension culture method in the Densu Delta (vertical bars indicate standard errors of means).

Panel (b) of Figure 2 shows the growth of oysters cultured on the bottom-2-collectors of biofouled and cleaned coconut-shell cultches. Oysters at these positions grew up to 5.24 ± 0.08 cm SH and 5.32 ± 0.21 cm SH with mean growth rates of 0.76 ± 0.27 cm/month and 0.79 ± 0.30 cm/month, respectively. There was no significant difference between the treatments (F = 1.74, df = 4, p = 0.15).

The third panel (c) of Figure 2 presents the growth of oysters cultured on the top-2-collectors of biofouled and cleaned oyster-shell cultches. Oysters at this position on the biofouled and cleaned cultches grew up to 5.36 ± 0.16 cm SH and 5.48 ± 0.13 cm SH with mean growth rates of 0.83 ± 0.21 cm/month and 0.83 ± 0.19 cm/month, respectively. The treatments were not statistically significant (F = 1.74, df = 4, p = 0.15).

The fourth panel (c) of Figure 2 shows the growth of oysters cultured on the bottom-2-collectors of biofouled and cleaned oyster-shell cultches. Oysters at this position on the biofouled and cleaned cultches grew up to 5.83 ± 0.12 cm SH and 5.60 ± 0.10 cm SH with mean growth rates of 0.85 ± 0.26 cm/month and 0.81 ± 0.29 cm/month, respectively. The treatments were not statistically significant (F = 0.90, df = 1, p = 0.35).

The survival of biofouled and cleaned oysters cultured at the top- and bottom-2-collectors of coconut-shell and oyster-shell cultches is presented in Figure 3. Generally, the survival of biofouled and cleaned oysters followed a similar pattern, where it declined slowly from January to June and thereafter decreased sharply from June to July 2018. The first panel (a) of Figure 3 illustrates the survival of oysters cultured on the top-2-collectors of biofouled and cleaned coconut-shell cultches. Survival of oysters on the biofouled and cleaned coconut-shell cultches was 59.49% and 50.90%, respectively, in July 2018. The difference in survival of the treatments was not significant (X² = 0.22, df = 4, p = 0.99). Panel (b) of the figure shows the survival of oysters cultured on the bottom-2-collectors of biofouled and cleaned coconut-shell cultches. Survival of oysters on the biofouled and cleaned cultches was 54.79% and 43.32%, respectively, in July 2018. The difference in survival of the treatments was not significant (X² = 0.22, df = 4, p = 0.99).

Figure 3.

Survival of Crassostrea tulipa cultured on the top- and bottom-2-collectors of biofouled and cleaned coconut-shell and oyster-shell cultches using the suspension culture method in the Densu Delta (vertical bars indicate standard errors of means).

The third panel (c) of Figure 3 presents the survival of oysters cultured on the top-2-collectors of biofouled and cleaned oyster-shell cultches. Survival of oysters on the biofouled and cleaned cultches was 53.95% and 48.10%, respectively, in July 2018. There was no significant difference between the treatments (X² = 0.18, df = 4, p = 0.99). Panel (d) of Figure 3 shows the survival of oysters cultured on the bottom-2-collectors of biofouled and cleaned oyster-shell cultches. Survival of oysters on the biofouled and cleaned cultches was 49.68% and 46.8%, respectively, in July 2018. There was no statistical significance in the survival of the treatments (X² = 0.06, df = 4, p = 0.99).

Oyster growth and survival on biofouled and cleaned cultches at the top and bottom collectors showing no significant difference could be a result of a comparable community of biofoulers on the top and bottom collectors, possibly, given the shallow depth of the culture site in the Densu Delta (approximately 0.61 m high tide).

