Are There Any Marine Animals That Are Domesticated

• Journal List
• Anim Front end
• 5.11(iii); 2021 May
• PMC8214440

Anim Forepart. 2021 May; 11(iii): 87–91.

Fish domestication in aquaculture: 10 unanswered questions

Fabrice Teletchea

Unité de Recherche Animal and Fonctionnalités des Produits Animaux, Institut National de Recherche cascade l'Agronomics, l'Alimentation et fifty'Environnement, Université de Lorraine, 54505 Vandœuvre-lès-Nancy, France

Keywords: diversification, fish domestication, selective breeding programs, sustainability, global issues

Implications

• Aquaculture is the fastest-growing food-product sector in the earth.

• The number of farmed and domesticated fish species has increased tremendously in the past decades, fifty-fifty though the twenty most-produced species accounted for >fourscore% of total fish aquaculture production.

• This article discusses ten partially unanswered questions related to fish domestication that could help enhancing the sustainable development of aquaculture.

• Domestication is a powerful tool to keep improving the production of already domesticated species and subcontract new species, peculiarly those native, which could all be better adapted to cope with economic, social, and environmental bug.

Introduction

The commencement trials of farming fish species for human being consumption might date back to viii,000 twelvemonth ago, with the managed aquaculture of common bother (Cyprinus carpio) in Henan Province, China (Nakajima et al., 2019). Evidence of farming was also plant on Egyptian tombs from about 3,500 twelvemonth, with some kind of control over the reproduction of Nile tilapia (Oreochromis niloticus) in irrigation ponds (Teletchea, 2019a). In Europe, the farming of common carp in ponds was already developed during the Middle Ages. The Italian "Vallicoltura" (extensive farming of various marine species in coastal lagoons and large open waterbodies) dates back to the 15th century. The French trout civilization started around the second one-half of the nineteenth century (Teletchea, 2019a). In North America, aquaculture started well-nigh 100 twelvemonth ago. In Africa, aquaculture dates back to the 1940s. In Australia, New Zealand, and various Pacific Island states, the development of aquaculture is fifty-fifty more recent. In conclusion, the rearing of fish is very old (Gjedrem et al., 2012), particularly in Asia (De Silva et al., 2009), fifty-fifty though this is not before the early 1980s that aquaculture truly boomed, becoming the fastest-growing food-production sector globally (Teletchea, 2016a; FAO, 2019). In only four decades, aquaculture production has surpassed capture fisheries, and today more than half of the fish destined to homo consumption are farmed globally (Teletchea 2016a; FAO, 2019; Houston et al., 2020). The exponential growth of aquaculture has relied partly on the domestication of an increasing number of fish species (FAO, 2019; Teletchea, 2019b). The aim of the present commodity is to discuss briefly 10 partly unanswered questions linked to fish domestication, which could be taken into account to promote a more sustainable global aquaculture production.

Question 1: What Is Fish Domestication?

In that location is no scientific reason to consider fish domestication differently from any other animal domestication (Balon, 2004; Bilio, 2008; Hedgecock, 2012; Lorenzen et al., 2012; Teletchea, 2015a; Saraiva et al., 2019). Therefore, fish domestication could be defined equally a dynamic and countless process, which starts as soon as individuals are transferred from wild to captive atmospheric condition (Teletchea, 2015a). Five genetic processes are involved in the evolution of fish during domestication: two uncontrolled (inbreeding, genetic drift), 2 partially controlled (natural choice in captivity, relaxation of natural choice in captivity), and one controlled (active pick) (Teletchea, 2015a). In add-on, the diverse molecular mechanisms involved in 'nongenetic' modes of inheritance tin can change aspects of genome action and affect progeny gene expression (Adrian-Kalchhauser et al., 2020). Summing upwards, domestication allows adapting continuously a batch of fish to both captive weather and humans, with the ultimate goal of modifying, generations after generations, selected traits, to produce, in near cases, more than productive and efficient individuals (Bilio, 2008; Olesen et al., 2015; Houston et al., 2020).

