Abstract
Nutrition and the lack of an established protocol for the larviculture of Octopus are some of the bottlenecks for the development of Octopus aquaculture. This study aims to start filling in these knowledge gaps by obtaining daily feeding rates (FR) of Octopus americanus paralarvae at different ages by testing different live prey types (Artemia nauplii, Acartia lilljeborgii copepods, and Callinectes sapidus zoeae) and densities (20, 40, 60, 80, 120, and 160 prey L−1). In addition, prey preference was assessed by exposing paralarvae to these prey types simultaneously. The dry weight (DW) of the prey was obtained and used to estimate the daily DW ingestion rate of paralarvae. Experiments were performed with 1- and 8–9-day-old paralarvae. The FRs recorded for different prey densities and the effect of different prey types on prey preference were analyzed through one-way ANOVA. The FRs recorded were quite different among the preys tested. The highest mean FRs for hatchlings was 26.2±6.9 zoeae paralarva−1 day−1 and for 8-day-old paralarvae was 63–69 Artemia nauplii paralarva−1 day−1. Therefore, the following prey densities are recommended for the larviculture of paralarvae up to 10 days of age: 80 copepods L−1, 160 Artemia nauplii L−1, and 80 zoeae L−1. Hatchlings showed a significant preference for zoeae, and Artemia nauplii and zoeae were significantly more preyed by 8-day-old paralarvae. Our results demonstrated that increasing prey density increases FR and predation by paralarvae, and zoeae were by far the preferred prey of hatchlings.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Availability of data and material
Available upon request.
Code availability
Not applicable
References
Ahlstrom EH, Thrailkill JR (1963) Plankton volume loss with time of preservation. Cal Coop Ocean Fish 9:57–73
Amor MD, Norman MD, Roura A, Leite TS, Gleadall IG, Reid A, Perales-Raya C, Lu C, Silvey CJ, Vidal EAG, Hochberg FG, Zheng X, Strugnell JM (2017) Morphological assessment of the Octopus vulgaris species complex evaluated in light of molecular-based phylogenetic inferences. Zool Scr 46:275–288. https://doi.org/10.1111/zsc.12207
Anufriieva E, Shadrin N (2014) The swimming behavior of Artemia (Anostraca): new experimental and observational data. Zoology 117:415–421. https://doi.org/10.1016/j.zool.2014.03.006
Avendaño O, Roura Á, Cedillo-Robles, CE, Gonzalez AF, Rodríguez-Canul R, Velázquez-Abunader I, Guerra A (2020) Octopus americanus: a cryptic species of the O. vulgaris species complex redescribed from the Caribbean. Aquat Ecol 54:909–925. https://doi.org/10.1007/s10452-020-09778-6
Boidron-Métairon, IF (1995) Larval nutrition. In McEdward L (ed) Ecology of Marine Invertebrate Larvae. CRC Press, Boca Raton, Florida pp 223–248
Buskey EJ (1994) Factors affecting feeding selectivity of visual predators on the copepod Acartia tonsa: locomotion, visibility and escape responses. Hydrobiologia 292(293):447–453. https://doi.org/10.1007/BF00229971
Buskey EJ, Lenz PH, Hartline DK (2002) Escape behavior of planktonic copepods in response to hydrodynamics disturbances: high speed video analysis. Mar Ecol Prog Ser 235:135–146. https://doi.org/10.3354/meps235135
