Aquaculture of Polychaete annelids and their importance for Latin America

doi:10.21203/rs.3.rs-3112629/v1

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Aquaculture of Polychaete annelids and their importance for Latin America

https://doi.org/10.21203/rs.3.rs-3112629/v1

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Interest in using polychaeta annelids as an alternative feed source for aquaculture was generated by providing an alternative to clams and mussels as bait. This has subsequently led to increased interest in their reproduction, with countries such as the United Kingdom, China, Japan, Australia and France successfully creating extensive, semi-intensive, and intensive systems of production. Studies have also reported the use of polychaeta annelids in Integrated Multi-trophic Systems (IMTA), their interest as ornamental species, and research at the biotechnological level. In Latin America, Ecuador, Chile and Peru report research on their exploration in culture, their use as shrimp feed and their involvement in IMTA. However, so far, Chile is the only country that has successfully achieved knowledge of the reproductive cycle of two polychaeta species.

The polychaeta families that demand greater research include Eunicidae, Onuphidae, Nereididae, Arenicolidae, and Glyceridae. Due to their ecological characteristics, some species are also potential contributors to parasite infections. As such, correct taxonomic identification based on their ecological and physiological characteristics, could increase the potential for their use as an alternative aquaculture feed ingredient, reducing feeding costs through recirculation systems. The present investigation was conducted through research using the bibliographic databases: Elsevier, Science Direct, Scielo, Scopus and Google Scholar.

Live Feed

Aquaculture

Feed

Ornamental Aquaculture

Integrated Multitrophic Aquaculture

Latin America

Over the last two decades, the aquaculture sector has seen an important growth in its contribution to food security and human nutrition (FAO 2022), with a record global aquaculture production of 122.6 million tons in 2020, valued at USD 281.5 billion, with 87.5 million tons of aquatic animals worth USD 264.8 billion. (FAO 2022). It is estimated that by 2030, the total number of aquatic animals produced from aquaculture will reach 106 million tons (FAO 2022). In Latin America, it is expected that by 2030 more than 65% of aquatic food will come from aquaculture, accounting for 30% of total protein consumed in developing countries and 15% in Europe and North America (OECD-FAO 2018), due to increasing consumption and trade, albeit at slow growth rates, as reported by FAO (2022) and Zhou et al. (2017).

However, the continuous growth of this sector is dependent on the availability and cost of feed (Zhou et al. 2017). As one of the costliest, but most essential parts of aquaculture production, with an estimated 46.1% dependence on fresh or industrialized feed, there is a constant search for new and better feed alternatives (Priscilla et al. 2022).

Thus, since the 1990s, several countries have been trying to research and explore feed alternatives for the production of aquatic animals from aquaculture, applying technologies to obtain food supplements or diets that contribute adequate levels of nutrients, and are accepted by the species under cultivation. Among these alternatives, polychaete annelids stand out, as they contain high levels of polyunsaturated fatty acids, proteins, vitamins and minerals, which are essential for the development of shrimp and fish. As such, they are competitive alternatives to other invertebrates like bivalve mollusks and squid, containing an equal or higher percentage of these macronutrients (Chimsung 2014). This is demonstrated in studies that were, and continue to be conducted by countries such as the United States, United Kingdom, France, Holland, Canada, China, Egypt, and Australia, encouraging researchers from other countries to use “polychaetes” as a marine resource for different areas of research (Coutinho et al. 2017). In these studies, polychaete annelids have been involved in "Recirculating Aquaculture Systems" (RAS); bait in sport fishing, an ancient practice that triggered their use in aquaculture; as well as cultivation in laboratories or aquaculture farms for research at the biotechnological level (Broquard et al. 2022) and application in the medical field. This is demonstrated by the company, Hemarina S.A., in France with the production of the polychaete Arenicola marina for the creation of different therapeutic products from the hemolymph of the annelid (Herrera-Perez 2020; García-Garza et al. 2021).

This research is also not foreign to Latin America, with Chile, Ecuador, and Brazil also reporting studies in the areas of aquaculture and evolutionary biology. In addition, Peru also has a record of technical collaboration with Chile, and such examples will be discussed later. However, it is important to first consider what are “polychaetes”. “Polychaetes” are segmented worms that traditionally belong to the Phylum Annelida (Lamarck 1802), Class Polychaeta (Grube 1850; Fauchald 1977), and are considered the most diverse of the annelids (Weigert and Bleidorn 2016). However, this classification is no longer accepted, because they are considered a paraphyletic group, as many studies point out (Rouse and Pleijel 2001; Rouse and Pleijel 2006; Rouse and Pleijel 2007; Struck et al. 2015). They are characterized as having setae, structures also known as silks, ketas, or bristles. Their body consists of three basic regions: prostomium, metastomium and pygidium. The prostomium is the anterior part of the body, which is basically the head and carries sensory structures (eyes, antennae, palps). The metastomium is the trunk of the body, which contains the segments, which derive the legs or parapods from which the setae emerge. Finally, the pygidium, which is the posterior end or tail, carries the anus (Harris et al. 2009, 2021). These regions and structures are not only very important for their taxonomic identification, but also confer an enormous morphological variety, giving rise to different lifestyles, and contributing to why they are considered the most diverse group of annelids (Rouse and Pleijel 2001), with 11,456 "polychaete" species recognized (Pamungkas et al. 2019, Read and Fauchald 2020), 1,417 genera and 85 families. There are expected to be another 5,200 species classified by 2100 (Pamungkas et al. 2019). While most “polychaetes” are distributed throughout marine benthic ecosystems, 95 species, forming part of nine families, including the previously excluded families Yndolacidae and Flotidae, have been identified as successfully colonizing the pelagic (holoplanktonic) environment nine families, (Suárez-Morales et al. 2005; Díaz-Díaz et al. 2009; Cárdenas-Oliva et al. 2010; Márquez-Rojas et al. 2013; Guglielmo et al. 2014; Rozbaczylo et al. 2020), but their phylogenetic relationships have not yet been fully elucidated (Rouse and Fauchald 1997; Rouse and Pleijel 2001). Polychaete annelids have also been found to live in estuaries, the terrestrial environment and freshwater bodies, with 168 known species included in 70 genera and 24 families, representing less than 2% of the total estimated number of species.