Question 2: What Is a Domesticated Fish?

For Balon (2004), animals become domesticated when they modify form, part, color, and behaviour; oft only partially resemble their wild ancestors; and survive poorly as feral forms if returned to the wild without human being protection. For Bilio (2008), fish species are considered domesticated when they show first results of selective breeding or when no such evidence is establish, afterward at to the lowest degree iii successive cycles of reproduction (generations) under controlled weather condition (the choice of 3 full cycles in captivity was an capricious criterion). Duarte et al. (2007) considered that fish are domesticated when breeding, caring, and feeding of organisms are controlled by humans. For Gjedrem et al. (2012), domesticated fish strains are the result of several generations of selection. Hence, rather than trying to define what a domesticated fish is, which could be in fine considered an capricious decision because information technology varies widely betwixt authors and no articulate threshold separates wild from domesticated animals (Teletchea, 2017), Teletchea and Fontaine (2014) coined a new concept (domestication levels) based on the degree of human control over the life bike of farmed fish species. This domestication scale contains five levels (Table 1). According to this new classification, it was proposed that simply fish species reaching at least the level four (full life cycle completed in captivity without wild inputs) could exist considered domesticated. Yet, a domesticated fish is neither a definitive status equally these animals continue evolving all the time (to cope with new captive atmospheric condition or because new traits are selected), nor a final end signal of domestication considering they can sometimes return to the wild, a procedure known as feralization (readaptation to the natural environment), which is one of the main issues of aquaculture globally (Lorenzen et al., 2012; Glover et al., 2017).

Tabular array 1.

Clarification of the domestication levels of fish species (modified from Teletchea, 2019b)

Level	Description	northward species	n families	Three master families (n)
5	Selective convenance programs are practical focusing on specific goals	30	10	Cyprinidae (ten), Salmonidae (eight), Acipenseridae (five)
4	Full life cycle is controlled in captivity without the use of wild inputs	45	25	Cichlidae (6), Sparidae (5), Cyprinidae (4)
3	Full life bicycle is controlled in captivity, yet wild inputs are yet used	61	35	Sparidae (eight), Cyprinidae (4), 4 families (3)
2	Simply part of the life cycle is controlled in captivity due to central bottlenecks	75	39	Cyprinidae (9), Serranidae (5), Carangidae (4)
1	Kickoff trials of acclimatization to captive conditions	39	24	Cyprinidae (8), Sciaenidae (3), Siganidae (3)

Question three: How Many Fish Species Are Domesticated?

The number of fish species considered domesticated varies tremendously between authors from two for Balon (2004), 42 for Bilio (2008) to over 250 for Duarte et al. (2007). Yet, the number proposed by Balon (2004) is conspicuously besides low because of his strict definition (see in a higher place). Conversely, the very high number documented by Duarte et al. (2007) only reflects the growth of aquaculture globally (Hedgecock, 2012); farming a fish species does not necessarily imply that it has been domesticated (Bilio, 2008; Klinger et al., 2013; Teletchea and Fontaine, 2014). Amid the 250 fish species listed by Duarte et al. (2007), which were established from the FAO database for the years 1950 to 2009, only one-third had reached the level iv (due north = 30) or level 5 (n =45) (Teletchea and Fontaine, 2014); which is much closer to Bilio's estimations. Most a decade later, information technology is likely that new species have reached levels 4 and 5 (e.g., Teletchea, 2015b; Valladão et al., 2018) and probably 100 could be considered domesticated globally (see besides FAO, 2019; Houston et al., 2020).

Question 4: How Long Does It Take to Domesticate a Fish Species?

