Do Sustainably Reared Marine Sponges Represent A Potential New Product in Aquariology? A Citizen Science-Based Approach

Abstract

Marine sponges have historically been targeted for different purposes, mainly as bath sponges or more recently as a source of bioactive metabolites. However, their use as ornamental species for aquariology is less thoroughly studied. In light of the rise in the importance of sustainable production systems and to valorize the biomass obtained from them, this work assessed the market potential of sustainably reared marine sponges in Italian aquariology. Information was obtained by means of an anonymous questionnaire distributed using social media and printed QR codes targeting Italian aquariophily groups. A total of 101 people from almost all Italian regions participated in the study. Among the people with marine aquariums, almost two-thirds had marine sponges (obtained mainly from fishing discards and trusted shops), and those without them stated that there was no availability in the specialized shops. However, when people were asked about a hypothetical change in purchase intention or frequency of these invertebrates, 68.3% of the respondents showed a positive attitude toward the idea of acquisition. This study constitutes the first preliminary assessment of the valorization potential for sustainably cultivated sponges as ornamental species, which shows a promising prospective in the Italian aquariology sector.

1. Introduction

Since Egyptian civilization, marine sponges have been harvested and used by humans [1]. The method of harvesting the biomass and the commercial interest in it have changed over the decades (i.e., from collection to cultivation and from cosmetics to production of bioactive secondary metabolites [2]); however, these marine invertebrates still persist in the economy of some countries as an alternative source of income, from “bath sponges” in the Mediterranean (e.g., Greece, Italy, Croatia, Cyprus or Tunisia) and underdeveloped countries (e.g., Micronesia or Zanzibar) to ornamental species for aquariology, especially in the USA (reviewed in [3]).

Although there is an absence of specific regulations on ornamental invertebrate species trade except those subjected to a protection regime (e.g., European Habitat Directive, CITES), the exploitation of wild stocks to support this business sector is not environmentally sustainable or ethical. This reason has increased interest in developing pilot production systems aiming to reduce harvesting pressure on natural stocks and to provide the amount of biomass required for various other purposes. Thus, since the end of the 18th century [4], numerous attempts have been made to cultivate sponges and reduce costs.

Among the systems proposed, Integrated Multi-Trophic Aquaculture (IMTA) is a sustainable and environmentally friendly polyculture that combines the rearing of fed species (e.g., fish or shrimp) and extractive species that use waste from the fed species for their growth and does not require additional dietary inputs (such as macroalgae to remove inorganic substances and filter-feeding or detritivorous invertebrates to remove the dissolved and particulate organic component). In this context, marine sponges emerge as potential bioremediators of fish farming-derived organic matter, as they have a high capacity for filtration and retention of dissolved and particulate matter between 0.5 and 50 µm in diameter (e.g., [5,6,7,8]). As a result, up to 200% growth of biomass in just a few months has been obtained, with some Mediterranean species reared in these systems (e.g., [9,10,11,12,13,14]). Despite these impressive results, their inedibility for humans hinders the profitability of the reared by-product and slows down its implementation and the development of the aforementioned systems. Nevertheless, when these bioremediator by-products have a potential valorization, such as aquariology, the higher profitability of the system, the possible reduction of effluent fees, entry into new markets, and greater public and governmental acceptance have been described as favorable elements for its implementation [15]. In this sense, IMTA may increase revenues by up to 4% and reduce the natural and market risks of the aquaculture sector, making conversion from monoculture to polyculture a worthwhile undertaking [16]. On the other hand, this conversion has been shown to positively affect local benthic communities by promoting higher species recruitment that increases diversity and improves the ecological quality status of these systems, therefore reducing its environmental impact [17]. Marine ornamental aquaculture can play a crucial role in achieving a balance between economic viability and environmentally friendly practices. In fact, today less than 5% of marine ornamental species are farmed and even fewer are available in mass production to supply the growing demand of this business [18]. The rest come from natural stocks that are probably already overexploited, as an excess of specimens must be harvested to offset all losses along the supply chain. These unsustainable practices may lead to the collapse of this industry, as is currently known, so new policies arising from this problem may restrict the harvesting and sale of marine animals [18]. By then, aquaculture alternatives would have to be ready since a drastic decrease in the availability of wild organisms would lead to an increase in demand that could only be met by farmed specimens [18]. To this end, there is a great need to better understand the global marine aquarium trade as well as the risks and benefits of its aquaculture industry. At the same time, the focus should be on the potential market for its products and the reduction of its production costs. To do so, market analysis, optimization of farming methodology and increased knowledge of key biological aspects (such as reproduction, feeding and diseases) are necessary [18]. In this sense, IMTA with sponges can represent a sustainable and environmentally friendly specimen supply able to minimize the impacts of wild ornamental organisms’ collection; indeed, they may potentially be employed for the restoration of depleted ornamental populations [19].