In addition to being found in natural habitats, some “polychaete” species have managed to establish viable populations in artificial environments of anthropogenic origin, such as port and maritime structures (marker buoys, boat hulls, dock piles, floating restaurants), as well as in aquaculture structures, such as oyster planting trays, shrimp farm piles, or gates (Tovar-Hernández et al. 2018).

In the benthos, “polychaetes” are often the dominant component in terms of species diversity and abundance (Rouse and Pleijel 2001; Tomassetti and Porrello 2005, Nesto et al. 2012).

They play fundamental roles in the ecosystem, contributing to the overall energy flow, decomposition of detritus, and nutrient cycling (Pires et al. 2017). Their wide range of alimentary strategies allows them to be classified as microphagous or macrophagous (carnivores, scavengers, parasites, herbivores), omnivorous or osmotrophic (Jumars et al. 2015), and their different reproductive strategies (Bybee et al. 2006) are an important link in marine trophic webs (Fauchald and Jumars 1979; Hutchings 1998; Drazen et al. 2008; Fadhullah and Syakir 2016; Kihia et al. 2017). These characteristics also make them bioindicators of the marine ecosystem (Giangrande et al. 2005; Nesto et al. 2012; Parandavar et al. 2015; Pires et al. 2017).

Therefore, the present work aims to inform, integrate and analyze, the scattered information on the aquaculture potential of polychaete annelids worldwide, and thus their potential research in Latin America. It aims to be a source of information to enhance other areas of basic and applied research: taxonomy, ecology, biotechnology, nutrition, aquaculture, genetics, developmental biology, medicine, nanotechnology, toxicology, and pharmacology, immunology, among others.

For the research of this article, a bibliographic search was performed in different databases (Elsevier, Science Direct, Scielo, Web of Science, Scopus and Google Scholar), with the keywords in English and Spanish: “polychaete”, “aquaculture with polychaete”, “Recirculating systems with polychaete (a)”, “sewage treatment and polychaetes”, “bait worms”, “bait polychaeta”, “bait polychaeta for recreational fishing”, “aquaculture with polychaetes” and “los poliquetos en la acuicultura”.

Ornamental Polychaete Annelids

Some coral species of “polychaetes” from the Sabellidae and Serpulidae families are commonly known as "marine flowers" and are commercialized in the ornamental market (Olivotto et al. 2011; Jäger 2011, 2012; Murray et al. 2012, 2013; Palmtag 2017; Carvalho et al. 2019; Capa et al. 2021). This is because their anterior region, called the gill crown, exhibits a variety of colors, and their large size makes them very attractive to consumers (Tovar-Hernández 2009; Olivotto et al. 2011; Dávila-Jiménez et al. 2017). The genera of the Sabellidae family include: Sabellastarte with species like : S. japonica; S. magnifica, S. sanctijosephi, S. spectabilis, S. fallax, and S. samoensis (Bybee et al. 2006; Bybee et al. 2007; Murray et al. 2012; Bybee and Murray 2017) and S spp. (Costa et al. 2016); the genus Bispira (Tovar-Hernández and Pineda-Vera 2008; Bastidas-Zavala 2009; Bastidas-Zavala and Sánchez-Ovando 2021; Capa et al. 2021) includes Bispira brunnea (Capa et al. 2021); the genera Anamobaea, Notaulax (Capa et al. 2021) and Branchiomma, with the species Branchiomma luctuosum (Carvalho et al. 2019); as well as the genus Sabella with species like Sabella spallanzanii and Sabella pavonina (Capa et al. 2021). In the Serpulidae family, genera include Spirobranchus, Protula and Serpula (Bastidas-Zavala 2009; Bastidas-Zavala and Sánchez-Ovando 2021; Capa et al. 2021). Unfortunately, though, this valuation in the market, means that there are often destructive practices used to obtain these polychaete annelids, a similar situation to what is seen in sport fishing (Bybee et al. 2006; Dávila-Jiménez et al. 2017). Hence, aquaculture can be considered as an alternative way to conserve and commercialize these species without destroying them.

Sport fishing

The trend of using “polychaetes” rather than clams and mussels as bait in sport fishing began sometime between 1921 and 1922 in the United States (Long Island, N.Y.), (Creaser et al. 1983). This thus expanded its catchment area to the coast of North America, East Asia and Borthern Europe (Gambi et al. 1994).

Since 1980, there has been an interest in the lucrative production of these “polychaetes”, thus increasing its economic value (Sá et al. 2017; Cabral et al. 2019) and demand as bait for fishing (Garcês and Pereira 2011; Sá et al. 2017; Pombo et al. 2018; Mandario 2020; Martin et al. 2020; Broquard et al. 2022; Escobar-Ortega et al. 2022). It also became directly used by the crustacean and fish aquaculture industries (Olive and Cowin 1994; Olive 1994; Fidalgo and Costa 1999; Olive 1999; Messina et al. 2005; Fidalgo and Costa et al. 2006; Brown et al. 2011; Garcês and Pereira 2011; Hamdy et al. 2014; Mohammad 2015; Pombo et al. 2018; Martin et al. 2020), as is the case of the company, Seabait Ltd in the UK United. As a result, Seabait Ltd. became a sector leader in the production and sale of Alitta virens (N. virens), and was later taken over by the company Topsy Baits (Netherlands). This also sparked other countries’ interest in the research and production of “polychaetes”, such as Australia, China and Korea (Nesto et al. 2012).

In Australia, 1996, the company Aquabait was established in Dora Creek (New South Wales), and began production of Diopatra aciculate. Meanwhile, in China, the company Qidong King Power Polychaete Aquaculture Co., Ltd., became focused on the production of Alitta virens (N. virens) (Nesto et al. 2012). Font and Lloret (2011), reported that between 2007 and 2009, the polychaetes Perinereis aibuhitensis "Korean worm", Marphysa sanguinea "threadworm", Glycera dibranchiata "American worm" and Arenicola spp. "sandworm”, accounted for 43.2% of the total invertebrates used as bait, Globally, there are roughly 60 species of polychaetes, belonging to 12 families (Cole et al. 2018; Pamungkas et al. 2019), being used as bait (Cole et al. 2018; Pamungkas et al. 2019; Kannapan et al. 2021). However, this number varies between studies, with Pombo et al. (2020), and Yang et al. (2022), reporting the use of 27 species.