Domesticating a fish species implies that the full life cycle is controlled in captivity without wild inputs (Table 1). The time required to reach this milestone varies tremendously betwixt species, if always attained (Bilio, 2008; Teletchea and Fontaine, 2014). Indeed, numerous farming trials of new species failed only afterward a few years more often than not due to insufficient biological, ecological, and zootechnical knowledge (Teletchea and Fontaine, 2014). Primal bottlenecks in closing the life bicycle in captivity are (1) inadequate feeds, particularly for the first feeding of tiny larvae of numerous marine fish species, (two) poor gonadal development, and (3) lack of spawning (run into also Bilio, 2008). Most ofttimes, we accept no information about the domestication history of farmed species (Teletchea, 2019a); yet see for instance Gjedrem (2010, 2012) and Glover et al. (2017) for Atlantic salmon (Salmo salar) and Fontaine and Teletchea (2019) for Eurasian perch (Perca fluviatilis) (Figure 1A). In conclusion, domesticating a new fish species is a risky journey that may take years or even decades (Bilio, 2008; Teletchea and Fontaine, 2014; FAO, 2019).

Examples of two freshwater fish species that have reached in 2009 the level 4: European perch Perca fluviatilis (A) and the level five: common carp Cyprinus carpio (B). Pictures taken from www.storefish.fr (Teletchea and Teletchea, 2020).

Question five: Is Fish Domestication Going as well Fast?

Once the full life wheel is controlled in captivity, in that location are no longer exchanges between farmed individuals and their wild congeners, and domestication tin proceed toward the production of improved individuals (Table 1). For some domesticated species, several generations under selection have allowed improving specific traits very rapidly (Olesen et al., 2015; Nguyen, 2016; Teletchea, 2016b; Houston et al., 2020). Therefore, the time lag between the onset of domestication and selective breeding can be considerably short in aquaculture (less than a decade), with both occurring in tandem in many cases (Houston et al., 2020). However, it was plant that without proper management, numerous breeding programs resulted also in a quick loss of genetic diversity because of inbreeding, possibly leading to a decline of productivity, a reduced population fitness, and an increased susceptibility to stress and disease (Olesen et al., 2015; Nguyen, 2016; Houston et al., 2020). Therefore, circumspection should be taken not to get too apace when implementing breeding programs and adequately balance market (due east.g., growth charge per unit, fillet quality) and non-market place values, such every bit ideals and welfare (Saraiva et al., 2019). Inquiry has pushed the physiological limits of many fish species in growth, fertility, and size, every bit a consequence of (or resulting in) highly artificial conditions, mayhap altering their welfare, which is one of the central issues of aquaculture today (Saraiva et al., 2019). It is besides crucial to maintain sufficient genetic variability (e.thou., constitute a base population with ample genetic variability, keep a big constructive population size, and introduce genetic variability from exterior the breeding stock) of domesticated and selected fish to ensure that they are more robust and able to cope with diverse environmental changes (Olesen et al., 2015; Nguyen, 2016; Teletchea, 2016b). Supported by continuous advances in sequencing and bioinformatics, genomic tools appear now hugely valuable to inform sustainable genetic improvement and their affordability and accessibility mean that they can now exist applied across the broad range of aquaculture species and at all stages of the domestication process to optimize selective breeding (Houston et al., 2020).

Question half-dozen: What Are the Nigh Domesticated Fish Species?

Thirty species belonging to 10 families take reached the level 5 (Table 1), including Acipenseridae (n = five), Cichlidae (n =1), Cyprinidae (northward = x), Gadidae (n = 1), Ictaluridae (n = ane), Moronidae (n =1), Paralichthyidae (northward =1), Salmonidae (n = 8), Scophthalmidae (n = 1), and Sparidae (n = 1) (Teletchea, 2019b). Among those thirty fish species, common carp (Figure 1B) and Nile tilapia are probably the about selected for the longest menses of fourth dimension globally (Bilio, 2008; Gjedrem et al., 2012; Nguyen, 2016; Teletchea, 2019a). In Europe, the most domesticated and selected species are common bother, rainbow trout (Oncorynchus mykiss), Atlantic salmon, gilthead bounding main bream (Sparus aurata), European seabass (Dicentrarchus labrax), and turbot (Psetta maxima) (Janssen et al., 2017).

Question 7: Which Traits Were Selected?