The reef aquarium market is expected to continue growing worldwide at an annual rate of more than 10% to reach a value of USD 11 billion by 2028 [20]. The sponge and coral trade alone accounted for USD 171 million in 2020 [21]. In Europe, the pet-related industry is an important sector of the economy that is growing mainly due to the increase in the number of pets, and among these, there are more than 16 million aquariums, of which fish in Italy account for almost 50% of pets [22]. The use of questionnaires to assess the origin and quantity of ornamental species sold for aquariology has been shown to reveal possible underestimates in data published by official databases, which would provide necessary information to control the trade market [23]. In fact, the current supply chain of ornamental species is long, with too many intermediaries that hinder the traceability of the organisms traded and their regulation for the sustainable management of the natural communities from which they originate. The current methods used for this purpose are not adequate due to their invasiveness and non-destructive techniques such as bacterial barcoding have been proposed for their traceability [24]. Marine sponges and IMTA systems would be a sustainable solution to the problems described above, thanks to being holobionts and their regenerative capacity (which facilitates the use of traceability techniques) and the reduction of the number of intermediaries between the farmers and the client, respectively.

Overall, the exchange of cultured aquarium ornamental species seems a profitable opportunity for the development of valorization chances for specimens supplied from polyculture facilities. In this context, we conducted a survey to understand the interest of Italian aquariologists in sponge specimens and their willingness to purchase them from sustainable farms.

2. Materials and Methods

2.1. Design

The intended information for the study was obtained by means of an anonymous questionnaire organized into four sections (Appendix A and Appendix B). The first three questions evaluated general knowledge on marine sponges, their filtering ability and IMTA systems, and were the same for every participant; the second section targeting aquariology habits followed a “conditional branching” path (represented in Figure 1) with which the following data was obtained: type of aquarium, the presence of sponges or the reasons for their absence and the method of acquisition, geographical origin and frequency; the third section consisted of five sustainability questions, regarding environmental concern, awareness of own actions environmental impact, willingness to make sacrifices for it and the im-portance of sustainable production systems and the proximity between production and sale locations. Section four collected sociodemographic information about participants, specifically, gender, age, education level, and region of residence, with the latter being the only mandatory information.

All questions in the first two sections were closed-ended in order to ease respondents’ experience and obtain quantifiable data, in some of them with either an open answer or an “I don’t know” (IDK) option. Information from section three followed a 5-point Likert scale (from 1 = “not at all” to 5 = “completely”). After parts I and II, a short paragraph with corresponding general information and images was added. At the end of parts II and III, a hypothetical question about purchase intention was proposed to evaluate a possible market. After part IV, a final open box was added to express any information or suggestions. After its preparation using Google forms, the survey was distributed on March 2023 using social media, such as Facebook, Instagram, WhatsApp and Telegram, in which Italian aquariophily groups were targeted. A printed QR code was also distributed among local pet stores and the University of Bari Aldo Moro, Bari, Italy. The answering period ended on September 2023 after 6 months.

2.2. Data Analysis

The possible relationships between sociodemographic status (regions of residence grouped in northern, central and southern areas and education level) and all information gathered in parts I, II and III as well as the final question were examined by univariate chi-square (χ²) analysis using R 4.3.0 (R Foundation, Vienna, Austria). Adjusted Standardized Residuals were used to detect over- or under-represented proportions in the case of significant relationships.

2.3. Privacy Considerations

At the beginning of the questionnaire, information about funding projects and data treatment procedures was available. Being an online questionnaire posted on social media groups (or QR format) and therefore the accession being voluntary, it was considered that by answering the questionnaire completely anonymously, they agreed to participate in the study.