Cunha et al. (2005) and Barrington et al. (2009), reported that in 1999, the worm market in Europe reached a valuation of around € 200 million, but the exact value is not known, as it is the “black market”, and there is a lack of sales reporting. Likewise, Whatson et al. (2017), De Cubber et al. (2018), Mandario (2018), Cabral et al. (2019), and Mandario (2020) estimated that the annual harvest of polychaetes used for bait, was 121,000 tons worth USD 9.15 billion in 2016. However, the same authors note that FAO reported 314 tons of marine worms caught in 2015 (not all countries are included in the study), which suggests the same problematic, under-reporting of sales. In the United States, Maine reported that sales of Glycera dibranchiata and Alitta virens (Nereis virens) reached USD 8.7 million in 2020 (Maine.gov).

Despite not having an updated record of the volume of commercialization of “polychaetes” as live bait, due to its dependence on the species and country, some authors have reported the price of some species (Table 1). Currently, the estimated percentage of bait that “polychaetes” make up is 19.5% in Australia, 4.7% in North America, 1.6% in Europe and Africa, and less than 0.3% in Asia (Cole et al. 2018). The following table organizes the bibliographic information regarding the families and species of “polychaetes” harvested from their environment for recreational or aquaculture purposes, as well as their locality of provenance, and in some cases their commercial value, with the source of information also identified (Table 1).

