Adaptation and potential culture of wild Amphipods and Mysids as potential live feed in aquaculture: a review

Morphology characteristics and distribution: Amphipods and Mysids

Amphipods

Amphipoda (Crustacea, Malacostraca) is a major aquatic, estuarine, and terrestrial freshwater taxon. They live in pelagic and benthic compartments with various life patterns, ecosystems, environmental requirements, and ecological feeding (Podlesińska & Dąbrowska, 2019). The previous study indicates that amphipods are commonly used for assessing the quality of marine and estuary sediment, mostly due to their habitat preferences and lifestyle. Amphipods are herbivores, detritivores, scavengers, omnivores, or parasites and are important live feeds in marine ecosystems (Podlesińska & Dąbrowska, 2019). Amphipods such as gammarids and corophiids have laterally and dorsoventrally compressed bodies. According to Hyne (2011), sexual dimorphism and reproductive strategies vary within species. By looking at the presence of marsupium, a mature female can be identified. In contrast, the mature male can be identified by the emergence of genital papillae on the body’s ventral side (Podlesińska & Dąbrowska, 2019). In preparation for the next spawning, gravid females with embryos developing in the outer marsupial sac, oocyte maturation within their ovaries. In exchange, amphipods bear their broods, which extend their breeding cycle after spawning (Hyne, 2011). Amphipods are commonly used as model organisms for determining the quality of marine and estuarine sediments due to their nature and lifestyle (Chapman, Wang & Caeiro, 2013; Podlesińska & Dąbrowska, 2019). Epibenthic amphipods, such as gammarids, are abundant and ecologically important parts of marine benthic habitats since they interact closely with sediment and are easy to manage and culture in the laboratory (Hyne, 2011). As for Malaysian waters, the knowledge of amphipods has been poorly studied (Lim, Azman & Othman, 2010). Even though eleven taxa, including the new species of grammarian amphipods, have been recorded by Azman & Othman (2013) in Pulau Tioman waters, this results in additional documented amphipods and provides new information on the range and distribution pattern of amphipods in the South China Sea. The amphipod genus Grandidierella is comprised of more than 43 species that have been documented worldwide (Wongkamhaeng et al., 2020; Shahin et al., 2023a). The genus has a wide distribution in marine habitats, including brackish, estuarine, and coastal waters (Azman & Othman, 2012; Myers & Desiderato, 2019; Myers, Sreepada & Sanaye, 2019). In addition to their potential application as live food in aquaculture (Jourde et al., 2013; Lo Brutto et al., 2016), certain species are utilized as an indicator in studies on the toxicity of sediments (Hindarti et al., 2015). G. halophila is a newly discovered species from the Aoridae family, identified by Wongkamhaeng, Pholpunthin & Azman (2012). It was found in the hypersaline waters of salt flats in the Samut Sakorn district, Thailand, located in the Inner Gulf of Thailand. The amphipods G. halophila, which are naturally abundant in the lagoons at Pantai Sri Tujuh in Kelantan, Malaysia, were discovered by Shahin et al. (2023a). This discovery makes the amphipods easily accessible to researchers for their study as a potential new feed resource for aquaculture. Figure 1 shows a morphological diagram of adult amphipods.

