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The Welfare of Invertebrate Animals pp 209–228Cite as

Cephalopod Welfare, Biological and Regulatory Aspects: An EU Experience

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Part of the book series: Animal Welfare ((AWNS,volume 18))

Abstract

Recent increased interest in the welfare of cephalopods may be mainly due to their inclusion in Directive 2010/63/EU, which regulates—in Member States of the European Union—the use of animals for scientific research and educational purposes. Here we aim to challenge this view by providing information and considerations that have a broader impact than the use of these animals in an experimental context. We aim to provide a discussion around arguments linked to cephalopods’ welfare.

We (1) discuss historical contributions to the knowledge of welfare of this class of molluscs, (2) review the most significant elements required to assess and manage animals’ well-being in a research context, (3) review issues related to fisheries and aquaculture and their implications for cephalopod welfare, (4) suggest that the identification of a list of “needs” for these animals is required and review how deviations in their management may affect their welfare, and finally comment (5) that standardization is required to assure the quality of data and also (6) on some ethical and public perceptions of cephalopods as laboratory animals vs their use as food for human consumption.

We believe this chapter will promote discussion around arguments that drive the consideration of welfare issues in all aspects of cephalopod science, from basic to applied, that extend well beyond the boundaries of the European Union.

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Notes

  1. 1.

    http://eur-lex.europa.eu/legal-content/EN/TXT/HTML/?uri=CELEX:12012E/TXT&from=EN

  2. 2.

    Freedom from hunger and thirst; Freedom from discomfort; Freedom from pain , injury, or disease; Freedom to express normal behavior; and Freedom from fear and distress (see also http://kb.rspca.org.au/Five-freedoms-for-animals_318.html).

  3. 3.

    Directive 2010/63/EU specifically refers to animals bred for experimental purposes. It also dedicates an article (Article 9) to “animals taken from the wild,” providing that their use shall be limited in experimental procedures, and only allowed in cases where scientific justification is provided, and/or considering the limitations of breeding them in purpose (see Article 10). In addition, the Commission recommendation is that the capture of animals from the wild shall be carried out only by competent persons using methods which do not cause the animal’s avoidable pain, suffering, distress, or lasting harm.

  4. 4.

    See http://ec.europa.eu/environment/chemicals/lab_animals/transposition_en.htm

  5. 5.

    EC 2009, Moderator P. Nowlan; see ec.europa.eu/environment/chemicals/lab_animals/pdf/report_ewg.pdf

  6. 6.

    See also discussion in Andrews et al. (2013).

References

  • Adamo S (2017) The “precautionary principle” – a work in progress. Anim Sentience 2:4

    Google Scholar 

  • Albertin CB, Simakov O, Mitros T, Wang ZY, Pungor JR, Edsinger-Gonzales E, Brenner S, Ragsdale CW, Rokhsar DS (2015) The octopus genome and the evolution of cephalopod neural and morphological novelties. Nature 524:220–224

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Allcock L (2011) Red list of globally threatened species: cephalopods. Marine Species News, 1–2 Apr

    Google Scholar 

  • Alupay JS, Hadjisolomou SP, Crook RJ (2014) Arm injury produces long-term behavioral and neural hypersensitivity in octopus. Neurosci Lett 558:137–142

    Article  CAS  PubMed  Google Scholar 

  • Amodio P, Andrews PLR, Salemme M, Ponte G, Fiorito G (2014) The use of artificial crabs for testing predatory behavior and health in the octopus. ALTEX:1–12. https://doi.org/10.14573/altex.1401282

  • Anderson RC, Wood JB, Byrne RA (2002) Octopus senescence: the beginning of the end. J Appl Anim Welf Sci 5:275–283

    Article  CAS  PubMed  Google Scholar 

  • André M, Solé M, Lenoir M, Durfort M, Quero C, Mas A, Lombarte A, van der Schaar M, López-Bejar M, Morell M (2011) Low-frequency sounds induce acoustic trauma in cephalopods. Front Ecol Environ 9:489–493

    Article  Google Scholar 

  • Andrews PL, Darmaillacq A-S, Dennison N, Gleadall IG, Hawkins P, Messenger JB, Osorio D, Smith VJ, Smith JA (2013) The identification and management of pain, suffering and distress in cephalopods, including anaesthesia, analgesia and humane killing. J Exp Mar Biol Ecol 447:46–64