Table 1

Species of “polychaetes” harvested for commercial use as live food worldwide
Family	Species	Country or Region	Commercial value	References
Eunicidae	Marphysa sanguinea	Italian Coast (Venice Lagoon)		Gambi, et al. 1994
				Olive 1994
				Scaps 2003
		Portugal		Fidalgo e Costa et al. 2006
				Da Fonseca and Fidalgo e Costa 2008
				Font and Lloret 2011
				Garcês and Pereira 2011
				Parandavar et al. 2015
				Mosbahi et al. 2015
		Portugal		Sá et al. 2017
		Portugal	US$ 67,97 kg^− 1	Watson et al. 2017
		Spain (Andalucia)	US$ 0,50	Font et al. 2018
			US$ 85 kg^− 1	Mandario 2018
				Martin et al. 2020
				Mandario et al. 2020
				Pombo et al. 2020
	Marphysa sp.	Europe		Cole et al. 2018
		Portugal (Ria de Aveiro Coastal Lagoon)		Cabral et al. 2019
		Portugal		Mandario 2018, 2020
		China		Yang et al. 2022
	Eunice aphroditois	Italian Coast		Bello 1993
		Italian Coast		Gambi et al. 1994
				Yang et al. 2022
	Eunice sebastiani	Brazilian Coast		Amaral and Jablonski 2005
	Marphysa maxidenticulata	North China		Yang et al. 2022
Arenicolidae	Arenicola defodiens			Olive 1994
				Scaps 2003
		United Kingdom	US$ 65,50 kg^− 1	Watson et al. 2017
		North America		Cole et al. 2018
				Pombo et al. 2018
			US$ 82	Mandario 2018
	Arenicola marina	United States		D´asaro and Chen 1976
		Netherlands		Hellingerberg 1982
		Spain		Sardá 1989
		United Kingdom		Olive 1994
		Ireland		Olive 1994
		United Kingdom		Olive and Cowin 1994
		United Kingdom, Netherlands and Cantabria Estuary		García del Real 2007
		United Kingdom	US$ 49,43 kg^− 1	Watson et al. 2017
		Northern France Spain (Cantabrian Sea)	US$ 0,75/ind.	Font et al. 2018
				Pombo et al. 2020
		North America		Cole et al. 2018
				Broquard et al. 2022
				Mosbahi et al. 2015
	Arenicola spp.	China		Font and Lloret 2011
		Korea
		North America
		Canada
		United Kingdom
		Netherlands
	Arenicolides branchialis			Pombo et al. 2020
	Arenicolides ecaudata
	Arenicola brasilensis			D´asaro, 1973
		North America		Cole et al. 2018
	Arenicola cristata	EEUU		D´asaro, 1973
		North Mediterranean coast		Sardá 1989
		North America		Cole et al. 2018
Nereididade	Nereis spp.			Sá et al. 2017
	Perinereis cultrifera	Italian Coast (Venice Lagoon)		Gambi et al. 1994
				Scaps 2003
				Younsi et al. 2010
				Mosbahi et al. 2015
		China		Sá et al. 2017
		Algerian	US$ 7,41 kg^− 1	Watson et al. 2017
				Pombo et al. 2020
				Jayaseelan et al. 2021
				Goti et al 2021
	Perinereis rullieri	Italian Coast (Lagoon from Venice)		Gambi et al. 1994
	Perinereis nuntia			Pombo et al. 2020
		Thailand		Yang et al. 2022
	Hediste diversicolor	Italy		Ansaloni et al. 1986
		France		Bellán 1964
		Spain
	(*Nereis diversicolor)	United Kingdom		Olive and Cowin 1994
				Fidalgo e Costa 1999
		Portugal		Fidalgo e Costa et al. 2006
		United Kingdom		García del Real 2007
				Da Fonseca and Fidalgo e Costa 2008
		Italian Coast (Lagoon from Venice)		Gambi et al. 1994
		Portugal (Ria de Aveiro and Canal de Mira)		Cunha et al. 2005
				Younsi et al. 2010
				Aberson et al. 2011
		Portugal Coast France Italy		Nesto et al. 2012
				Carvalho et al. 2013
				Mosbahi et al. 2015
		Portugal		Sá et al. 2017
		Algerian	US$ 7,41 kg^− 1	Watson et al. 2017
		English Channel (Northern France)	US$ 0,75	Font et al. 2018
		Europe		Cole et al. 2018
				Pombo et al. 2020
		Portugal (Ria de Aveiro Coastal Lagoon)		Cabral et al. 2019
				Broquard et al. 2022
	Perinereis spp.	Southwest Japan		Scaps 2003
	Perinereis sp.	Asia		Yang et al. 2022
	Perinereis Vallata (Perinereis nuntia vallata)*	Thailand
				Panakorn 2015
				Pombo et al. 2020
				Broquard et al. 2022
	Perinereis aibuhitensis	Sureste de Asia		Grupo de Ecología, Universidad de Cantabria y TEICAN Medioambiental S.L 2002
		China		Fidalgo e Costa et al. 2006
		China		Da Fonseca and Fidalgo e Costa 2008
		Vietnam		Font y Lloret 2011
				Nesto et al. 2012
		China	US$ 12,36 kg^− 1	Watson et al. 2017
		United States
		Portugal		Pombo et al. 2020
		North China		Yang et al. 2022
	Perinereis linea	China		Sá et al. 2017
		China	US$ 0,32	Font et al. 2018
		Portugal		Pombo et al. 2020
	Perinereis helleri			Broquard et al. 2022
	Perinereis brevicirrata	Taiwan		Scaps 2003
	Platynereis dumerilii			Pombo et al. 2020
	Alitta succinea			Pombo et al. 2020
	Allita virens (Nereis virens)*			Klawe and Dickie 1957
		United Kingdom		Blake 1979a
				Olive and Cowin 1994
			US$ 40,78 kg^− 1	Sá et al. 2017
		England		Olive 1999
				Nesto et al. 2012
		United States		Creaser et al. 1983
			US$ 76,62 kg^− 1	Watson et al. 2017
		Europe		Cole et al. 2018
				Pombo et al. 2020
		Netherlands		Baits 2022
			US$ 96 kg^− 1	Mandario 2018
				Jayaseelan et al. 2021
				Goti et al. 2021
				Broquard et al. 2022
		United States Europe		Yang et al. 2022
	Namalycastis rhodochorde	Vietnam		Sá et al. 2017
		Vietnam	US$ 3,21	Font et al. 2018
		Vietnam		Pombo et al. 2020
	Platynereis dumerilii			Pombo et al. 2020
	Nereis pelagica			Pombo et al. 2020
	Neanthes nubila	Portugal		Pombo et al. 2020
	Neanthes spp	Spain France		Sardá 1989
	Neanthes acuminata (Nereis caudata)*	Spain France		Sardá 1989
	Perinereis oliveirae	Portugal
	Pseudonereis anomala	Egypt		Hamdy et al. 2014
	Cheilonereis cyclurus	North China		Yang et al. 2022
	Nereis vexilllosa	North China		Yang et al. 2022
	Hediste japónica (Neanthes japónica)*	China		Yang et al. 2022
Onuphidae	Diopatra spp.			Sá et al. 2017
	Diopatra cuprea			Olive 1994
		Italian coast (Santa Gilla Lake coast)		Gambi et al. 1994
				Scaps 2003
		Brazilian coast		Amaral and Jablonski 2005
				Sá et al. 2017
				Pombo et al. 2020
				Cabral et al. 2019
	Hyalinoecia tubícola	Spain		Sardá 1989
	Diopatra aciculata	Australia	US$ 119,87 kg^− 1	Watson et al. 2017
		Australia	US$ 107,93 kg^− 1	Cole et al. 2018
				Davies et al. 2008
			US$ 150	Mandario 2018
				Pombo et al. 2020
		Australia		Mandario 2020
				Broquard et al. 2022
	Diopatra neapolitana	Portugal		Cunha et al. 2005
		Portugal		Fidalgo e Costa et al. 2006
		Spain Italy Portugal		García del Real 2007
		Portugal		Da Fonseca and Fidalgo e Costa 2008
		Ria Formosa Sado estuary Aveiro estuary Portugal		Carvalho et al. 2013
	(Diopatra claperedii*)	Malaysia		Idris and Arshad 2013
		Portugal		Sá et al. 2017
		Portugal	US$ 7,41 kg^− 1	Watson et al. 2017
		Spain (Galicia and Cantabria)	US$ 0.75	Font et al. 2018
		Europe		Cole et al. 2018
				Pombo et al. 2020
		Portugal (Ria de Aveiro Coastal Lagoon)		Cabral et al. 2019
	Diopatra biscayensis	San Vicente de la Barquera estuary		Arias and Paxton 2015
	Americonuphis reesei	Costa Rica (Gulf of Nicoya)		Rojas and Vargas 2008
		Panamanian Pacific (Gulf of Montijo)		Vega et al. 2014
		Panama		Goti et al. 2021
	Australonuphis teres	Europe		Cole et al. 2018
	Australonuphis parateres			Cole et al. 2018
	Australonuphis sp.	United States		Yang et al. 2022
				Carrera-Parra 2021
	Hirsutonuphis sp.			Carrera-Parra 2021
Oenonidae	Halla parthenopeia		Small: US$ 8,04 Medium: US$ 10,71 Big: US$ 12,86	Font et al. 2018
				Sá et al. 2017
				Pombo et al. 2020
	Halla okudai	Malaysia		Idris and Arshad 2013
			US$ 46,21 kg^− 1	Saito et al. 2014
		Japan	US$ 0,46 100g	Cole et al. 2018
Nephyidae	Nephtys caeca			Olive and Cowin 1994
				Scaps 2003
				Pombo et al. 2020
	Nepthys spp.	Spain		Sardá 1989
		United Kingdom		Olive 1994
	Nephtys hombergii	Spain		Sardá 1989
		United Kingdom		Olive 1994
		United Kingdom		Olive and Cowin 1994
		Portugal		Sá et al. 2017
		Europe		Cole et al. 2018
				Pombo et al. 2020
	Nephtys cirrosa			Pombo et al. 2020
		Europe		Cole et al. 2018
Glyceridae	Glycera americana			Olive 1994
				Scaps 2003
				Carvalho et al. 2013
				Pombo et al. 2020
				Olive 1994
	Glycera dibranchiata			Klawe and Dickie 1957
				Olive and Cowin 1994
				Sypitkowski et al. 2008
		United States		Fidalgo e Costa et al. 2006
		United States		Da Fonseca and Fidalgo e Costa 2008
				Nesto et al. 2012
		North America Canada	US$ 1,07	Font et al. 2018
				Font and Lloret 2011
		United States		Sá et al. 2017
		United States	US$ 189,07 kg^− 1	Watson et al. 2017
		United States	US$ 200 kg^− 1	Cole et al. 2018
		United States		Pombo et al. 2020
			US$ 237 kg^− 1	Mandario 2018
	Glycera robusta	North America		Cole et al. 2018
	Glycera sp.			Jayaseelan et al. 2020
				Goti et al. 2021
Lumbrineridae	Scoletoma laurentiana (Lumbrineris impatiens* o Scoletoma impatiens)	Italian coast		Gambi et al. 1992
		Spain		Sardá 1989
				Gambi et al. 1994
				Olive 1994
				Scaps 2003
		Spain (Galicia)	US$ 0,96	Font et al. 2018
		Gulf of naples (Italian)		Messina et al. 2005
				Font et al. 2018
				Pombo et al. 2018
				Cabral et al. 2019
	Scoletoma spp.			Sá et al. 2017
Sabellidae	Sabella spallanzanii	Italian coast		Gambi et al. 1992
		Italian coast		Gambi et al. 1994
		Portugal		Sá et al. 2017
	Sabella pavonina			Sá et al. 2017
Sigalionidae	Sigalion squamosus	Spain (Catalonia)	US$ 1,29	Font et al. 2018
Opheliidae	Ophelia neglecta	Spain (Catalonia)		Font et al. 2018
	Ophelia bicornis	Portugal		Sá et al. 2017
	Ophelia radiata	Portugal		Sá et al. 2017
	Ophelia spp.	Italy Córcega		Bellán 1964
Spionidae	Scolelepis squamata	Algerian		Younsi et al. 2010
		Algerian	US$ 7,41 kg^− 1	Watson et al. 2017
Amphinomidae	Eurythoe complanata	Brazilian coast		Amaral and Jablonski 2005
Orbiniidae	Phylo nuda (Phylo nudus, S. nudus*)			Sá et al. 2017