Mysids

The shrimplike crustaceans, Mysids that commonly referred to as “opossum shrimps,” are common in both marine and freshwater environment (Ogonowski et al., 2013). Most mysids range in size from 5 to 25 mm, although deep-water species are generally larger, with the largest species known having lengths of up to 350 mm (Porter, 2016). Distinguishing mysid features include the presence of a statocyst in the uropod (but absent in six out of nine families) and, in females, the presence of a marsupium, also known as the brood pouch which is the basis of the group’s common name, “opossum shrimps” (Porter, 2016). Mysid species are omnivorous and cannibalistic (Berezina, Razinkovas-Baziukas & Tiunov, 2017). The stomach of mysids gathered along the coast includes detritus, tiny crustacean bodies and appendages, and limited numbers of diatom shells (Herrera et al., 2011). Male mysids can be recognized by the presence of panels and secondary sexual characteristics, while females have a marsupium presence (Ramarn, Chong & Hanamura, 2012). Mysid shrimps are prevalent crustaceans found in a variety of aquatic environments such as oceans (~95%), estuaries, brackish water ecosystems, and freshwater lakes (Viherluoto & Viitasalo, 2001; Miyashita & Calliari, 2016). They are highly adaptable species and thus proficient in colonizing new territories (Ketelaars et al., 1999; Viherluoto & Viitasalo, 2001; Rastorgueff et al., 2015). Mysids are one of the most morphologically diverse classes of crustaceans (Tan & Rahim, 2018). They are good candidates for determining endocrine disruption due to the abundance of information available on their endocrinology (Verslycke et al., 2004). Mysids are highly abundant and widely distributed crustaceans, inhabiting various aquatic areas, with a particular preference for marine environments (Gan et al., 2010). Mysid is a significant constituent in the shallow coastal and estuarine waters, serving a crucial function in the transfer of energy from lower to higher trophic levels (Mauchline, 1980; Mees & Jones, 1997; Yolanda et al., 2023). The spatial distribution of crustacean zooplankton has been documented to be affected by tidal waves or water currents (Hall & Burns, 2003; Macías et al., 2010; Yolanda et al., 2023). There are 41 species of mysids recorded in Peninsular Malaysian waters (Tan, Azman & Othman, 2014), with the most common being Erythrops minute, Mesopodopsis orientalis, Acanthomysis longispina, Acanthomysis quadrispinosa, Lycomysis spinicauda, Pseudanchialina inermis, and Prionomysis aspera. The first mysid species from Malaysian waters was recorded by Tattersall (1965), in the northern region of the Malacca Straits. Several mysid species belonging to the Anisomysini tribe have been found in the waters of Southeast Asia (Sawamoto, 2014; Nurshazwan, Sawamoto & bin Abdul Rahim, 2021). Two species, which is Anisomysis (Anisomysis) aikawai Ii, 1964 and A. (Paranisomysis) ohtsukai Murano, 1994, have been recorded from Malaysian waters (Gan et al., 2010; Tan, Azman & Othman, 2014; Tan & Rahim, 2018) and there was no record of any mysid of the genus Idiomysis. However, recent study by Nurshazwan, Sawamoto & bin Abdul Rahim (2021) has found another species of Idiomysis, which is Idiomysis bumbumiensis sp. nov. that was found at Pulau Bum Bum, Sabah, Malaysia. Species found is the seventh member of the genus Idiomysis and it is the first described in Southeast Asia (Nurshazwan, Sawamoto & bin Abdul Rahim, 2021). Figure 2 shows a morphological diagram of adult mysids.

