Abstract
Amphipods are emerging as an alternative food resource for fishes and cephalopods in aquaculture. Gammarus insensibilis (Stock, 1996), one of the dominant amphipods inhabiting marsh ponds in southern Spain, has been recently proposed as a promising candidate for being intensively cultured due to its adequate nutritional profile, large body size, and high natural densities. The main aim of this study was to determine whether waste products of aquaculture (such as detritus in the form of fish feces or Ulva sp.) provided an adequate diet for the amphipod in comparison to other traditional diets, such as Artemia nauplii or phytoplankton. G. insensibilis was cultured twice in tanks with 5 treatments: 4 experimental diets (detritus, Ulva sp., Artemia nauplii, and phytoplankton) were used, and one no-feed treatment. Amphipods fed with the two alternative diets, detritus and Ulva, showed promising survival higher than 40% and high concentrations of palmitic acid (16:0), oleic acid (18:1n9), arachidonic acid (20:4n6) (ARA), eicosapentaenoic acid (20:5n3) (EPA), and docosahexaenoic acid (22:6n3) (DHA). Therefore, large-scale culture of this amphipod using inexpensive diets in indoor facilities could provide a nutritious product for aquaculture. The potential development of a sustainable culture using this species in marsh ponds is also discussed in the context of Integrated Multi-Trophic Aquaculture (IMTA).
Similar content being viewed by others
References
Alavi Yeganeh MS, Abedian Kenari AM, Rezaii M (2008) Effect of Gammarus powder as a supplementary diet on growth and survival of rainbow trout larvae (Oncorhynchus mykiss). Pajouhesh Sazandegi 77:113–123 (In Persian with English abstract)
Alberts-Hubatsch H, Slater MJ, Beermann J (2019) Effect of diet on growth, survival and fatty acid profile of marine amphipods: implications for utilisation as a feed ingredient for sustainable aquaculture. Aquac Environ Interact 11:481–491
Anderson MJ (2005) PERMANOVA, a FORTRAN computer program for permutational multivariate analysis of variance. Department of Statistics, University of Auckland, New Zealand
Arias A, Drake P (1999) Fauna acuática de las Salinas del Parque Natural Bahía de Cádiz. EGMASA, Sevilla
Baeza-Rojano E, García S, Garrido D, Guerra-García JM, Domínguez P (2010) Use of amphipods as alternative prey to culture cuttlefish (Sepia officinalis) hatchlings. Aquaculture 300:243–246
Baeza-Rojano E, Domínguez P, Guerra-García JM, Capella S, Noreña-Barroso E, Caamal-Monsreal C, Rosas C (2013) Marine gammarids (Crustacea, Amphipoda), a new live prey to culture Octopus maya hatchlings. Aquac Res 44:1602–1612
Baeza-Rojano E, Hachero-Cruzado I, Guerra-García JM (2014) Nutritional analysis of freshwater and marine amphipods from the Strait of Gibraltar and potential aquaculture applications. J Sea Res 85:29–36
Christie WW (1982) A simple procedure for rapid transmethylation of glycerolipids and cholesteryl esters. J Lipid Res 23:1072–1075
Clarke KR, Gorley RN, PRIMER v5 (2001) User manual/tutorial. PRIMER-E, Plymouth, UK
Correia AD, Costa MH, Luis OJ, Livingstone DR (2003) Age-related changes in antioxidant enzyme activities, fatty acid composition and lipid peroxidation in whole body Gammarus locusta (Crustacea: Amphipoda). J Exp Mar Biol Ecol 289:83–101
Coste O, Malta E, López JC, Férnandez-Díaz C (2015) Production of sulfated oligosaccharides from the seaweed Ulva sp. using a new Ulvan-degrading enzymatic bacterial crude extract. Algal Res 10:224–231
