There is a globally unmet demand for the luxury seafood product, sea urchin gonads (termed roe by the industry or uni in Japan). This is largely driven by the Asian market, but urchins are grown, sold, and consumed across the world, including regions such as North America (Eddy et al., 2015; Sun and Chiang, 2015; Stefánsson et al., 2017). Regional demand can range from local restaurants serving uni raw as sushi or incorporating it into a sauce served with cooked pasta, to regional processors who can remove and prepare uni into aesthetically appealing packaged trays in preparation for shipping. Marketable uni should ideally have a firm and non-gamete-shedding texture and bright orange or yellow in color with a pleasant sweet-salty flavor (Sun and Chiang, 2015). Sea urchins have been wild harvested for at least six decades, with highest yields produced during the times when sushi became popular during the 1960s, however, most catches dropped dramatically following this period due to overexploitation (Stefánsson et al., 2017). Harvesting pressure to meet market demand led to over 40 species populations to overexploitation (Andrew et al., 2002; McBride, 2005) and there is pressure to identify other candidate species and to also rely more heavily on aquaculture production to meet this demand. In recent years new or emerging species have included the European Sea urchin species, Psammechinus miliaris (Suckling et al., 2011; Suckling et al., 2018; Suckling et al., 2020a; Suckling, 2021) and Sphaerechinus granularis (José et al., 2019), but there remain many species which have not yet been investigated for market potential.

The Atlantic purple sea urchin, Arbacia punctulata (Lamarck, 1816) is a common model species for toxicology studies (Ward et al., 2006; Nelson et al., 2010; Barron et al., 2020) but is not fished commercially at all and little is known about its market potential. It is a regular echinoid with a similar morphology to other echinoids which are currently commercially exploited, and has a wide distribution in the western Atlantic Ocean, from Massachusetts through the Gulf of Mexico and along the coast of Central and South America towards Belize, from the low tide line down to approximately 230 m depth (Kier, 1975; Serafy, 1979; Hendler & Pawson, 2000). A combination of literature reviewing and pilot sampling (Suckling, unpublished data) of sea urchins collected in the Cape Cod and Narragansett Bay regions (Rhode Island, USA) have highlighted that A. punctulata are gonochoristic and generally spawn in the Summer (Harvey, 1956) with firm non-gamete-shedding gonads during the austral winter indicating a lack of distinct gametes (Suckling et al., 2011). While the broad reproductive stages for A. punctulata need further investigation this indicates a similar reproductive stage pattern to many other temperate/sub-tropical sea urchin species (e.g. Psammechinus miliaris and Paracentrotus lividus; Byrne, 1990; Kelly et al, 2000) where firm roe are marketable within the late fall through to early spring months ( Figure 1 ). Pilot sampling of sea urchins sampled Vineyard Sound (Massachusetts) and Narragansett Bay (Rhode Island, U.S.A) also identified that A. punctulata uni were small and undesirable in market color indicating that fishing alone would not meet market demand (Suckling, unpublished data) and is typical for animals found within habitats with low food supplies (Hughes et al., 2006; Symonds et al., 2009; Suckling et al., 2011). Their omnivorous feeding habits on a range of animal and algal food sources (Lawrence, 1975; Wahl & Hay, 1995) indicate a strong ability to digest various compounds. This therefore strongly suggests that intervention using formulated feeds could be feasible, an approach used to influence and yield uni with marketable attributes for some existing commercially exploited sea urchin species (e.g. large size, firm texture and appealing bright colors; Robinson et al., 2002; Pearce et al., 2002; McBride et al., 2004; Shpigel et al., 2005; Symonds et al. 2007; Suckling et al., 2011).