Reproductive biology of Amphipods and Mysids

Amphipods

Amphipods have a direct development from juvenile to adulthood; after the juveniles are released from the females’ brood chambers, they undergo several molts without metamorphosing before becoming adults (Väinölä et al., 2008; Baeza-Rojano et al., 2010). The molt cycle can be divided into four periods, which are post-molt, inter-molt, pre-molt, and ecdysis. The first stage, which starts at the end of the aged exoskeleton shedding, is known as an early post-molt period. The second stage starts with the incremental coloring of the antennas and legs. During the late post-molting cycle, the calcareous concrete within the posterior caeca is then used to mineralize the fresh skeleton. After that, during intermolting process, secretion of calcium carbonate and calcification of the last layer will continue to consolidate, which make up to 40% of the crustaceans’ cuticle. When the new skeleton is gradually developed under the aged one, it shows that it is entering the pre-molting period (Hyne, 2011). Molting and oogenic processes are closely related to malacostracan crustaceans, which have a high degree of fecundity and body development (Subramoniam, 2000). In preparation for the next spawning, sexually mature females with developing embryos in their external marsupial pouches undertake concurrent oocyte maturation within their ovaries. Also, amphipods bear their broods beyond spawning, extending their breeding period. The initiation of molting in these species is postponed until their juveniles are hatched and released (Sainte-Marie, 1991). The molting of the rigid exoskeleton happens at the same time as the ovarian cycle. This lets the newly fertilized oocytes move to the oviducts through the marsupium while the exoskeleton is still strong enough to let them through (Hyne, 2011). According to Sainte-Marie (1991), Baeza-Rojano et al. (2011), and Shahin et al. (2023a), amphipods such as Grandidierella halophila, Pontoporeia affinis, Orchestia mediterranea, Caprella grandimana, and Gammarus palustris have iteroparous, semiannual, multivoltine life histories that produce multiple broods in a brief lifespan. The characteristics of tropical amphipods can be defined by their maturation time, size and length of brood, fecundity rate, and juveniles’ development (Cunha, Moreira & Sorbe, 2000b; Grabowski, Bacela & Konopacka, 2007; Baeza-Rojano et al., 2013b; Xue et al., 2013; Shahin et al., 2023a, 2023b). According to Wang et al. (2009), a female of Grandidierella japonica can produce 13 to 17 juveniles from four broods in their lifespan. Previous studies have documented that among different species of amphipods, the number of embryos per brood varies. As an example, in average, Cymadusa filosa produces 20 juveniles, Parhyale hawaiensis produces 13 juveniles, Elasmopus pectenicrus produces seven juveniles, Elasmopus levis produces 22 juveniles, and Eogammarus possjeticus produces from 48 to 16 juveniles in their lifespan (Borowsky, 1986; Aravind et al., 2007). Understanding the potential fecundity of amphipods depends on a variety of aspects of their reproductive biology (Wang et al., 2009). Cymadusa vadose, a marine amphipod, was studied and reported by Shahin et al. (2023c) with the aim of assessing its potential as a new potential live feed. The amphipods that were obtained from the offshore at Bidong Island, Terengganu, were cultivated in filtered water with a salinity of 30 ppt at 28 °C in transparent plastic containers with a capacity of 500 mm. The life history of C. vadosa was observed by studying juveniles, individuals from a single offspring with five replicates. This species had a life history pattern characterized by two reproductive cycles each year and several generations. The duration required for the female to reach maturity was recorded as 17.4 days, with a corresponding size of 4.10 mm at the moment of maturation. The average duration of the incubation period was found to be 7.4 days. The average longevity for males was found to be 81.2 days, whereas females had a longer average lifespan of 113.6 days. The average number of broods generated during the course of an individual’s lifetime was found to be 4.2 days. The brood sizes exhibited a wide range, spanning from 3 to 40 youngsters, with an average of 24.5 individuals per brood. The female population had a reproductive output of 103.0 offspring during their whole lifespan. A highly significant positive connection, with a coefficient of determination (R2) of 0.97, was observed between the size of female individuals and the quantity of offspring they generated. The observed mean maximum length of males and females across their lives was 5.95 and 6.11 mm, respectively. The initial examination of the life cycle of C. vadosa provides a basis for further investigations into its viability as a substitute live feed in aquaculture. Figure 3 shows the general life cycle of amphipods that have been modified from Birmingham et al. (2005).