    Article  Google Scholar 

  • Antunes L (2011) Euthanasia. In: Howard B, Nevalainen T, Perretta G (eds) The COST manual of laboratory animal care and use: refinement, reduction, and research. CRC, Boca Raton, FL, pp 355–368

    Google Scholar 

  • Aske KC, Waugh CA (2017) Expanding the 3R principles: more rigour and transparency in research using animals. EMBO Rep 18:1490–1492. https://doi.org/10.15252/embr.201744428

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bentham J (1907) An introduction to the principles of morals and legislation. Clarendon Press, Oxford

    Google Scholar 

  • Bert B, Chmielewska J, Hensel A, Grune B, Schönfelder G (2016) The animal experimentation quandary: stuck between legislation and scientific freedom. EMBO Rep 17:790–792

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Birch J (2017) Animal sentience and the precautionary principle. Anim Sentience 2:1

    Google Scholar 

  • Boal J (2011) Behavioral research methods for octopuses and cuttlefishes. Vie Milieu 61:203–210

    Google Scholar 

  • Boletzky SV, Hanlon RT (1983) A review of the laboratory maintenance, rearing and culture of cephalopod molluscs. Mem Natl Mus Victoria 44:147–187

    Article  Google Scholar 

  • Borrelli L (2007) Testing the contribution of relative brain size and learning capabilities on the evolution of Octopus vulgaris and other cephalopods. Ph.D. thesis, Stazione Zoologica Anton Dohrn, Italy & Open University, UK

    Google Scholar 

  • Borrelli L, Fiorito G (2008) Behavioral analysis of learning and memory in cephalopods. In: Byrne JJ (ed) Learning and memory: a comprehensive reference. Academic, Oxford, pp 605–627

    Chapter  Google Scholar 

  • Borrelli L, Gherardi F, Fiorito G (2006) A catalogue of body patterning in Cephalopoda. Stazione Zoologica A. Dohrn; Firenze University Press, Napoli

    Google Scholar 

  • Bovenkerk B, Braithwaite V (2016) Beneath the surface: killing of fish as a moral problem. In: Meijboom F, Stassen E (eds) The end of animal life: a start for ethical debate: ethical and societal considerations on killing animals. Wageningen Academic Publishers, Wageningen, pp 433–441

    Google Scholar 

  • Boyle PR (1991) The UFAW handbook on the care and management of cephalopods in the laboratory. Universities Federation for Animal Welfare, Potters Bar

    Google Scholar 

  • Brambell F (1965) Report on the technical committee to enquire into the welfare of livestock kept under intensive conditions. Her Majesty’s Stationary Office, London

    Google Scholar 

  • Burnard C, Ralph C, Hynd P, Edwards JH, Tilbrook A (2017) Hair cortisol and its potential value as a physiological measure of stress response in human and non-human animals. Anim Prod Sci 57:401–414

    Article  CAS  Google Scholar 

  • Capaz JC, Tunnah L, MacCormack TJ, Lamarre SG, Sykes AV, Driedzic WR (2017) Hypoxic induced decrease in oxygen consumption in cuttlefish (Sepia officinalis) is associated with minor increases in mantle octopine but no changes in markers of protein turnover. Front Physiol 8:344

    Article  PubMed  PubMed Central  Google Scholar 

  • Carbone L, Austin J (2016) Pain and laboratory animals: publication practices for better data reproducibility and better animal welfare. PLoS One 11:e0155001. https://doi.org/10.1371/journal.pone.0155001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cardoso P, Borges PA, Triantis KA, Ferrández MA, Martín JL (2012) The underrepresentation and misrepresentation of invertebrates in the IUCN Red List. Biol Conserv 149:147–148

    Article  Google Scholar 

  • Carere C, Grignani G, Bonanni R, Gala MD, Carlini A, Angeletti D, Cimmaruta R, Nascetti G, Mather JA (2015) Consistent individual differences in the behavioural responsiveness of adult male cuttlefish (Sepia officinalis). Appl Anim Behav Sci 167:89–95. https://doi.org/10.1016/j.applanim.2015.03.005