3. Results

3.1. Sociodemographic Characteristics and General Knowledge

A total of 101 people from almost all Italian regions participated in the study (Figure 2), mainly from the northern (Lombardy, Liguria, Veneto and Emilia-Romagna) and southern (Apulia) areas, with a mean age of 38 years (SD = 14.22). The gender ratio was 2:1 (66% male, 33% female), while the education level showed equal frequencies between respondents who graduated and did not graduate from university (49 and 51%, respectively). Interestingly, although almost 90% of people were aware of marine sponges and their filtering activity, only 21.8% knew what IMTA systems were and how they worked, regardless of their education level (χ² = 1.149, p = 0.284).

3.2. Aquarium Matters

In the data retrieved from part II (represented in Figure 3) and despite trying to address the questionnaire to people with aquariums (and preferably marine aquariums), 34.7% of the respondents stated that they had none and 34.6% that they had freshwater aquariums. Of those with marine aquaria (30.7%), 61.3% said they had sponges in their aquarium, acquiring them mainly once a year or less (89.5%). Ownership of marine aquariums was proportionally higher in the central area, where 75% of respondents confirmed their presence at home (Figure 4A; χ² = 15.462, p = 0.004).

In terms of where the sponges come from, discards from professional fishing dominate (42.1%), followed by aquarium shops (36.8%), private aquarists (10.5%) and personal collection and online shopping (both 5.3%) (Figure 3). A respondent noted that some sponges arrived from purchasing rocks matured in other aquariums that, at that time, were undeveloped and thus unnoticeable. These methods of acquisition varied among areas (χ² = 20.571, p = 0.008), with trusted shops being the option selected significantly more often by the interviewees from the North (100%) (Figure 4B). Discards from commercial fishing accounted for 66% of the responses from the southern area, and online shops and private individuals appeared as an acquisition method only among respondents from central regions (Figure 4B). At the same time, when sponge keepers were asked if they knew the geographical origin of the sponges they owned, more than half (58%) said they did not (Figure 3). All of those who answered positively to the question (42%) pointed to the Mediterranean as the origin of their sponges, some of them specifying regions such as the Northern Tyrrhenian, Ionian, Adriatic or Aegean Seas. Just one interviewee who declared a trusted shop as the main source of sponges mentioned sponges reared in diverse geographical locations as their general origin. This knowledge of the possible geographical area of provenience of traded sponges significantly varied among Italian regions (χ² = 8.550, p = 0.014), as no northern respondents knew the origin of their individuals, compared to 83.3% of southerners, who in fact did (Figure 4C). In central regions, the proportions appeared to be equal (50% for both Yes and No answers).

Those who did not have sponges in their marine aquaria (29%) stated that the reasons for this were mainly the impossibility of acquiring them from trusted shops (58.3%) as well as lack of knowledge about them and voluntary disinterest (25 and 16.7%, respectively, Figure 3), which varied among regions (χ² = 9.578, p = 0.048). The southern regions were dominated by lack of availability and the central regions by lack of interest, the latter reason being registered only among respondents (Figure 4D). Nevertheless, in the last question of this part regarding a possible purchase intention proposed to aquariophilists unfamiliar with marine sponges (owing to the lack of either a marine aquarium or knowledge), 82.2% of the people showed a positive attitude towards the proposed idea. Geographic area did not influence these results (χ² = 1.473, p = 0.831), with a mean positive answer proportion of 79.77% (SD = 5) for all three areas.

3.3. Sustainable Awareness

In the sustainability section, the vast majority of respondents declared that they were concerned and willing to make sacrifices for the environment (95 and 84%, respectively; ≥4 in Figure 5), although 37% were hesitant about the impact of their actions on the environment (<4 in Figure 5). This dubious attitude slightly differed among areas (χ² = 6.053, p = 0.048), with central regions showing a higher proportion of these respondents (66% against the 36.1 and 8.8% recorded from the north and south, respectively).

Regarding production systems, almost all of them (92%) agreed on the high value of using sustainable systems and 77% attributed high importance to the geographical proximity between the place of production and the sale of the products (≥4 in Figure 5). Nevertheless, the latter results had a strong geographic component (χ² = 27.989, p < 0.001), as almost 70% of respondents from the south assigned moderate or less importance to the proximity compared to the 16.7% from each of the other regions.