A proprietary diet specifically designed for sea urchins has been emerging in recent years. This was initially developed by and referred to as the ‘Nofima’ diet [Norway (e.g. Siikavuopio and Mortensen, 2015)], but has since been globally licensed to Urchinomics (www.urchinomics.com) and undergone further formulation developments and is now a different diet. This diet has shown extremely promising results, yielding marketable uni in wild collected sea urchins collected to protect diminishing kelp forests within as little as 8-12 weeks. At present this feed is not available as an off the shelf diet with selective commercial agreements with the company required. Determining the suitability of alternative off the shelf options would therefore be valuable for growers. A range of available high protein (e.g. fishmeal and or soya bean protein sources) formulated feeds designed for other aquaculture species such as salmon have shown to be palatable by many sea urchin species and to yield large uni (Brown and Eddy, 2015; Fernandez and Boudouresque, 2000; Suckling et al., 2011). These feeds often incorporate natural carotenoids such as astaxanthin to promote the red/pink salmon flesh color prized by consumers, but these do not always translate well to promote marketable uni colors in sea urchins (Suckling et al., 2020b), often instead needing β-carotene supplementation through the provision of macroalgae (e.g. Shpigel et al., 2005; Carrier et al., 2017) and microalgae (McLaughlin and Kelly, 2001; Shpigel et al., 2006). Commercially available proprietary formulated feeds designed for Tilapia (e.g. Zeigler) incorporate both high protein inclusions as well as algae which would likely include desirable carotenoids which could positively influence uni color (Shpigel et al., 2005; Suckling et al., 2020b), but these remain untested in sea urchins to date.

With species such as A. punctulata where the effect of formulated feeds on uni development is currently unknown, some of the initial steps are to determine palatability and whether uni size and color can be influenced. Pilot trials indicate that the above listed formulated feeds are palatable and ingested and processed by A. punctulata (Suckling, unpublished data) and therefore the next step is to determine whether prolonged feeding can enhance uni marketable attributes. The aim of this study was to therefore assess the potential commercial prospects of A. punctulata by providing a range of food treatments for a period of up to 3 months, a period known to be sensitive enough to measure nutritional influences on the development of the uni (e.g. Suckling et al., 2011).

This study highlights that the gonad index of A. punctulata can be positively enhanced using pelleted feed which is in agreement with a wide number of studies (e.g. de Jong-Westman et al., 1995; Fernandez et al., 1997; Lawrence et al., 1997; Akiyama et al., 2001; Robinson et al, 2002; Suckling et al., 2011; Zupo et al., 2018). While there was no significant improvement on marketable gonad colors, there was a subtle increase which highlights potential to manipulate gonad color through diet in this species and would need further trials to elucidate this. The colors of the uni were a darker range of colors (i.e. dark shades of purple, brown, red, orange and yellow) than the market would typically prefer from established marketable species (Suckling and Zavell, personal observation). At present we do not know for certain whether this species can achieve the familiar and preferred market uni colors typically being bright orange or yellow. But some individuals did exhibit darker pink/cream/red colors which have been classed as acceptable to the European market for P. miliaris and may provide an interesting new color aesthetic experience for the sushi market (Suckling et al., 2011). It is possible that the carotenoids included within these diets might not be compatible for biochemical conversion to color in the uni, and this has been shown to differ across species (Tsushima et al., 1997; Suckling et al., 2020b). Further work assessing the influence of differing carotenoids included into a base diet such those described by Robinson et al. (2002) and Suckling et al. (2011) would be required to determine this. Despite the darker uni colors, this study highlights that there was a clear influence of diet on gonad coloration. Additionally, the uni were observed to be at reproductive stages which would be conducive to typical late harvesting periods ( Figure 1 ), thus showing that A. punctulata has potential for the market.

While it was clear that diet could influence and enhance gonadal growth in A. punctulata, in comparison to commercially exploited or emerging species, this growth was markedly slow (e.g. de Jong-Westman et al., 1995; Fernandez et al., 1997; Lawrence et al., 1997; Akiyama et al., 2001; Robinson et al, 2002; Suckling et al., 2011; Zupo et al., 2018). This could in part be explained by the collection method, scallop dredging. During this collection method, the harvested animals are caught within a mesh collection bag and dragged some distance with other dredged materials which can incur injury and high stress. Scallop dredging has been used in the past to collect Strongylocentrotus droebachiensis for the US market with some success (Scattergood, 1961), but the animals were sold and consumed within a short period of time after harvesting, thus omitting the longer-term impacts of this method. Dredging is used in other sea urchin fisheries across the world (e.g. Greenland and Iceland) but can be modified to reduce the stress and damage on the harvested sea urchins (James and Hannon, 2017). It is therefore possible that the harvested A. punctulata could have been highly stressed and therefore physiologically compromised and/or needing to allocate energy towards repair, despite efforts to use only healthy intact and undamaged looking animals in this study. Although survival data was not significantly different, this could also explain the mortalities recorded for both Urchinomics diet treatments ( Figure 2 ), however, only a single animal died in a replicate tank thus representing 10% of that population and therefore was overall a low number. The Urchinomics diet has shown strong unanimous successes in its use (www.urchinomics.com) and would unlikely have been the cause of mortality in this trial.