    Article  Google Scholar 

  • Carruthers P (2011) Animal mentality: its character, extent, and moral significance. In: Frey RG, Beauchamp TL (eds) The Oxford handbook of animal ethics. Oxford University Press, Oxford, pp 373–406

    Chapter  Google Scholar 

  • Castellanos-Martínez S, Gestal C (2013) Pathogens and immune response of cephalopods. J Exp Mar Biol Ecol 447:14–22

    Article  CAS  Google Scholar 

  • Castellanos-Martínez S, Arteta D, Catarino S, Gestal C (2014a) De novo transcriptome sequencing of the Octopus vulgaris hemocytes using illumina RNA-Seq technology: response to the infection by the gastrointestinal parasite Aggregata octopiana. PLoS One 9:e107873

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Castellanos-Martínez S, Diz AP, Álvarez-Chaver P, Gestal C (2014b) Proteomic characterization of the hemolymph of Octopus vulgaris infected by the protozoan parasite Aggregata octopiana. J Proteome 105:151–163

    Article  CAS  Google Scholar 

  • Crabbe JC (2016) Reproducibility of experiments with laboratory animals: what should we do now? Alcohol Clin Exp Res 40:2305–2308. https://doi.org/10.1111/acer.13228

    Article  PubMed  Google Scholar 

  • Crook RJ, Walters ET (2011) Nociceptive behavior and physiology of molluscs: animal welfare implications. ILAR J 52:185–195

    Article  CAS  PubMed  Google Scholar 

  • Crook RJ, Lewis T, Hanlon RT, Walters ET (2011) Peripheral injury induces long-term sensitization of defensive responses to visual and tactile stimuli in the squid Loligo pealeii, Lesueur 1821. J Exp Biol 214:3173–3185

    Article  PubMed  PubMed Central  Google Scholar 

  • Crook RJ, Hanlon RT, Walters ET (2013) Squid have nociceptors that display widespread long-term sensitization and spontaneous activity after bodily injury. J Neurosci 33:10021–10026

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Darmaillacq AS, Dickel L, Chichery MP, Agin V, Chichery R (2004) Rapid taste aversion learning in adult cuttlefish, Sepia officinalis. Anim Behav 68:1291–1298

    Article  Google Scholar 

  • Darmaillacq A-S, Mezrai N, O’Brien CE, Dickel L (2017) Visual ecology and the development of visually guided behavior in the cuttlefish. Front Physiol 8:402

    Article  PubMed  PubMed Central  Google Scholar 

  • Dawkins MS (2017) Animal welfare with and without consciousness. J Zool 301:1–10. https://doi.org/10.1111/jzo.12434

    Article  Google Scholar 

  • Di Cristina G, Andrews P, Ponte G, Galligioni V, Fiorito G (2015) The impact of Directive 2010/63/EU on cephalopod research. Invertebr Neurosci 15:8. https://doi.org/10.1007/s10158-015-0183-y

    Article  CAS  Google Scholar 

  • Edelman DB (2011) How octopuses see the world and other roads less traveled: necessity versus sufficiency and evolutionary convergence in the study of animal consciousness. J Shellfish Res 30:1001

    Google Scholar 

  • Edelman DB, Seth AK (2009) Animal consciousness: a synthetic approach. Trends Neurosci 32:476–484

    Article  CAS  PubMed  Google Scholar 

  • Estefanell J, Socorro J, Afonso J, Roo J, Fernández-Palacios H, Izquierdo M (2011) Evaluation of two anaesthetic agents and the passive integrated transponder tagging system in Octopus vulgaris (Cuvier 1797). Aquac Res 42:399–406

    Article  Google Scholar 

  • Estefanell J, Roo J, Fernández-Palacios H, Izquierdo M, Socorro J, Guirao R (2012a) Comparison between individual and group rearing systems in Octopus vulgaris (Cuvier, 1797). J World Aquacult Soc 43:63–72

    Article  Google Scholar 

  • Estefanell J, Roo J, Guirao R, Izquierdo M, Socorro J (2012b) Benthic cages versus floating cages in Octopus vulgaris: biological performance and biochemical composition feeding on Boops boops discarded from fish farms. Aquac Eng 49:46–52