Carrasco JF, Arronte JC, Rodríguez C (2006) Paralarval rearing of the common octopus, Octopus vulgaris (Cuvier). Aquac Res 37:1601–1605. https://doi.org/10.1111/j.1365-2109.2006.01594.x
Chen DS, Dykhuizen GV, Hodge J, Gilly WF (1996) Ontogeny of copepod predation in juvenile squid (Loligo opalescens). Biol Bull 190:69–81. https://doi.org/10.2307/1542676
Dan S, Iwasaki H, Takasugi A, Yamazaki H, Hamasaki K (2018) An upwelling system for culturing common octopus paralarvae and its combined effect with supplying natural zooplankton on paralarval survival and growth. Aquaculture 495:98–105. https://doi.org/10.1016/j.aquaculture.2018.05.036
Dan S, Iwasaki H, Takasugi A, Shibasaki S, Yamazaki H, Oka M, Hamasaki K (2019) Effects of co-supply ratios of swimming crab Portunus trituberculatus zoeae and Artemia on survival and growth of East Asian common octopus Octopus sinensis paralarvae under an upwelling culture system. Aquac Res 50:1–10. https://doi.org/10.1111/are.14013
Dan S, Takasugi A, Iwasaki H, Shibasaki S, Yamashita K, Hamasaki K (2020) Flocculation of Artemia induced by East Asian common octopus Octopus sinensis paralarvae under culture conditions. Aquacult Rep 17:100330. https://doi.org/10.1016/j.aqrep.2020.100330
De Wolf T, Lenzi S, Lenzi F (2011) Paralarval rearing of Octopus vulgaris (Cuvier) in Tuscany, Italy. Aquac Res 42:1406–1414. https://doi.org/10.1111/j.1365-2109.2010.02756.x
Durbin EG, Durbin AG (1978) Length and weight relationship of Acartia clausi from Narragansett Bay, R.I. Limnol Oceanogr 23(5):958–969. https://doi.org/10.4319/lo.1978.23.5.0958
Escánez A, Rubio J, Riera R, Almansa E (2017) Assessment of various anesthetic agents on Octopus vulgaris paralarvae. J World Aquacult Soc 49(6):1019–1025. https://doi.org/10.1111/jwas.12444
Fiorito G, Affuso A, Basil J, Cole A, Girolamo P, D’Angelo L, Dickel L, Gestal C, Grasso F, Kuba M, Mark F, Melillo D, Osorio D, Perkins K, Ponte G, Shashar N, Smith D, Smith J, Andrews PLR (2015) Guidelines for the care and welfare of cephalopods in research – a consensus based on an initiative by CephRes, FELASA and the Boyd Group. Lab Anim 49(S2):1–90. https://doi.org/10.1177/0023677215580006
Franco-Santos RM, Iglesias J, Domingues PM, Vidal EAG (2014) Early beak development in Argonauta nodosa and Octopus vulgaris (Cephalopoda: Incirrata) paralarvae suggests adaptation to different feeding mechanisms. Hydrobiologia 725:69–83. https://doi.org/10.1007/s10750-013-1721-4
Garrido G, Martín MV, Rodríguez C, Iglesias J, Navarro JC, Estévez A, Hontoria F, Becerro M, Otero JJ, Pérez J, Varó I, Reis DB, Riera R, Sykes AV, Almansa E (2016) Meta-analysis approach to the effects of live prey on the growth of Octopus vulgaris paralarvae under culture conditions. Rev Aquac 0: 1-12.https://doi.org/10.1111/raq.12142
Gerritsen J, Strickler JR (1977) Encounter probabilities and community structure in zooplankton: a mathematical model. J Fish Res Board Can 34:73–82
Globefish (2019) Octopus market report. http://www.globefish.org/. Acessed January 2019.