The commercial value was standardized to the current economic value of the dollar in April 2023

Aquaculture

History

The first commercial cultivation of “polychaetes” began in 1984 (Olive 1999). Intensive commercial aquaculture of “polychaetes” has also been successfully carried out in countries like the United Kingdom by the company Dragon Bait, England by the company Seabait Ltd, and Holland and Ireland by the company Topsy Bait with the cultivation of Alitta virens (Nereis virens), also known as "ragworm". This has also occurred in Australia by the company Aquabait Ltd, which is dedicated to the cultivation of the "tube worm", Americonuphis reesei. In France, this has been achieved by the company Hemarina S.A. with the species Arenicola marina (Herrsera-Perez 2020) and Lumbrinereis impatiens. In Spain, the production of Hediste diversicolor (Nereis diversicolor, scientific name not accepted) and Arenicola marina is reported (García del Real 2007). Other examples of cultivation include the species Neanthes japonica in Japan; Perinereis brevicirrus in Taiwan; and the cultivation of Glycera dibranchiata and Alitta virens (Nereis virens) by Maine in the United States (Olive and Cowin 1994; Grupo de Ecología, Universidad de Cantabria y TEICAN Medioambiental S.L 2002).

Since then, “polychaete” aquaculture has shown sustained growth, thanks to the collaboration of industry, which has helped fund research on reproductive biology and the growth of polychaete annelids to meet the demands of aquaculture, sport fishing and the ornamental market (Murray et al. 2012; Palmer et al. 2016; Cole et al. 2018). Currently, its commercialization is evident in different forms, such as being sold live, frozen (Yang et al. 2022) dried, flaked, canned, or in the feed formula of species of commercial interest, like in shrimp brood stock as reported by Nascimento et al. (1991) and Mandario et al. (2018). This trade is considered a profitable business, and has one of the highest costs in the international market (Table 1).

“Polychaetes” as Food in Aquaculture

“Polychaetes” are the highly preferred prey of fish and shrimp in benthic communities of natural ecosystems (Böggemann 2009; Choi 2016; Younsi et al. 2010; Priscilla et al. 2022). As such, it can be and is used as a feed resource in aquaculture production systems (Dinis 1986; Fidalgo e Costa et al. 2000; Stabili et al. 2013; Broquard et al. 2022). They have high nutritional content, as they are rich in fatty acids (FA), especially polyunsaturated fatty acids (PUFAS) and essential FA, better known as highly unsaturated fatty acids (HUFAS) which make them a valuable feed ingredient for fish and crustaceans (Pairohakul et al. 2021; Olive 1999; Brown et al. 2011; Stabili et al. 2013; Moussa et al. 2015; Pajand et al. 2017; Sahu et al. 2017; Mandario 2020; Jerónimo et al. 2021b; Kannappan et al. 2021), especially when some of these HUFAS include arachidonic acid (AA), eicosapentaenoic acid (EPA), and docosahexaenoic acid (DHA) (Poltana et al. 2007; Pombo et al. 2018; Chimsung et al. 2014; Palmer et al., 2014; Kannappan et al. 2021). “Polychaetes” also have an adequate ratio of n3:n6 FA (Moussa et al. 2015), which makes them very important for shrimp, as they have a limited capacity to synthesize FA (Mussucci 2013). These essential FA favor the development and maturation of gonads (Fidalgo et al. 2003; Fidalgo e Costa et al. 2006; Kumar et al. 2017; Palmer et al. 2014; Mandario et al. 2020; Kannappan et al. 2021), help induce spawning in several fish and crustacean species (Parandavar et al. 2015; Muli et al. 2016; Wang et al. 2019a; Mandario 2020; Kannappan et al. 2021; Yang et al. 2022), interfering with fertilization, hatching rates, egg production, egg viability, larval survival, and spawning frequency in shrimp brood stock (Pajand et al. 2016; Jerónimo et al. 2021b). They also affect P. vannamei (L. vannamei), P. kerathurus, Penaeus monodon, Cryphiops caementarius and fish in the families of Sparidae: Pagellus bogaraveo "bream" (Moussa et al. 2015); and Soleidae: Solea senegalensis "senegal sole", S. vulgaris "sand sole", and Solea solea "common sole" (Fidalgo e Costa 1999; Meunpol et al. 2005; Safarik et al. 2006; Cardinaletti et al. 2009; Leelatanawit et al. 2014; Moussa et al. 2015; Panakorn 2015; Mandario 2020;Yang et al. 2022; Zavala-Zavaleta et al. 2022).

“Polychaetes” are also an important source of protein, amino acids and vitamins (Muli et al. 2016; Murugesan et al. 2011a; Stabili et al. 2013) and are a good source of reproductive hormones, similar to those found in shrimp (Mandario 2020; Kannappan et al. 2021). Chimsung et al. (2014), found that the reproductive hormones found in “polychaetes”, progesterone (P4) and 17α-hydroxyprogesterone, are responsible for the induction of oocyte development in shrimp. In addition, Meupol et al. (2010) report that prostaglandin E2 (PGE2) extraction in “polychaetes” has positive effects on oocyte maturation, specifically during late maturation and the ovulation period.

“Polychaetes” are marketed as live, frozen or dried feed (Bloodwormdepot 2022; Seaanglingireland 2022; Hookersbaits 2022; Baitsrus 2022; Valfishing 2022; Topsybaits 2022; Proaqua 2023).