    Article  Google Scholar 

  • Estefanell J, Socorro J, Izquierdo M, Roo J (2015) Effect of two fresh diets and sexual maturation on the proximate and fatty acid profile of several tissues in Octopus vulgaris: specific retention of arachidonic acid in the gonads. Aquac Nutr 21:274–285

    Article  CAS  Google Scholar 

  • Finke E, Pörtner H-O, Lee P, Webber D (1996) Squid (Lolliguncula brevis) life in shallow waters: oxygen limitation of metabolism and swimming performance. J Exp Biol 199:911–921

    CAS  PubMed  Google Scholar 

  • Fiorito G, Affuso A, Anderson DB, Basil J, Bonnaud L, Botta G, Cole A, D’Angelo L, de Girolamo P, Dennison N, Dickel L, Di Cosmo A, Di Cristo C, Gestal C, Fonseca R, Grasso F, Kristiansen T, Kuba M, Maffucci F, Manciocco A, Mark FK, Melillo D, Osorio D, Palumbo A, Perkins K, Ponte G, Raspa M, Shashar N, Smith J, Smith D, Sykes A, Villanueva R, Tublitz N, Zullo L, Andrews PLR (2014) Cephalopods in neuroscience: regulations, research and the 3Rs. Invertebr Neurosci 14:13–36

    Article  CAS  Google Scholar 

  • Fiorito G, Affuso A, Basil J, Cole A, de Girolamo P, D’Angelo L, Dickel L, Gestal C, Grasso F, Kuba M (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 49:1–90

    Article  PubMed  Google Scholar 

  • Gestal C, Castellanos-Martínez S (2015) Understanding the cephalopod immune system based on functional and molecular evidence. Fish Shellfish Immunol 46:120–130

    Article  CAS  PubMed  Google Scholar 

  • Gleadall IG (2013) The effects of prospective anaesthetic substances on cephalopods: summary of original data and a brief review of studies over the last two decades. J Exp Mar Biol Ecol 447:23–30

    Article  CAS  Google Scholar 

  • Gonçalves RA, Aragão C, Frias PA, Sykes AV (2012) The use of different anaesthetics as welfare promoters during short-term human manipulation of European cuttlefish (Sepia officinalis) juveniles. Aquaculture 370:130–135

    Article  CAS  Google Scholar 

  • Grimaldi AM, Agnisola C, Fiorito G (2007) Using ultrasound to estimate brain size in the cephalopod Octopus vulgaris Cuvier in vivo. Brain Res 1183:66–73

    Article  CAS  PubMed  Google Scholar 

  • Grimaldi AM, Belcari P, Pagano E, Cacialli F, Locatello L (2013) Immune responses of Octopus vulgaris (Mollusca: Cephalopoda) exposed to titanium dioxide nanoparticles. J Exp Mar Biol Ecol 447:123–127

    Article  CAS  Google Scholar 

  • Grimpe G (1928) Pflege, Behandlung und Zucht der Cephalopoden fur zoologische und physiologische Zwecke. In: Äberhalden E (ed) Handbuch der biologischen Arbeitsmethoden. Verlag Urban & Schwarzenberg, Berlin, pp 331–402

    Google Scholar 

  • Grimsbø E, Nortvedt R, Hjertaker BT, Hammer E, Roth B (2016) Optimal AC frequency range for electro-stunning of Atlantic salmon (Salmo salar). Aquaculture 451:283–288

    Article  Google Scholar 

  • Hanlon RT (1988) Behavioral and body patterning characters useful in taxonomy and field identification of cephalopods. Malacologia 29:247–264

    Google Scholar 

  • Hanlon RT, Messenger JB (1996) Cephalopod behaviour. Cambridge University Press, Cambridge

    Google Scholar 

  • Hanlon RT, Maxwell MR, Shashar N, Loew ER, Boyle K-L (1999) An ethogram of body patterning behavior in the biomedically and commercially valuable squid Loligo pealei off Cape Cod, Massachusetts. Biol Bull 197:49–62

    Article  CAS  PubMed  Google Scholar 

  • Hochner B (2012) An embodied view of octopus neurobiology. Curr Biol 22:R887–RR92