3.4. Final Question: Effect of Sustainability on Hypothetical Purchase Intention

After part III, in the final question on the hypothetical purchase intention or frequency change regarding sponges reared in sustainable production systems such as IMTA (represented in Figure 6), only 17% of the total number of respondents showed no interest, of which 76.5% did not confirm the presence of marine sponges (either because they lacked marine aquariums or sponges in them). On the other hand, of the 2 out of 3 respondents who would be willing to acquire them (68.3%), 17.4% were people who currently had sponges (mainly from aquarium shops) and 10.1% did not have them due to unavailability or lack of knowledge, and the rest were people without an aquarium or with a freshwater one. Of the respondents, 15% were hesitant about the market possibility proposed, being predominantly people without a marine aquarium (73.3%). Although not significant, geographic area slightly influenced these results (χ² = 8.4, p = 0.078), with people from the central area being rather less willing to buy sponges (41.67%) and those from the south being the most willing (76.92%) (Figure 4E).

4. Discussion

Marine sponges represent emerging by-products of IMTA systems, although their profitability is still under development [3]. Their most promising economic potential concerns the ability to produce bioactive metabolites that have been interesting in different industries over the last decades; nevertheless, their market is not yet well established owing to the so-called “biomass supply problem”. Collection of ornamental species for aquariology is equally based on natural stocks that remove millions of marine organisms annually from local ecosystems, with the tropical countries of Asia and the US being the largest exporters and importers, respectively [25,26]. In this context, sponge farming (and, more specifically, IMTA systems) could represent a suitable alternative that has proven to be effective with bath sponges and affects the local economy positively (e.g., [27,28]). Therefore, rearing ornamental species for aquariology represents another valorization route that may benefit from this sustainable production method and the present paper has proven so.

The designed questionnaire and different spreading social platforms enabled the researchers to obtain 101 responses from almost all of the Italian territory (Figure 2). The locally spread physical format (i.e., QR code) has also proven to be effective, being responsible for the significantly higher amount of answers received from Apulia. Even in inland regions, sponges and their filtering ability are well known among Italians (88%). IMTA systems, despite being an increasingly topical research issue in the aquaculture sector with more than 160 research items in the last 15 years (using the “Integrated Multitrophic Aquaculture” term in Scopus, accessed on 11 September 2023), were known to only 1 out of 5 respondents, which highlights the need for the development and communication of this sustainable approach.

Part II showed interesting results regarding the method of acquisition of sponges and the reason for their absence. Fishing discards were identified as the source of choice for almost half of the sponge owners, followed by purchases from local stores (42.1 and 36.8%, respectively, Figure 3). These results show a geographic component, with discards being more common in southern coastal regions and stores being the option selected by all of the aquariophilists surveyed from the north (Figure 4). In relation to this, the methodology of obtaining sponges seems to be related to the knowledge of their origin. Since most of the sponges came from fishing discards in the south, among respondents of this area, their origin was significantly better known than in the north, where 100% of the holders bought them in stores and none of them knew their origin. These results denote a lack of interest or information about the animals sold in aquarium stores. In this sense, more sustainable and local methodologies for their collection would improve the knowledge of aquariophilists about the product and the traceability of the organisms for a more sustainable management of the natural communities from which they originate. On the other hand, unavailability in stores is the main reason for the absence of Porifera in aquariums at the national level, comprising 85.7% of responses from the southern regions. In fact, of the more than 600 aquarium stores registered in Italy (according to [29]), almost half of them are located in the 8 northern regions, doubling the number of stores in the south.

The vast majority of respondents showed a high sustainable awareness valuing the proximity of the products, their sustainable production and even being willing to make sacrifices for the environment (Figure 5). In fact, 68.3% of respondents would change their intention/frequency of purchasing sponges if they came from sustainable systems, such as IMTA (Figure 6). Although about a third of them were people without aquariums and therefore without the knowledge of the effort involved in maintaining an aquarium in optimal conditions. What is most encouraging for the proposed potential market is (1) that the absence of these animals in the marine aquariums of people willing to purchase them (left path in Figure 6) could be solved with awareness and greater availability of sponges in stores and (2) that the respondents who showed doubts or denied the change of attitude towards the proposed hypothetical market (center and right paths in Figure 6) are mainly people who currently do not pay for them and therefore are not customers of the industry.