Hernández-García V, Martin AY, Castro JJ (2000) Evidence of external digestion of crustaceans in Octopus vulgaris paralarvae. J Mar Biol Assoc UK 80:559–560. https://doi.org/10.1017/S0025315400002320
Iglesias J, Fuentes L (2014) Octopus vulgaris: paralarval culture. In: Iglesias J, Fuentes L, Villanueva R (eds) Cephalopod Culture. Springer, New York
Iglesias J, Otero JJ, Moxica C, Fuentes L, Sánchez FJ (2004) The completed life cycle of the octopus (Octopus vulgaris, Cuvier) under culture conditions: paralarval rearing using Artemia and zoeae, and first data on juvenile growth up to 8 months of age. Aquac Int 12:481–487. https://doi.org/10.1023/B:AQUI.0000042142.88449.bc
Iglesias J, Fuentes L, Sánchez J, Otero JJ, Moxica C, Lago MJ (2006) First feeding of Octopus vulgaris Cuvier, 1797 paralarvae using Artemia: effect of prey size, prey density and feeding frequency. Aquaculture 261:817–822. https://doi.org/10.1016/j.aquaculture.2006.08.002
Iglesias J, Sánchez FJ, Bersano JGF, Carrasco JF, Dhont J, Fuentes L, Linares F, Muñoz JL, Okumura S, Roo J, van der Meeren T, Vidal EAG, Villanueva R (2007) Rearing of Octopus vulgaris paralarvae: present status, bottlenecks and trends. Aquaculture 266:1–15. https://doi.org/10.1016/j.aquaculture.2007.02.019
Iglesias J, Fuentes L, Villanueva R (2014) Cephalopod culture. Springer, New York 494p
Jiang H, Kiørboe T (2011) Propulsion efficiency and imposed flow fields of a copepod jump. J Exp Biol 214(3):476–486. https://doi.org/10.1242/jeb.049288
Kilkenny C, Browne W, Cuthill IC, Emerson M, Altman DG (2010) Animal research: reporting in vivo experiments: the ARRIVE guidelines. Br J Pharmacol 160(7):1577–1579. https://doi.org/10.1111/j.1476-5381.2010.00872.x
Kiørboe T, MacKenzie B (1995) Turbulence-enhanced prey encounter rates in larval fish: effects of spatial scale, larval behaviour and size. J Plankton Res 17(12):2319–2331. https://doi.org/10.1093/plankt/17.12.2319
Márquez L, Quintana D, Almansa E, Navas JI (2007) Effects of visual conditions and prey density on feeding kinetics of paralarvae of Octopus vulgaris from a laboratory spawning. J Molluscan Stud 73:117–121. https://doi.org/10.1093/mollus/eym003
Mauchline J (1998) The biology of calanoid copepods. Advances in Marine Biology. Academic Press, San Diego
Muxagata E, Williams JA (2011) Larval body size-mass relationships of barnacles common to the English Channel coast of the U.K. J Mar Biolog Assoc UK 91(1):181–189. https://doi.org/10.1017/S0025315410001402
Nande M, Iglesias J, Domingues P, Pérez M (2017a) Effect of temperature on energetic demands during the last stages of embryonic development and early life of Octopus vulgaris (Cuvier, 1797) paralarvae. Aquac Res 48:1951–1961. https://doi.org/10.1111/are.13032
Nande MPP, Roura Á, Andrews PLR, Pérez M (2017b) Prey capture, ingestion, and digestion dynamics of Octopus vulgaris paralarvae fed live zooplankton. Front Physiol 573(8):1–16. https://doi.org/10.3389/fphys.2017.00573
Navarro JC, Villanueva R (2000) Lipid and fatty acid composition of early stages of cephalopods: an approach to their lipid requirements. Aquaculture 183:161–177. https://doi.org/10.1016/S0044-8486(99)00290-2
Navarro JC, Villanueva R (2003) The fatty acid composition of Octopus vulgaris paralarvae reared with live and inert food: deviation from their natural fatty acid profile. Aquaculture 2019:613–631. https://doi.org/10.1016/S0044-8486(02)00311-3
Navarro JC, Henderson RJ, McEvoy LA, Bell MV, Amat F (1999) Lipid conversions during enrichment of Artemia. Aquaculture 174:155–166. https://doi.org/10.1016/S0044-8486(99)00004-6
Norman MD, Hochberg FG, Finn JK (2014) Octopods and vampire squids. In: Jereb P, CFE R, NormanMD FJK (eds) FAO Species Catalogue for Fishery Purposes, No 4, Vol. 3. Cephalopods of the world. An annotated and illustrated catalogue of cephalopods species known to date. FAO, Rome, pp 42–47