Costello M, Bellan-Santini D (2017) Gammarus insensibilis Stock, 1966. In: Horton T, Lowry J, De Broyer C, Bellan-Santini D, Coleman CO, Daneliya M, Dauvin JC, Fišer C, Gasca R, Grabowski M, Guerra-García JM, Hendrycks E, Holsinger J, Hughes L, Jaume D, Jazdzewski K, Just J, Kamaltynov RM, Kim YH, King R, Krapp-Schickel T, Le Croy S, Lörz AN, Senna AR, Serejo C, Sket B, Tandberg AH, Thomas J, Thurston M, Vader W, Väinölä R, Vonk R, White K, Zeidler W. World Amphipoda Database. Accessed through, World Register of Marine Species at http,//www.marinespecies.org/aphia.php?p=taxdetailsandid=102280 on 2017-04-25
D’Avanzo CD, Valiela I (1990) Use of detrital foods and assimilation of nitrogen by coastal detritivores. Estuaries 13:20–24
De Broyer C, Jazdzewski K (1996) Biodiversity of the Southern Ocean, towards a new synthesis for the Amphipoda (Crustacea). Boll Museo Civico Storia Nat Verona 20:547–568
Deegan LA, Peterson BJ, Portier R (1990) Stable isotopes and cellulase activity as evidence for detritus as a food source for juvenile Gulf menhaden. Estuaries 13:14–19
Duffy JE, Hay ME (1991) Food and shelter as determinant of food choices by an herbivorous marine amphipod. Ecology 72:1286–1298
Duffy JE, Hay ME (1994) Herbivore resistance to seaweed chemical defence, the roles of mobility and predation risk. Ecology 75:1304–1319
EasyReef (2019) http://www.easyreefs.com/en/freeze-dried-microalgae.html. Visited on 18/08/2020
FAO (2018) El estado mundial de la pesca y la acuicultura 2018. Cumplir los objetivos de desarrollo sostenible. Roma
Fernandez-Gonzalez V, Toledo-Guedes K, Valero-Rodríguez JM, Agraso MM, Sanchez-Perez P (2018) Harvesting amphipods applying the integrated multitrophic aquaculture (IMTA) concept in off-shore areas. Aquaculture 489:62–69
Folch J, Lees M, Sloane-Stanley GH (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226:497–509
Gates AR (2006) “The physiological ecology of the specialist lagoon amphipod, Gammarus insensibilis”. University of Southampton. School of Ocean and Earth Sciences. PhD Thesis
González ML, Pérez-Schultheiss J, López DA (2011) Exotic amphipods in aquaculture systems, presence and potential use. Crustaceana 84:759–775
Guerra-García JM, Tierno de Figueroa JM, Navarro-Barranco C, Ros M, Sánchez-Moyano JE, Moreira J (2014) Dietary analysis of the marine Amphipoda (Crustacea, Peracarida) from the Iberian Peninsula. J Sea Res 85:508–517
Guerra-García JM, Hachero-Cruzado I, González-Romero P, Jiménez-Prada P, Cassell C, Ros M (2016) Towards integrated multi-trophic aquaculture, lessons from Caprellids (Crustacea, Amphipoda). PLoS One 11(4):e0154776. https://doi.org/10.1371/journal.pone.0154776
Harlıoğlu MM, Farhadi A (2018) Importance of Gammarus in aquaculture. Aquac Int 26(6):1327–1338
Jia R, Liu BL, Feng WR, Han C, Huang B, Lei JL (2016) Stress and immune responses in skin of turbot (Scophthalmus maximus) under different stocking densities. Fish Shellfish Immunol 55:131–139
Jiménez-Prada P, Hachero-Cruzado I, Guerra-García JM (2015) The importance of amphipods in diets of marine species with aquaculture interest of Andalusian coast. Zool Baetica 26:3–29
Jiménez-Prada P, Hachero-Cruzado I, Giráldez I, Fernández-Diaz C, Vilas C, Cañavate JP, Guerra-García JM (2018) Crustacean amphipods from marsh ponds, a nutritious feed resource with potential for application in Integrated Multi-Trophic Aquaculture. PeerJ 6:e4194. https://doi.org/10.7717/peerj.4194
Kneib RT, Newell SY, Hermeno ET (1997) Survival, growth and reproduction of the salt-marsh amphipod Uhlorchestia spartinophila reared on natural diets of senescent and dead Spartina alterniflora leaves. J Mar Biol 128:423–431
Kolanowski W, Stolyhwo A, Grabowski M (2007) Fatty acid composition of selected fresh water gammarids (Amphipoda, Crustacea), a potentially innovative source of omega-3 LC PUFA. J Am Oil Chem Soc 84:827–833
Liu X, Mai K, Liufu Z, Ai Q (2015) Dietary protein requirement of juvenile turbot (Scophthalmus maximus Linnaeus). J Ocean Univ China 14(2):325–328