Selective breeding programs in fish take historically focused on improving growth (Nguyen, 2016; Gjedrem and Rye, 2018). Genetic proceeds averages about ten% to 20% per generation for growth charge per unit when this is the main, or only, selected trait (Gjedrem et al., 2012). In addition to growth, feed conversion efficiency, historic period at sexual maturity, improved resistance to bacterial and viral diseases, and a number of traits related to production quality (due east.g., muscle lipid content, flesh color, tenderness, season) have been gradually included in various convenance programs, specially for Atlantic salmon (Gjedrem, 2010, 2012). In a contempo survey conducted among breeding companies of v species farmed in Europe, Janssen et al. (2017) found that growth operation was universally selected upon. Among the 27 breeding programmes, both morphology and illness resistance were included in fifteen, product quality in 13, processing yield in 12, and reproduction and feed efficiency in 7 (Janssen et al., 2017). In conclusion, the future seed market volition most probable go on to request genetic material that is selected for growth rates also every bit other traits (Olesen et al., 2015; run across also Table 25 in FAO, 2019).

Question eight: Is there a link betwixt fish domestication level and production volume?

It is impossible today to definitively conclude whether domestication levels (Table 1) and production volumes are positively linked given the bodily nature of data provided to the FAO by its members and associated nations (Klinger et al., 2013; Teletchea and Fontaine, 2013). Yet, Bilio (2008) highlighted that the pct of domesticated species is increasing with the production level. The share of domesticated species is probably shut to zero as long equally the production per species remains beneath 100 tons and shut to 100% for species reaching a product of 1 million tons (see Table vii in Bilio, 2008). In other words, fully closing the life cycle in captivity seems positively related to a significant production: the meridian 15 almost-produced species in 2009 all take reached level 4 or v (Teletchea and Fontaine, 2013). This includes species for which the onset of domestication is either centuries old, such as common carp or Nile tilapia, or a few decades old, such as Atlantic salmon (Teletchea, 2019b). In Europe, the proportion of aquaculture product that originates from selective breeding is very high, with a market share that exceeds eighty% (Janssen et al., 2017). Atlantic salmon clearly appears every bit an outlier with shut to 100% of the production that are at present based on improved stocks (Gjedrem, 2010; Gjedrem et al., 2012). Yet, for most farmed species reaching level 4 or 5 does not necessarily imply that their full aquaculture production is based on this level (stocks of the same species tin can be at different domestication levels). Overall, only 10% of the global aquaculture production comes from genetically improved stocks (Gjedrem et al., 2012; Olesen et al., 2015).

Question nine: Should Nosotros Cease Domesticating New Fish Species?

The blast of fish aquaculture has relied partly on the domestication of an increasing number of fish species, even though most domestication experiments stopped or failed to reach a pregnant volume and the global product is today heavily skewed toward the farming of a few species (FAO, 2019; Teletchea 2019b; Sicuro, 2021). The 20 nigh-produced species account for >84% of full production (FAO, 2019; Teletchea, 2019b). The primary farmed species have been extensively introduced around the world (De Silva et al., 2009; Teletchea, 2019a). Seven of the eight most widely farmed fish species are more than often reported by countries where they are non-native than by countries where that are native (FAO, 2019). For instance, common carp is farmed in 48 countries, amid which 37 where it was introduced (FAO, 2019). As well, Nile tilapia is farmed in 45 countries (33 introduced) and rainbow trout in 45 countries (40 introduced) (FAO, 2019). The introduction of non-native species can affect biodiversity, straight or indirectly, and these impacts can be firsthand or long term (De Silva et al., 2009). Therefore, reducing the dependence on non-native species, and thereby minimizing possible negative impacts on biodiversity, is increasingly perceived every bit an imperative for the sustainable evolution of aquaculture (De Silva et al., 2009). In this context, there are conflicting demands for further diversification versus the need to focus and improve the efficiency of production of existing farmed species (FAO, 2019). Bilio (2008) considered that information technology is no longer desirable to seek farther diversification by subjecting yet more species to experimentation, but rather restrict our efforts to a few species and exploit intra-specific diversity potential, that is, the still largely unknown genetic diversity resources within truly domesticated species. Conversely, there is still huge potential for domesticating new fish species, particularly native ones, to develop a more diverse aquaculture sector likely to be more resilient to challenges of environmental change (Valladão et al., 2018; FAO, 2019; Fontaine and Teletchea, 2019). Such a strategy might also assist to eliminate, or at least minimize, the adverse ecological and genetic impacts of either directly or indirect introduction of non-native species (De Silva et al., 2009). In contempo years, the willingness to promote native species for aquaculture enterprise has resulted in meaning changes in diverse countries, particularly in Southward America (Valladão et al., 2018). For example, the product of pacu Piaractus mesopotamicus has increased significantly in recent years, exceeding the product of the non-native rainbow trout in 2012 in Argentina (Valladão et al., 2018). The contribution of native species to global aquaculture will maybe increase, resulting in a more diversified and even production than today (Teletchea, 2019b). In conclusion, it is likely that both intra- and interspecific diversification will be pursued at least in the coming decade, that is to go on improving already domesticated and selected species and to farm new fish species (FAO, 2019; Teletchea, 2019b).