Mysids

Numerous species of tropical mysids have been found to reproduce continuously throughout the year (Hanamura, Siow & Chee, 2008; Hanamura et al., 2009; Biju & Panampunnayil, 2010; Biju, Gireesh & Panampunnayil, 2010; Ramarn, Chong & Hanamura, 2012). Mysid reproductive biology resembles that of marsupials, including an embryonic stage, a nauplioid stage, and a post-nauplioid stage (Wittmann, 1981; San-Vicente, Guerao & Olesen, 2014). Mysid female marsupium has three distinct but sequential stages of development, from oviposition to early embryonic stages (Wortham-Neal & Price, 2002). At some point during her ecdysis, the mother will release her young before laying another clutch of eggs in the marsupium. Oocytes undergo a secondary vitellogenic phase beginning on day two of the molten stage (Verslycke et al., 2004). In crustaceans, including amphipods, isopods, and decapods, secondary vellogenesis is cyclical and closely associated with the molten stage, serving as an example of a two-type form for the control of concurrent gonadal and somatic development (Verslycke et al., 2004). Therefore, the average number of mysids in females that are ovigerous could be used to guess how long the embryonic, nauplioid, and post-nauplioid phases last (Mauchline, 1973; Wortham-Neal & Price, 2002). The nauplioid stage, the embryonic stage, and the post-nauplioid stage occur in progressively shorter succession as development proceeds (Mauchline, 1980; Delgado et al., 2013). According to Yolanda et al. (2023), mysids, Rhopatophtalmus hastatus brooding females with the nauplioid stage have a larger proportion than the brooding females with the embryonic and post-nauplioid stages. The mean body length among the brooding females, females with the naupiolid stage were the largest (10.73 ± 0.14 mm), followed by the post-naupiolid stage (10.67 ± 0.15) and embryonic phase (10.20 ± 0.13 mm) (Yolanda et al., 2023). While the number of offspring in a given brood may vary greatly amongst mysid species, in general, tropical mysids are smaller overall and have fewer broods than their temperate counterparts, who are bigger overall and have more broods (Mauchline, 1980; Fenton, 1992; Mees, Abdulkerim & Hamerlynck, 1994). Rhopalopthalmus hastatus may lay as many as 17 eggs at once. Rhopalopthalmus indicus, Rhopalopthalmus mediterraneus, and Rhopalopthalmus tattersallae are all in the same genus and each have between 13 and 31 larvae (Grabe, 1989; Baldó et al., 2001; Biju, Gireesh & Panampunnayil, 2010). Brood loss or abortion during data collection, storage, and experimental processing accounts for differences in brood size, as stated by Murtaugh (1989) and Paul et al. (2016). In contrast, the brood limits for temperate mysids like Archaeomysis articulata, Gastrosaccus spinifer, Orientomysis japonica, and Neomysis integer are 93, 162, 102, and 88, respectively (Hanamura, 1999; Rappé et al., 2011; Akiyama, Ueno & Yamashita, 2015). Little is known about the factors affecting brood size, although a study on R. hastatus by Yolanda et al. (2023) indicated a substantial correlation between the size of the brood and the length of the brooding females. This indicates that a larger marsupial mother is capable of producing and caring for a larger brood (Saltzman, 1996). Figure 4 shows the general life cycle of mysids that have been modified from McKenney (2005).

Culture method

Nutritional value of Amphipods and Mysids

In order to increase the production of aquaculture, knowledge of the biochemical profile of marine organisms is vital for the discovery of new live feed that can be used effectively. According to Leaver et al. (2008), fish larvae required essential fatty acids (EFAs) such as polyunsaturated fatty acids (PUFAs) and highly unsaturated fatty acids (HUFAs) for sustainable growth and survival. In addition, both amphipods and mysids also show adequate characteristics for use as live feed in aquaculture, such as suitable optimum sizes (0.3–2.5 cm), digestibility, and an adequate amount of lipids (10–15%) and protein (~40%) in dry weight (Jiménez-Prada et al., 2018; Lee et al., 2020; Jiménez-Prada, Hachero-Cruzado & Guerra-García, 2021).