Olmos-Pérez L, Roura Á, Pierce GJ, Boyer S, González ÁF (2017) Diet composition and variability of wild Octopus vulgaris and Alloteuthis media (Cephalopoda) paralarvae: a metagenomic approach. Front Physiol 8(321):1–21. https://doi.org/10.3389/fphys.2017.00321
Reis DB, Acosta NG, Almansa E, Navarro JC, Tocher DR, Andrade JP, Sykes AV, Rodríguez C (2017) Comparative study on fatty acid metabolism of early stages of two crustacean species: Artemia sp. metanauplii and Grapsus adscensionis zoeae, as live prey for marine animals. Comp Biochem Physiol B Biochem Mol Biol 204:53–60. https://doi.org/10.1016/j.cbpb.2016.11.002
Rothschild BJ, Osborn TR (1988) Small-scale turbulence and plankton contact rates. J Plankton Res 10(3):465–474. https://doi.org/10.1093/plankt/10.3.465
Roura Á, González ÁF, Redd K, Guerra Á (2012) Molecular prey identification in wild Octopus vulgaris paralarvae. Mar Biol 159:1335–1345. https://doi.org/10.1007/s00227-012-1914-9
Roura Á, Álvarez-Salgado XA, González ÁF, Gregori M, Rosón G, Otero J, Guerra Á (2016) Life strategies of cephalopod paralarvae in an upwelling system (NW Iberian Peninsula): insights from zooplankton community and spatio-temporal analyses. Fish Oceanogr 25(3):241–258. https://doi.org/10.1111/fog.12151
Sargent JR, Mcevoy LA, Bell JG (1997) Requirements, presentation and sources of polyunsaturated fatty acids in marine larval feeds. Aquaculture 155:117–127. https://doi.org/10.1016/S0044-8486(97)00122-1
Smith JA, Andrews PL, Hawkins P, Louhimies S, Ponte G, Dickel L (2013) Cephalopod research and EU Directive 2010/63/EU: Requirements, impacts and ethical review. J Exp Mar Biol Ecol 447:31–45. https://doi.org/10.1016/j.jembe.2013.02.010
Stappen GV (1996) Introduction, biology and ecology of Artemia. In: Lavens P, Sorgeloos P (eds) Manual on the production and use of live food for aquaculture. FAO, Rome
Steedman HF (1976) Monographs on oceanography methodology No. 4 – Zooplankton fixation and preservation. Unesco Press, Paris 350p
Støttrup JG, Norsker NH (1997) Production and use of copepods in marine fish larviculture. Aquaculture 155:231–247. https://doi.org/10.1016/S0044-8486(97)00120-8
Trager G, Achituv Y, Genin A (1994) Effects of prey escape ability, flow speed, and predator feeding mode on zooplankton capture by barnacles. Mar Biol 120:251–259. https://doi.org/10.1007/BF00349685
Vidal EAG, Boletzky SV (2014) Loligo vulgaris and Doryteuthis opalescens. In: Iglesias J, Fuentes L, Villanueva R (eds) Cephalopod Culture. Springer, New York pp 271–313
Vidal EAG, Salvador B (2019) The tentacular strike behavior in squid: functional interdependency of morphology and predatory behaviors during ontogeny. Front Physiol 10:1558. https://doi.org/10.3389/fphys.2019.01558
Vidal EAG, DiMarco FP, Wormuth JH, Lee PG (2002a) Optimizing rearing conditions of hatchling squid. Mar Biol 140:117–127. https://doi.org/10.1007/s002270100683
Vidal EAG, DiMarco FP, Wormuth JH, Lee PG (2002b) Influence of temperature and food availability on survival, growth and yolk utilization in hatchling squid. Bull Mar Sci 71:915–931
Vidal EAG, DiMarco FP, Lee P (2006) Effects of starvation and recovery on the survival, growth and RNA/DNA ratio in loliginid squid paralarvae. Aquaculture 260:94–105. https://doi.org/10.1016/j.aquaculture.2006.05.056
Vidal EAG, Villanueva R, Andrade JP, Gleadall IG, Iglesias J, Koueta N, Rosas C, Segawa S, Grasse B, Franco-Santos RM, Albertin CB, Caamal-Monsreal C, Chinal ME, Edsinger-Gonzalez E, Gallardo P, Pabic CL, Pascual C, Roumbedakis K, Wood J (2014) Cephalopod culture: current status of main biological models and research priorities. In: Vidal EAG (ed) Advances in Marine Biology, vol 67. Oxford, United Kingdom, pp 1–98
Villanueva R (1994) Decapod crab zoeae as food for rearing cephalopod paralarvae. Aquaculture 128:143–152. https://doi.org/10.1016/0044-8486(94)90109-0
Villanueva R (1995) Experimental rearing and growth of planktonic Octopus vulgaris from hatching to settlement. Can J Fish Aquat Sci 52:2639–2650. https://doi.org/10.1139/f95-853