Maehre HK, Hamre K, Elvevoll EO (2013) Nutrient evaluation of rotifers and zooplankton, feed for marine fish larvae. Aquac Nutr 19:301–311
Moren M, Suontama J, Hemre GI, Karlsen Ø, Olsen RE, Munheim H, Julshamn K (2006) Element concentrations in meals from krill and amphipods, possible alternative protein sources incomplete diets for farmed fish. Aquaculture 261:174–181
NRC (2012) In: Jobling M (ed) National Research Council: Nutrient requirements of fish and shrimp, Aquacult Int, vol 20, pp 601–602. https://doi.org/10.1007/s10499-011-9480-6
Olsen RE, Henderson RJ (1989) The rapid analysis on neutral and polar marine lipids using double development HPTLC and scanning densitometry. J Exp Mar Biol Ecol 129:189–197
Opstad I, Suontama J, Langmyhr E, Olsen RE (2006) Growth, survival, and development of Atlantic cod (Gadus morhua L.) weaned onto diets containing various sources of marine protein. J Mar Sci 63:320–325. https://doi.org/10.1016/j.icesjms.2005.11.014
Rayner TA, Jørgensen NOG, Blanda E, Wu CH, Huang CC, Mortensen J, Hwang JS, Hansen BW (2015) Biochemical composition of the promising live feed tropical calanoid copepod Pseudodiaptomus annandalei (Sewell 1919) cultured in Taiwanese outdoor aquaculture ponds. Aquaculture 441:25–34. https://doi.org/10.1016/j.aquaculture.2015.01.034
Sargent JR, McEvoy LA, Estevez A, Bell G, Bell M, Henderson J, Tocher D (1999) Lipid nutrition of marine fish during early development: current status and future directions. Aquaculture 1779:217–229
Shpigel M, Guttman L, Shauli L, Odintsov V, Ben-Ezra D, Harpaz S (2017) Ulva lactuca from an integrated multi-trophic aquaculture (IMTA) biofilter system as a protein supplement in gilthead seabream (Sparus aurata) diet. Aquaculture 481:112–118
Suontama J, Kiessling A, Melle W, Waagbø R, Olsen RE (2007) Protein from Northern krill (Thysanoessa inermis), Antarctic krill (Euphausia superba) and Arctic amphipod (Themisto libellula) can partially replace fish meals in diets to Atlantic salmon (Salmo salar) without affecting product quality. Aquac Nutr 13:50–58
Underwood AJ, Chapman MG, Richards SA (2002) GMAV-5 for 979 Windows. An analysis of variance programme. Centre for Research on Ecological 980 Impacts of Coastal Cities. Marine Ecology Laboratories, University of Sydney, Australia
Van der Meeren T, Olsen RE, Hamre K, Fyhn HJ (2008) Biochemical composition of copepods for evaluation of feed quality in production of juvenile marine fish. Aquaculture 274:375–397. https://doi.org/10.1016/j.aquaculture.2007.11.041
Acknowledgments
The authors acknowledge Gonzalo Angulo who helped with sampling and sorting amphipods, Rafael Castro for his knowledge and arranging of the experiment facilities, and Clara Gavira O’Neill for the English revision. We would like to give special thanks to Dr. Pilar Yamuza for her vital help during the experiment.
Funding
Financial support of this work was provided by the “Consejería de Innovación, Ciencia y Empresa, Junta de Andalucía (project P11-RNM-7041),” which includes a Ph.D. grant to Pablo Jiménez-Prada. I. Hachero-Cruzado was supported by an INIA postdoctoral contract.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Research involving human participants and/or animals
None.
Informed consent
We ensure that this article does not contain any studies with animals performed by any of the authors.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Jiménez-Prada, P., Hachero-Cruzado, I. & Guerra-García, J.M. Aquaculture waste as food for amphipods: the case of Gammarus insensibilis in marsh ponds from southern Spain. Aquacult Int 29, 139–153 (2021). https://doi.org/10.1007/s10499-020-00615-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10499-020-00615-z