Potential feed enhancement for Amphipods and Mysids

Research on marine amphipods and mysids has been stimulated by the need to find substitute live feed for aquaculture marine fish and crustaceans’ species (Shahin et al., 2023b). Live food such as Artemia, rotifer, and copepod are common species that are used in marine aquaculture; however, to fill in the lack of long-chain HUFA, especially DHA in the rotifer and Artemia, they need to be enriched with a fatty acid (Rasdi & Qin, 2016; Azani et al., 2023). The same also goes for the amphipods and mysids, even though they already contain high nutritional value, as reported by Woods (2009) and Eusebio, Coloso & Gapasin (2010), they still need to be fed with microalgae or zooplankton, which can help in increasing growth and population size. A nutritional enrichment of Phronima pacifica, a type of Amphipoda microcrustacean, has been studied by Herawati et al. (2020) by enriching them with two species of microalgae, which are Chlorella vulgaris and Chaetoceros calcitrans. Their study has found that P. pacifica mass-cultured with C. vulgaris resulted in the highest biomass, growth, and proteins and fats of P. pacifica. Gammaridan amphipod Gammarus insensibilis was proven by Jiménez-Prada et al. (2018) to possess all the characteristics for supplementing formulated diets in aquaculture due to its good biochemical composition, such as proteins, lipids, and amino acids for feed (live or dry), but they still need to be enriched with a fatty acid. The research by Awal, Christie & Nieuwesteeg (2016) on a different type of feed for caprellid amphipods reveals that the caprellids fed on Phaeodactylum tricornutum showed massive development and reproductive performance, resulting in an increase in population size. Other than microalgae and zooplankton as feed for amphipods, a study by Jiménez-Prada, Hachero-Cruzado & Guerra-García (2021) found that waste products such as detritus are useful for amphipod culture and provide a desirable biochemical profile. The use of detritus as a waste product to feed amphipods is an interesting topic due to its advantages of being cheap to produce.

Mysids are frequently used by aquarium hobbyists or in laboratory settings as a food source for a variety of aquatic species, such as cuttlefish, seahorses, and fish. They are also considered alternative live foods for the culture of marine species (Oliveira et al., 2023). In mysid culture, Artemia nauplii is usually used as feed; however, due to the expensive cost of Artemia cyst, a less expensive feed needs to be found to produce mass culture. Table 4 shows the major nutritional components and examples of live feed enrichment diets that were used by other researchers and farmers as guidelines to find a suitable diet for live feed culture and enrichment. Therefore, to meet the nutritional requirements of fish and prawn larvae, it is crucial to study the nutritional composition of enrichment diets so that it will contribute to the healthy development of fish during their early critical life stages. Live feeds that are enriched with essential nutrients are one of the crucial factors for the growth performance of fish larvae (Ma & Qin, 2014). Enrichment diets provide live feeds with the adequate amount of nutritional value necessary for survival, growth, and stability. Achieving natural live feeds, including amphipods and mysids, with higher growth rates, stress tolerance, and good nutritional quality after enrichment are goals in the aquaculture industry in order to produce better-quality fish larvae with high growth rate (Li, Zheng & Wu, 2021). Numerous studies have focused on establishing methods for enhancing the nutritional quality of live feed with nutrients such as protein, lipids and fatty acids (Kandathil Radhakrishnan et al., 2020). In aquaculture, enriched zooplankton is essential for improving the nutritional value of fish and shellfish.

Potential use of Amphipods and Mysids as alternative live feed in aquaculture

Amphipods and mysids have been recognized as crucial natural prey for various marine species. Studies on the nutritional effects of their partial substitution for fish meal in fish diets have produced promising results. Amphipods and mysids have been reported to be essential components of aquatic food webs in the wild because they act as conduits of nutrients and energy to higher trophic levels (Shahin et al., 2023b). Hence, their potential use for aquaculture species under captivity and laboratory conditions is ecologically acceptable. Live feeds, including amphipods and mysids, provide a suitable initial feed for fish and shrimp larvae compared to fish pellets due to their ability to swim in the water, which stimulates a feeding response in larvae, and also because they are high in digestibility and provide adequate nutrients (Kandathil Radhakrishnan et al., 2020). Protein and lipid are crucial for the growth, development, and survival of fish and shrimp larvae. A study on the use of amphipod meal as a fishmeal substitute on grey mullet has been conducted by Ashour et al. (2021). Their result shows that amphipod meal with 50% partial replacement with fishmeal has benefited growth performance, feed utilization, and the histological and economic status of grey mullet (Mugil cephalus) fry. Table 5 shows a comparison of the proximate biochemical compositions of fishmeal and amphipod meal based on the study by Ashour et al. (2021). According to their results, fishmeal has a higher amount of crude protein, while amphipod has produced a higher amount of ether extract and crude fiber than fishmeal.