Question ten: Practise Nosotros Already Demand a 6th Level of Domestication?

Given the tremendous progresses in fish domestication, information technology might exist timely to propose a sixth level of domestication for the species for which selection has resulted in strains. According to the FAO (2019), a strain is a "farmed type of aquatic species having homogeneous appearance (phenotype), homogeneous behaviour and/or other characteristics that distinguish it from other organisms of the same species and that can be maintained by propagation." Some strains (notably for mutual carp and rainbow trout) are already officially registered in a limited number of countries (Bilio, 2008), merely at that place are still very few distinct, stable, and reproducible strains in aquaculture (Bilio, 2008; FAO, 2019). I very well-known example is the genetically improved farmed tilapia (Gift) strain adult in the early 1990s from a base of operations population including wild and farmed strains from eight African and Asian countries (Gjedrem, 2012; Nguyen, 2016; Houston et al., 2020). The Souvenir strain is now farmed in 16 countries beyond Asia, Africa, and Latin America and grows 85% faster than the base population (Houston et al., 2020). Similarly, the Atlantic salmon is certainly the fish for which the domestication history is all-time known (Teletchea, 2019b) and was the first species to exist subject to a systematic family-based breeding program (Gjedrem, 2010, 2012). Currently, over 12 generations have been consecutively bred in captivity for the oldest breeding programs in Norway and multiple strains were established in several countries (Glover et al., 2017). All the same, information technology might still be also early to advise a sixth level of domestication for only a few strains in a scattering of species; this situation might modify quickly, and many recognizable strains could be soon officially recognized and registered as observed for the thousands breeds in farmed country mammals and birds (FAO, 2019).

Conclusions

Domestication is a long and endless procedure that allows adapting fish to both captive conditions and humans. This process started only a few decades (or even years) ago for nigh farmed species, and therefore probably less than i-tertiary could be considered domesticated. Several traits, amidst which growth, were modified during domestication. New convenance programs volition need to balance market place and non-marketplace values while maintaining a sufficient genetic variability to ensure that fish are productive also as robust enough to cope with diverse environmental changes. The sustainable hereafter of aquaculture will rely first on the continuous improvement of already domesticated fish species and second on our willingness and capacity to diversify the number of farmed, preferably native, species to promote a more diversified and even aquaculture production.

Notes

Well-nigh the Authors

Fabrice Teletchea studied marine biology and then systematics in France. Since 2010, he is associate professor at the University of Lorraine in Nancy, France. He first worked on fish taxonomy and then moved to the study of fish domestication in aquaculture. He developed a comparative framework of the reproductive strategies of European freshwater fish species in order to better sympathise the unlike trade-offs observed at the early-life stages (www.storefish.org), to help domesticating them more efficiently. Besides his research and didactics activities, he is in charge of a professional person bachelor entitled "Inland Aquaculture and Aquariology" for nigh 10 years at the IUT Nancy-Brabois.

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