The appreciation of non-edible biomass from IMTA systems is a pending issue that slows down its globalization and implementation. However, in Italy, non-conventional biomass cultivated in an IMTA system, such as the polychaete worm Sabella spallanzanii, has been shown to obtain similar growth results to conventional feed when used as a food substitute for tropical aquarium fish [30]. In addition, some of the genera and species proposed by Calado [19] as potential ornamental sponge species have already been successfully reared in Italian IMTA systems (i.e., Ircinia spp. and Aplysina aerophoba [3]), supporting aquariology as a promising market for the by-products of these farms.

For example, there are a total of nearly 29,900,000 aquarium fish in Italy [22]. To make the calculations easier, considering that one out of 10 is marine [31] and placing 7 individuals per tank [22], this would mean the presence of 427,143 marine aquariums in Italy. Assuming one of them per person and applying the percentage of people with marine aquariums interested in buying sponges calculated in the present study (64.5%), there are more than 275,500 aquariophilists willing to purchase these sustainably reared animals. With prices of around EUR 10 per individual (e.g., Acquariomania.net and Exoticfarm.shop, (21 January 2024)), although underestimated compared to other national and most US prices) and a calculated average purchase rate of once a year (Part II of the present work), its estimated market value reaches almost EUR 3 million per year, which, added to the fact of its low production cost [32], would be a powerful source of income. These quick calculations exclude large public aquariums (where the number of aquariums, their size and the number of individuals per tank are greater) and other possible uses of the reared sponge biomass (such as bath sponges and bioactive compound production), which would be a fundamental market of these systems.

The overexploitation of marine resources for ornamental species collection in European waters poses a potential threat to marine ecosystems, especially in the absence of dedicated regulatory measures at the European level. Porifera, or sponges, are filter feeder organisms representing one of the dominant and most abundant components of benthic communities in the world’s oceans. They are considered “living hotels” because of the great variety and abundance of endobionts belonging to other taxonomic groups, including cnidarians, polychaetes, crustaceans and echinoderms, playing a fundamental role in increasing the biodiversity of ecosystems [33,34,35]. Historically, the systematic collection of sponges has meant a critical reduction in their natural stocks, such as the bath sponge Spongia officinalis (considered endangered [36]) or the pharmacologically interesting Dysidea avara (collected for its avarol content, a powerful bioactive compound [37]). However, despite the described positive ecosystem services provided by these animals and, therefore, the risk of reducing their populations, there is controversy related to the theoretically sustainable hand-collection of specimens, a study concluding that this practice probably has a negligible impact on certain communities [38]. In this context, in view of their economic potential, trials have been carried out to define the methodology and improve the yield of biomass production (either for bath sponges or for bioactive compound synthesis), which have promoted the development of the aquaculture of these animals (e.g., [9,13,39,40]).

Nowadays, however, the major threats to these animals are both direct (e.g., in the form of physical damage from trawling, oiling or deep-sea mining) and indirect (e.g., epidemic events, pollution, increased sedimentation from bottom fishing or climate change) [35]. Therefore, for some years now, the protection of their most vulnerable populations to the aforementioned direct activities, although still scarce, has been encouraged [41]”.

To protect benthic ecosystems and address this lack of regulation, it is crucial to propose alternative sustainable solutions and legislative measures for effective sector regulation. According to Wood [42], a comprehensive understanding of the resource and its dynamics, including breeding cycles, recruitment times and growth rates of targeted species, is essential for selecting an appropriate management strategy. Considerations should encompass the issuance of harvesting permits, establishment of certified wholesalers, adoption of suitable harvesting equipment and methods, implementation of size limits for harvested species, species-based quotas, protection of rare species and the introduction of harvesting seasons. Ultimately, the cultivation of commercially valuable ornamental organisms emerges as a sustainable alternative to harvesting from natural populations [42]. The suggestions presented in this research aim to promote the value of sponges cultivated in multi-trophic aquaculture systems as sustainable ornamental species, offering economic opportunities and benefiting local communities.

5. Conclusions

With the demonstrated capacity of IMTA systems to cultivate marine sponges and the social acceptance detected in this preliminary study, it has been shown that these invertebrates can be used as ornamental organisms in the aquariology sector. In particular, both in the north because of its demand and in the south because of the lack of supply, Italy could be a hot spot for the successful implementation of the proposed sustainable systems, which at the same time would reduce pressure on natural communities and support the local economy.