Villanueva R, Norman M (2008) Biology of the planktonic stages of benthic octopuses. Oceanogr Mar Biol 46:105–202. https://doi.org/10.1201/9781420065756.ch4
Villanueva R, Nozais C, Boletzky S (1996, 208) Swimming behaviour and food searching in planktonic Octopus vulgaris Cuvier from hatching to settlement. J Exp Mar Biol Ecol:169–184. https://doi.org/10.1016/S0022-0981(96)02670-6
Watanabe T, Katajima C, Fujita C (1983) Nutritional value of live organisms used in Japan for mass propagation of fish: a review. Aquaculture 34:115–143
Williams TA (1994) A model of rowing propulsion and the ontogeny of locomotion in Artemia larvae. Biol Bull 187(2):164–173. https://doi.org/10.2307/1542239
Young RE, Harman RF (1988) “Larva,” “Paralarva” and “Subadult” in Cephalopod Terminology. Malacologia 29(l):201–207
Zar JH (1999) Biostatistical Analysis. Prentice Hall, New Jersey
Acknowledgements
We thank the staffs of the Cephalopod Early-life Stages Laboratory and the Zooplankton Laboratory at Center of Marine Studies (UFPR), in special the Lab. technicians Paulo Soares and Vanessa Coquemala for their support during the experiments. We also thank Katina Roumbedakis for her valuable comments and suggestions. The authors are grateful to the Brazilian Ministry of Environment (MMA) and the Chico Mendes Institute for Conservation and Biodiversity for authorizing the capture and maintenance of octopuses for the experiments and the Coordination for Higher Education Improvement (CAPES) and the Araucária Foundation (Fundação de Apoio ao Desenvolvimento Científico e Tecnológico do Paraná) for the scholarships provided for Danielle Ortiz and Ivan Gavioli, respectively. We thank the Brazilian National Research Council (CNPq) for grants to EAGV (# 426797/2018-5 and 312332/2018-1).
Funding
The Coordination for Higher Education Improvement (CAPES), the Araucária Foundation (Fundação de Apoio ao Desenvolvimento Científico e Tecnológico do Paraná), and the Brazilian National Research Council (CNPq) (grants to EAGV, # 426797/2018-5 and 312332/2018-1).
Author information
Authors and Affiliations
Contributions
Danielle Ortiz de Ortiz: conceptualization, methodology, validation, formal analysis, investigation, data curation, writing original draft, writing review and editing, and visualization. Ivan Luiz Gavioli: validation, formal analysis, investigation, data curation, and writing original draft. J. Guilherme Bersano Filho: conceptualization, methodology, and resources. Erica A G Vidal: conceptualization, methodology, validation, data curation, resources, writing review and editing, supervision, project administration, and funding acquisition.
Corresponding author
Ethics declarations
Ethics approval
This study was conducted in accordance with the guidelines for the care and welfare of cephalopods (Fiorito et al. 2015) and the principles of the European Directive (2010/63/EU), which regulate cephalopod research in the European Union (E 121 U: Smith et al. 2013) and the recommendations of the ARRIVE Guideline (Kilkenny et al. 2010) for reporting in vivo experiments with research animals. The authors hold an authorization (number 61506-1) from the Brazilian Ministry of the Environment (MMA) to collect, transport, and maintain Octopus spp. for scientific purposes.
Consent to participate
Not applicable.
Consent for publication
The authors declare that they agree with the publication of the data reported in this paper.
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
ESM 1
(DOCX 19 kb)
Rights and permissions
About this article
Cite this article
de Ortiz, D.O., Gavioli, I.L., Bersano, J.G.F. et al. Feeding rates and prey preference in Octopus americanus paralarvae fed with different prey densities and types, Artemia, copepods, and zoeae. Aquacult Int 29, 779–800 (2021). https://doi.org/10.1007/s10499-021-00657-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10499-021-00657-x