The lack of effect of biofouling on the growth of oysters on coconut-shell cultches is consistent with earlier findings [19] where the authors observed no effect of biofouling on C. tulpa in three different lagoons, namely Benya, Nakwa, and Jange. Elsewhere, a lack of effect of biofouling on growth and survival has been documented for C. rhizophorae, C. virginica, and C. gigas as reported by [21], [22], and [23], respectively. The observation of no impact of biofouling on growth and survival of oysters could be attributed to a number of factors, that is, commensalism, food-resource partitioning stimulated primary production by some biofoulers to offset the limited food resources [21, 22, 24]. It has been reported that growing oysters can tolerate a considerable degree of biofouling before becoming harmful enough to necessitate some form of control intervention [14].

A positive effect of biofouling has, however, been reported for oysters [9, 24]. The underside of suspended or floating collectors or substrates has been found to be the preferred surface for epibionts including oysters [8, 19, 25]. Tanita et al. [1961, as cited in 9] reported that the later attachment of biofoulers could stimulate shell growth in oysters, as an attempt in competing for space.

Quite a considerable number of works have reported on the devastating effect of biofouling on cultured bivalves, including oysters [11, 12]. According to Arakawa [9], biofoulers like barnacles and mussels are known to engage in severe competition with cultured oysters, resulting in reduced growth rate. Moreover, biofouling has been reported to cause decline in growth rate and mortality in oysters [11] and mussles [26, 27]. Biofouling could have financial implications on the culture, in that, it could reduce the market value especially for half-shell trading, as a result of unsightly blister shells [23] as well as increased operational cost in preventing or treating biofouling [20]. The increase in operational cost due to biofouling of oysters could be up to 30% [28].

It is rational to investigate the effects of fouling organisms on oysters in situ before any mass cultivation of the species. In the case of deleterious effects of epibionts, control measures must be put in place to reduce or get rid of the biofoulers. Three strategies comprising avoidance, prevention, and treatment have been described in reducing fouling organisms [29]. In most cases, farmers employ some treatment measures when the effect of biofouling is harmful, which results in increased operational cost. Efficient, cost-effective, and environmentally friendly approaches used in treating fouling organisms in situ include exposure to freshwater [30] and air drying [31] on small scale farms. Other methods like application of heat [32] and use of organic acids and bases [33] could be used.

4. Conclusion

There is ample evidence that fouling organisms may not have harmful impact on C. tulipa cultivation in the estuarine mangrove ecosystem; therefore, there is no need to implement preventive or treatment measures. However, a farmer may want to avoid, prevent, and employ treatment approaches if the target is on half-shelf trading to avoid the unsightly appearance of oyster shells, which has implications of reducing the market value of the produce.

Given the coastal degradation and biofouling in some coastal water bodies, intensive culture of C. tulipa will be ideal to avoid the effect of contaminants and fouling organisms.

Acknowledgments

Our sincere thanks go to the USAID/UCC Fisheries and Coastal Management Capacity Building Support Project for the award of scholarship for the study under the directorship of Professor Denis Worlanyo Aheto of the Centre for Coastal Management (CCM), Africa Centre of Excellence in Coastal Resilience (ACECoR), University of Cape Coast (UCC) for providing the enabling environment for the research special thanks go to Prof. Denis W. Aheto, Director of Centre for Coastal Management (CCM)/ African Centre of Excellence in Coastal Resilience (ACECoR) at the University of Cape Coast for offering the enabling environment for the research to come to fruition.

Conflict of interest

The authors declare no conflict of interest.

Notes/thanks/other declarations

I (Dr. Isaac Kofi Osei) would like to express my profound indebtedness to the late Prof. Emeritus Kobina Yankson, Prof. Edward Adzesiwor Obodai and Prof. Denis Worlanyo Aheto for offering professional guidance and support. Edward Adzesiwor Obodai for supervising the study, both of the Centre for Coastal Management/African Centre of Excellence in Coastal Resilience and the Department of Fisheries and Aquatic Sciences (DFAS), University of Cape Coast for their professional guidance, encouragement and support during my PhD study. I am eternally grateful to them.