The dependence on Artemia as a feed for newly hatched larvae greatly impacts the aquaculture industry. Artemia is essential to the marine fish and ornamental industries due to its high nutritional content to satisfy the need for fish culture. A recent study introduced a new live feed such as amphipods and mysids to solve this problem. Research by Baeza-Rojano et al. (2013b) was the first to be able to grow caprellid amphipods in cultivation tanks big enough to achieve adequate densities for possible use as live feed for fish, with a maximum density of 10,460 individuals m⁻² and an average of 3,625 individuals m⁻² on the artificial substrates, which were dominated by juveniles. There has been a record of a few researchers using amphipods as feed for larvae rearing, such as in a study by Vargas-Abúndez, Simões & Mascaró (2018), who have already experimented by feeding the amphipods to the lined seahorse Hippocampus erectus. Therefore, Baeza-Rojano et al. (2010) also reported that they have used the amphipods as alternative prey to culture cuttlefish Sepia officinalis hatchlings. Both of these experiments have shown the positive result that the amphipods can successfully help in the growth and development of lined seahorse H. erectus (Vargas-Abúndez, Simões & Mascaró, 2018) and hatchlings of cuttlefish S. officinalis (Baeza-Rojano et al., 2010). In addition, González, Pérez-Schultheiss & López (2011) also did a test on feeding the amphipod Jassa marmorata to the “Baby Octopus” Robsonella fontaniana paralarvae. Based on the research that has been done on amphipods, it shows that a suitable substrate and feed play an important role in successfully culturing amphipods. Different species of amphipods need a different type of substrate and feed according to their habitat. It shares the same concept as zooplankton such as copepods, where the availability of various food sources is essential to enhance the nutritional value of live feed culture in hatcheries (Yuslan et al., 2022b). Other than that, mysids also show great potential as an alternative live feed. Mysid is one of the major constituents in coastal areas and estuaries that is important in transporting nutrients in the form of energy at trophic levels from low to high (Yolanda et al., 2023). Mysids are also regarded as the primary source of food for fish and crustaceans (Oh, Hartnoll & Nash, 2001; Link, Bolles & Milliken, 2002; Tomiyama, Uehara & Kurita, 2013). Mysid culture has been recorded by Wittmann (1984), Domingues et al. (1998), and Domingues et al. (1999).

Previous studies pointed out that the problem in the culture of mysids is the use of Artemia nauplii as a feed that is expensive and not economically sustainable for commercial culture. Aquaculturists and hatcheries are currently struggling with the cost of producing cysts for commercial hatchery operations, as well as the labor and infrastructure costs associated with producing live Artemia to operate hatcheries. As a result, alternative zooplankton options are required for hatchery propagation (Aziz et al., 2023). Thus, to ensure the effectiveness of aquaculture activities, scientists are concentrating their efforts on the development of low-cost live feed alternatives (Suhaimi et al., 2023). Both amphipods and mysids show great potential as an alternative live feed in the aquaculture industry. However, research findings on these two live feeds are still limited. Furthermore, more research is needed to look into how to grow a lot of amphipods and mysids, how different water conditions affect the reproduction of amphipods and mysids, how to make their food better, and how to find species that are good for farming. These research efforts are crucial for gaining a comprehensive understanding of the potential future use of these live feeds in aquaculture.