Integrated Multi-Trophic Aquaculture (IMTA)

Before the development of Integrated Multitrophic Aquaculture, “polychaetes” were already used in polyculture systems. Ryther et al. (1975) exposed two detritivores feeding “polychaetes”, Nereis virens and Capitella capitata, with wastewater in a shellfish culture alongside other hydrobiological resources, resulting in an effluent free of inorganic nitrogen and bacterial growth which contributes to eutrophication. The growth of the aquaculture industry has subsequently led to integrated multi-trophic aquaculture (IMTA) as a way to increase sustainability by looking for different mechanisms to remediate and take advantage of all its production (Tsutsumi et al. 1991; Tomassetti et al. 2015; Martinez-Garcia et al. 2019; Wang 2019b; Galasso et al. 2020; Giangrande et al. 2020; Giangrade et al. 2021).

These systems are characterized by the integration of species from different trophic levels, involving a main production with species like fish, and a secondary production using crustaceans, bivalves and algae. The aim of these systems is to use all the resources produced economically, and in turn, control the organic (food waste, feces, bacterial biomass and plant material) and inorganic matter generated from the production of the main species and the system (Granada et al. 2015; Stabili et al. 2019; Wang et al. 2019b; Galasso et al. 2020; Jerónimo et al. 2021a). Due to their suspensivorous, deposivorous and detritivores feeding, as well as the nutritional content of some “polychaetes”, they have been considered for use in IMTA systems. This is demonstrated in the research by Giangrande et al. (2005), Stabili et al. (2013), and Stabili et al. (2019), who used S. spallanzanii as a biofilter in the remediation of wastewater from aquaculture, thus removing different groups of bacteria including potentially pathogenic bacteria for humans such as vibrios (Stabili et al. 2010). Likewise, Licciano et al. (2005) found that S. spallanzanii has high bacterial removal efficiency of Vibrio alginolyticus, and this was later confirmed by Blake and Giangrande (2011), Olivotto (2011) and Naspirán-Jojoa et al. (2022). Tsutsumi et al. (2002) also found that Capitella sp. 1 was an efficient bio-remediator of organically enriched sediments. Similarly, Kang et al. (2013), exposed the “Polychaete” Perinereis aibuhitensis to the toxicant endosulfan, a contaminant from aquaculture, concluding that it can effectively break down the toxicant in contaminated aquatic sediments. Gómez et al. (2018, 2019), reported that Abarenicola pusilla has the potential to reduce organic matter of wastewater from marine recirculating systems. Furthermore, Wang et al. (2019a, b), evaluated the potential of the “polychaete” Hediste diversicolor for the recycling of wastewater from aquaculture, concluding that the high-quality increase of protein and lipids make it a potential ingredient for aquaculture feed. This conclusion was shared by Jerónimo et al. (2021b) with the “polychaetes” H. diversicolor, Terebella lapidaria, Diopatra neapolitana and Sabella pavonina that showed high levels of polyunsaturated fatty acids, and demonstrating that it is possible to produce a biomass of polychaetes with high nutritional content in an integrated multi-trophic system. Other species include Capitella sp., Nereis virens (Brown et al. 2011), Perinereis nuntia and Arenicola loveni loveni (Gómez et al. 2018), Marphysa sp. (Mandario et al. 2019), and Arenicola marina (Jerónimo et al. 2021a). Species of the genera Nereis, Arenicola, Glycera and Sabella can also be used for temperate systems (Barrington et al. 2009); while the species Alitta virens (Nereis virens) can be used for tropical systems (Chopin et al. 2012). Hence, the integration of “polychaetes” within an integrated multi-trophic system, requires knowledge of the biological and physiological characteristics of the species of interest. In addition, a suitable taxonomic identification is needed, as- some species identified in the research have not been reported in their place of origin.

Table 2. Polychaetes species incorporated within the Integrated Multitrophic Aquaculture (IMTA) and cultured.
Familia	Especie	IMTA	Cultivadas	País o Región	Valor comercial	References
Eunicidae	Marphysa sanguinea		√		€0.50/indv.	Font et al. 2018
			√			Amran and Mohamad 2022
	Marphysa iloiloensis	√	√			Amran and Mohamad 2022
Dorvilleidae	Ophryotrocha labronica		√			Amran and Mohamad 2022
Onuphidade	Diopatra aciculata		√	Australia		Safarik et al. 2006
			√	Australia		Mandario 2020
			√	Australia		Proaqua 2022
			√			Broquard et al. 2022
	Diopatra cuprea		√	Italy		Gambi et al. 1992
	Australonuphis teres		√	Australia		Olive 1994
Nereididae	Allita virens		√	United Kingdom		Olive and Cowin 1994
			√	United Kingdom		Olive 1994
		√				Olive 1999
			√			Brown et al. 2011
			√	United Kingdom		García del Real 2007
			√	Netherlands United Kingdom		Da Fonseca and Fidalgo e Costa 2008
			√	Inglaterra y Paises Bajos		Mandario 2020
		√				Jerónimo et al. 2021b
			√			Broquard et al. 2022
			√			Amran and Mohamad 2022
	Neanthes aenaceodentata		√			Resih 1980
	Perinereis linea		√		€0.30/indv.	Font et al. 2018
	Perinereis helleri	√				Brown et al. 2011
			√	Australia		Mandario 2020
		√				Jerónimo et al. 2021b
			√			Broquard et al. 2022
	Perinereis brevicirrata		√	Taiwan		Mandario 2020
	Perinereis spp.		√	Sur de Japón		Mandario 2020
	Perinereis brevicirrus		√			Chen 1990
			√			Olive 1994
			√			Da Fonseca and Fidalgo e Costa 2008
	Pereniereis nuntia	√				Brown et al. 2011
			√	Thailandia		Mandario 2020
		√				Jerónimo et al. 2021b
			√			Broquard et al. 2022
			√			Amran and Mohamad 2022
	Perineries rullieri		√			Amran and Mohamad 2022
	Perinereis Vallata (Perinereis nuntia vallata)*	√				Brown et al. 2011
	Perinereis vancaurica		√	Korea		Grupo de Ecología, Universidad de Cantabria y TEICAN Medioambiental S.L 2002
	Platynereis dumerilli		√			Amran and Mohamad 2022
	Perinereis aibuhitensis		√			Da Fonseca and Fidalgo e Costa 2008
	Hediste diversicolor		√			Da Fonseca and Fidalgo e Costa 2008
			√			Broquard et al. 2022
		√				Brown et al. 2011
		√				Pajand et al. 2016
		√				Jerónimo et al. 2021a
			√			Amran and Mohamad 2022
	Hediste japonica		√	Japon		Kurihara 1983
			√			Amran and Mohamad 2022
	Perinereis vallata (*Perinereis nuntia vallata)	√				Honda and Kikuchi 2002
			√			Kurihara 1983
	Perinereis cultrifera		√	Italy		Ansaloni et al. 1986
			√	France		Bellan 1964
Arenicolidae	Arenicola marina		√			Broquard et al. 2022
		√				Jerónimo et al. 2021a
		√				Jerónimo et al. 2021b
	Arenicola defodiens		√			Broquard et al. 2022
	Abarenicola pusilla	√				Jerónimo et al. 2021b
Capitellidae	Capitella capitata	√				Brown et al. 2011
	Capitella sp		√			Amran and Mohamad 2022
Spionidae	Pseudopolydora vexillosa		√			Amran and Mohamad 2022
Serpulidae	Spirobranchus kraussii		√			Amran and Mohamad 2022
	Hydroides elegans		√			Amran and Mohamad 2022
Sabellidae	Myxicola infundibulum		√			Amran and Mohamad 2022
	Sabella spallanzanii	√				Jerónimo et al. 2021b
			√			Amran and Mohamad 2022
Dinophilidae	Dinophilus gyrociliatus (*Dinophilus gyrociliatus)		√			Amran and Mohamad 2022
Glyceridae	Glycera dibranchiata		√	EEUU		Creaser et al. 1983
Oenonidae	Halla parthenopeia		√	Spain		Sardá 1989