Slow gonadal growth could also be explained by the geographical distribution and sourcing of this species. These animals were collected from and reared within the coldest northernmost range of their natural distribution (Serafy, 1979). This study was also carried out during the seasonally low winter temperatures ( Table 2 ) meaning that this species was likely to be functioning within its lowest metabolic scope (Clarke and Johnston, 1999; Addo-Bediako et al., 2000; Suckling et al., 2020a). In turn the collection method or cooler temperatures could have limited the carotenoid utilization from the diets thus leading to the darker uni colors. Therefore, it is recommended that more trials be conducted using less impactful harvesting methods and within warmer temperatures than those used in the current study and/or across longer periods of time and using different carotenoids (e.g., lutein and zeaxanthin; Suckling et al., 2011; Suckling et al., 2020b) to determine whether gonad growth and color in A. punctulata can be further enhanced. While these remain the most likely factors of influence, there is also the possibility the diets provided within this study were not optimized for this species, thus warranting further investigations on differing food supplies.

Numerous sea urchin species (e.g. Arbacia lixula, Strongylocentrotus droebachiensis, Psammechinus miliaris), have been shown to be resilient to projected variability in ocean conditions expected within the next few decades (e.g. alteration to CO₂ and temperature; Wangensteen et al., 2013; Suckling et al., 2014; Ross et al., 2015). The cellular processes of acid base buffering, that counteract increased CO₂, can be achieved within 7-10 days (Stumpp et al., 2012) and they have shown to be reproductive and marketable under medium to long term exposures to laboratory simulated climate change scenarios (Dupont et al., 2013; Suckling et al., 2014; Suckling et al., 2020a) across several generations (Suckling, unpublished data). Therefore, the production of sea urchins presents a potential sustainable option for growers, and to support this industry it is important that new (e.g. A. punctulata) and emerging species (e.g. P. miliaris, and S. granularis;Suckling et al., 2011; Suckling et al., 2018; José et al., 2019; Suckling et al., 2020a), are identified and investigated. This mitigation strategy of diversifying production (i.e. with tolerant sea urchin species) is increasing in interest and uptake by growers in the US (Reid et al., 2019) allowing for contingency against losses already being observed from climate change (e.g. shellfish production; Barton et al., 2012; Clements & Chopin, 2016).

At present on the Eastern US coast, the green sea urchin (Strongylocentrotus droebachiensis) is one of the most valuable sea urchin species. It is a cold-water species and is currently produced through wild fisheries capture and is emerging through aquaculture in the State of Maine (ME). But recent work funded by the Northeastern Regional Aquaculture Center led by lead author Suckling shows that there is interest to expand this production into other New England states (New Hampshire, Massachusetts, and Rhode Island). At present the Rhode Island governing bodies are uncertain of the native status of S. droebachiensis with unconfirmed reports provided from regional recreational scuba divers and one confirmed report in 1998 in a coastal pond (Rhode Island Department of Environmental Management). Therefore, there is a potential niche and interest for A. punctulata production in areas where sea urchin cultivation is not yet practiced expanding southwards comfortably within this species’ natural distribution range. However, further work is first needed to fully determine the economic potential for A. punctulata.

The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.

CS, MZ, and BT contributed to conception and design of the study. CS and MZ performed the statistical analysis, and wrote the first draft of the manuscript. AB conducted and contributed sex and reproductive stage determination data. AB and BT wrote sections of the manuscript. BT contributed the Urchinomics diet for the trial. All authors contributed to manuscript revision, read, and approved the submitted version.

This work was partly funded by the United States Department of Agriculture, National Institute of Food and Agriculture (Project #RI0019-H020), Northeastern Regional Aquaculture Center and the University of Rhode Island Department of Undergraduate Research and Innovation (URI²).

Thank you to Urchinomics and Yuma Yamamoto for supplying the diet for use in this study. Thank you to Alli McKenna and Tyler Pelletier for animal husbandry assistance and to Sara Lacourciere, Ellie Mulligan, and Kelsey Mudry for assistance in the laboratory. This work was generated through an undergraduate research skills course (AFS491) within the University of Rhode Island.

Author BT was employed by Urchinomics BV.

The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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