Ornamental Aquaculture

Additionally, it was demonstrated by Murugesan et al. (2011b) that the "clownfish", Amphiprion sebae’s consumption of “polychaetes” improves its physical appearance, resulting in an intensified color, as well as a greater weight and size, when compared to the consumption of fish feed (formula containing fish remains) and clam consumption. This skin pigmentation is a fundamental feature influencing the economic market and its production in aquaculture (Velasco-Santamaría and Corredor-Santamaria 2011). In addition, Hossen et al. (2014) identified that the polyunsaturated fatty acid (PUFA) content, an important component in gonadal maturation and spawning, is high in “polychaetes” with the "striped gourami" fish Colisa fasciatus achieving high quality larvae with the consumption of “polychaetes” (Sales and Janssens et al. 2003). Likewise, Khiabani et al. (2019), report that the combination of lipids and fatty acids are determinants for the reproductive success and survival of the offspring of ornamental fish, with fertility rate, egg production, gonad development and fecundity being important factors in the mass production of young fish and their final selection. Although the requirement of lipids and fatty acids will depend on the ornamental fish origin (freshwater or marine), both groups need long chain fatty acids and a high degree of unsaturation (Sales and Janssens et al. 2003) which can be provided by “polychaetes”. Furthermore, the different colors of “polychaetes” can provide ornamental fish with carotenoids, favoring color intensity (Sales and Janssens et al. 2003).

Parasites

Due to the characteristics of their habitat and ecological niche, as well as their abundance and location in the marine food web, “polychaetes” have the potential to contribute to the transmission of parasites, as they are the preferred food of species produced in aquaculture, like shrimp and fish (Huston et al. 2017). This was demonstrated by Desrina et al. (2020), which found Enterocytozoon hepatopenaei (Fungus, Microsporidia) in the polychaetes Dendronereis spp., Marphysa spp. and Nereis sp. from a shrimp aquaculture farm on the north coast of Java Island (Indonesia). Furthermore, they reported that this parasite was found in Penaeus monodon (Thailand) and Penaeus vannamei (Vietnam, Thailand and India). Likewise, the same authors Desrina et al. (2013) and Haryadi et al. (2015) found that the "white spot virus" (WSSV) is a host of the “polychaete” Dendronereis spp., as it is a favorite food of the mentioned shrimp. “Polychaetes” are also involved in the life cycle of myxozoans and aporocotylid blood flukes (Digenea), which use “polychaetes” during the production of their larvae, thus infecting fish with cercariae and actinospores of myxozoans, which are the most abundant in their habitat (Huston et al. 2017).

Impacts

Countries that harvest these species without any management plans, result in overexploitation and modification of the biotic and abiotic characteristics of their habitat and environment (Fidalgo e Costa et al. 2000, Çinar 2013, Carvalho et al. 2013, Godet et al. 2014, Kannappan 2021, Broquard et al. 2022), such as with the release and exposure of ammonium and phosphorus compounds that favor eutrophication (Watson et al. 2017) or the introduction of foreign invasive species (Blake and Giangrande 2011) that compete with native species. Çinar (2013), reported that the increase in these populations is responsible for the re-structuring of the food web, introducing new infectious agents or parasites, which modify the habitat structure and gene pool. This also results in economic losses. As a result, countries such as the United States, United Kingdom, Australia and Portugal, implemented regulatory measures for their harvest (De Cubber et al. 2018), such as requiring licenses for the use of recreational and professional fishing. Meanwhile, in northern France, a law was introduced to restrict the number of individuals harvested to 100, and the total closure of some Arenicola spp. harvest areas were ordered (De Cubber et al. 2018).

Other potential uses

Other potential uses of “polychaetes” include being a food attractant in the diet of pets and fish with partially cartilaginous skeletons, due to the high concentration of glycosaminoglycans (GAGs), as reported by Stabili et al. (2013) with Sabella spallanzanii.

Wang et al. (2019b) also reported that Hediste diversicolor could be a potential species for biogas production, due to its nutritional characteristics.

Meanwhile, Capa et al. (2021) suggest that “sabellids” can be used as models in biological regeneration, specifically for basic and functional development in regenerative ecology with polychaetes like Myxicola infundibulum; or Hydroides elegans for embryological research, larval ecology or studies in biofouling, as well as the species H. ezoensis and H. dianthus for larval ecology studies. Spirobranchus lamarcki can also be used as a model in molecular and embryological studies, and both H. elegans and S. triqueter can be used as models in ocean acidification and biomineralization.

The polychaete annelids Neanthes japonica and Perinereis nuntia (Perinereis nuntia var. Vallata) are potential species for the bioremediation of domestic wastewater (Kurihara, Y 1983).

Likewise, numerous studies suggest that “polychaetes” have medical applications for human health (Kuijk and van Die 2010; Singh et al. 2014; Coutinho et al. 2017; Herrera-Perez 2020, García-Garza et al. 2021; Broquard et al. 2022). For example, different biopharmaceutical products can be obtained from Arenicola marina hemolymph such as HEMO₂life, which can be used for transplant organ preservation; HEMOXYCarrier, which can be used as a universal oxygen carrier with potential use in blood transfusions, and HEMHealing, which can be used as dressing for chronic wound healing (Hemarina 2023).

Finally, research with Polychaete annelids is not only restricted to feed species of commercial interest in the reproductive stage. According to the Ecology Group, University of Cantabria, TEICAN Medioambiental S.L. (2002), Kolkovski et al. (1997) and Kolkovski (2000) report that polychaete annelids have been considered as a food source for fish larvae. It should be noted that within the life cycle of polychaete annelids, larvae can be a food alternative to artemia, copedecids and rotifers for fish and/or shrimp larvae, and this is an area that requires further study. Thus, the knowledge of polychaete annelids requires different areas of research and application.

Present and future in Latin America

Currently, Latin American countries are becoming increasingly interested in the production of polychaete annelids for the shrimp industry, with Naranjo and Tobías (2019) in Ecuador exploring species with aquaculture potential and concluding that the species Perinereis sp. is most optimal for reproduction and production in captivity. Likewise, in Chile, they have successfully reproduced “polychaete” species of the Nereididade family, including Perinereis gualpensis, Perinereis vallata, and of the Arenicolidae family, including Abarenicola pusilla. The collaboration of the company MARINAZUL S. A, and Ricardo Palma University in the project: "Technical Assistance and Training for the development of the Cultivation and Use of Nereis and Perinereis “polychaetes” as live and/or pelletized food in the aquaculture production of the company MARINAZUL S. A" as indicated in the subproject code PNIPA-ACU-SEREX-PP-000143, has enabled the transfer of knowledge and technology to neighboring countries like Peru, where the present author was part of the technical team on behalf of the University. However, regrettably, the company prioritized its own qualifications, and truncated lines of research at the biological and biotechnological levels.

In Mexico, Nuria Méndez (2016) and Dávila-Jiménez (2017) bred Capitella and Bispira brunnea at the laboratory level for research purposes, respectively. Their goal was to develop local “polychaete” worm culture technologies to meet the demand in shrimp and fish aquaculture, as well as ornamental aquaculture and sport fishing through technology transfer of research results to the productive sector. To this end, it is important that companies commit themselves to collaborate in an integral manner with research projects. Otherwise, it will result in research setback that would not be beneficial for the sector. In an initial phase, the aquaculture potential of local “polychaetes” of every Latin American country should be evaluated, and used as an alternative to live, frozen or dehydrated feed and food supplements. It is important to first determine their biochemical composition (carbohydrates, protein, lipids, fatty acids, amino acids and biomass), safety (detection of pathogens) and culture viability (ease of sampling of brood stock, maintenance in captivity, reproduction and obtaining viable larvae) before continuing onto the next stage. The second stage will involve the design and development of a method for production of pilot cultures of “polychaetes” which will be used to determine the optimal diets that will help increase the efficiency of shrimp and fish production. The third and final stage will be to determine the distribution presentation as food in order to conserve its properties. It is expected that the production and cultivation of “polychaetes” as an alternative feed for aquaculture will be more relevant in Latin American countries to reduce feed costs and be an additional and competitive alternative to those found in the market. It will also serve to open up different areas of research for the benefit of society.

“Polychaete” annelids are an alternative food resource for aquaculture, promoting the circular economy by reducing costs of cultivation or production, as well as providing essential nutrients for the species of interest. As such, it is important and fundamental that different countries select the polychaete annelid species that is most suitable for their needs. Likewise, “polychaete” aquaculture should be a tool used to expand into other areas of scientific research such as physiology, genetics, neurobiology, immunology, biochemistry, biotechnology, developmental biology, reproductive biology, molecular biology, and pharmacology.

RECOMMENDATIONS

Finally, it is important to emphasize that applied research is inseparable from basic research. This article discusses the ecology, correct taxonomic identification, and physiology of “Polychaete annelids”, which is essential knowledge needed for their successful production or cultivation in laboratory, regardless of whether it is intensive, semi-intensive or extensive.

ACKNOWLEDGMENTS

I would like to thank Dr. Maria Ana Tovar-Hernández, Dr. Gema Hidalgo, Dr. Sergio Salazar Vallejo and Dr. Victor Torres for their suggestions, corrections and comments. Thank you very much for your willingness to help. This article is dedicated to Dr. Nuria Mendez Ubach, a beautiful person and scientist. It is thanks to her support that I began my studies of polychaete annelids. Farewell dear Nuri.

The authors declare that no funds, grants, or other support were received during the preparation of this manuscript. The authors did not receive support from any organization for the submitted work. No funds, grants, or other support was received.

Competing Interests

“The authors have no relevant financial or non-financial interests to disclose”.

Research Data Policy and Data Availability Statements

Data availability

Data sharing not applicable to this article as no datasets were generated or analysed during the current study.

Ethical Responsibilities of Authors

Author contributions

All authors contributed to the study conception and design. The idea for the article, performed the literature search, data analysis, and drafted and critically revised the work by Melissa Herrera Perez.

Disclosure statement

The authors have no relevant financial or non-financial interest to disclose. The authors have no competing interest to declare that are relevant to the content of this article. All authors certify that have no affiliations with or involvement in any organization or entity with any financial interest or non-financial interest in the subject matter or material discussed in this manuscript. The authors have no financial or proprietary in any material discussed in this article.

“Ethics approval”

No approval of research ethics committees was required to accomplish the goals of this study because this an article review.

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Aquaculture of Polychaete annelids and their importance for Latin America

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Abstract

INTRODUCTION

MATERIALS AND METHODS

Ornamental Polychaete Annelids

Sport fishing

Aquaculture

History

Integrated Multi-Trophic Aquaculture (IMTA)

Ornamental Aquaculture

Parasites

Impacts

Other potential uses

Present and future in Latin America

CONCLUSIONS

RECOMMENDATIONS

Declarations

References

Additional Declarations

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