    Article  CAS  PubMed  Google Scholar 

  • Hochner B, Shomrat T, Fiorito G (2006) The octopus: a model for a comparative analysis of the evolution of learning and memory mechanisms. Biol Bull 210:308–317

    Article  PubMed  Google Scholar 

  • Hofmeister JKK, Voss KM (2017) Activity space and movement patterns of Octopus bimaculatus (Verrill, 1883) around Santa Catalina Island, California. J Exp Mar Biol Ecol 486:344–351. https://doi.org/10.1016/j.jembe.2016.10.024

    Article  Google Scholar 

  • Hough AR, Case J, Boal JG (2016) Learned control of body patterning in cuttlefish Sepia officinalis (Cephalopoda). J Molluscan Stud 82:427–431. https://doi.org/10.1093/mollus/eyw006

    Article  Google Scholar 

  • Huber N, Fusani L, Ferretti A, Mahr K, Canoine V (2017) Measuring short-term stress in birds: comparing different endpoints of the endocrine-immune interface. Physiol Behav 182:46–53

    Article  CAS  PubMed  Google Scholar 

  • Huffard CL (2007) Ethogram of Abdopus aculeatus (d’Orbigny, 1834) (Cephalopoda: Octopodidae): can behavioural characters inform Octopodidae taxomony and systematics? J Molluscan Stud 73:185–193

    Article  Google Scholar 

  • Huffard CL (2013) Cephalopod neurobiology: an introduction for biologists working in other model systems. Invertebr Neurosci 13:11–18

    Article  Google Scholar 

  • Hüske C, Sander SE, Hamann M, Kershaw O, Richter F, Richter A (2016) Towards optimized anesthesia protocols for stereotactic surgery in rats: analgesic, stress and general health effects of injectable anesthetics. A comparison of a recommended complete reversal anesthesia with traditional chloral hydrate monoanesthesia. Brain Res 1642:364–375

    Article  PubMed  CAS  Google Scholar 

  • ICES (2014) Report of the Working Group on Cephalopod Fisheries and Life History (WGCEPH). 16–19 June 2014, Lisbon, Portugal. Copenhagen, Denmark: ICES International Council for the Exploration of the Sea

    Google Scholar 

  • Iglesias J, Fuentes L, Villanueva R (2014) Cephalopod culture. Springer Science & Business Media, Heidelberg

    Book  Google Scholar 

  • Jantzen TM, Havenhand JN (2003) Reproductive behavior in the squid Sepioteuthis australis from South Australia: ethogram of reproductive body patterns. Biol Bull 204:290–304

    Article  PubMed  Google Scholar 

  • Jereb P, Roper C (2005) Chambered Nautiluses and Sepioids (Nautilidae, Sepiidae, Sepiolidae, Sepiadariidae, Idiosepiidae and Spirulidae). FAO Species Catalogue for Fishery Purposes, Rome. FAO, Rome

    Google Scholar 

  • Jereb P, Roper C (2010) Cephalopods of the world. An annotated and illustrated catalogue of species known to date. Volume 2. Myopsid and Oegopsid Squids. FAO Species Catalogue for Fishery Purposes. FAO, Rome

    Google Scholar 

  • Jereb P, Roper C, Norman M, Finn J (2016) Cephalopods of the world. An annotated and illustrated catalogue of species known to date. Volume 3. Octopods and Vampire Squids. FAO Species Catalogue for Fishery Purposes

    Google Scholar 

  • Kilkenny C, Browne WJ, Cuthill IC, Emerson M, Altman DG (2010) Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLoS Biol 8:e1000412. https://doi.org/10.1371/journal.pbio.1000412

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kröger B, Vinther J, Fuchs D (2011) Cephalopod origin and evolution: a congruent picture emerging from fossils, development and molecules. BioEssays 33:602–613

    Article  PubMed  CAS  Google Scholar 

  • Lahvis G (2017) Animal welfare: make animal models more meaningful. Nature 543:623

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Le Pabic C, Mottier A, Costil K, Koueta N, Lebel J-M, Serpentini A (2013) Haemocyte primary-culture from three mollusc species and its application in ecotoxicology. Cytotechnology 65:688

    Google Scholar 

  • Lin C-Y, Tsai Y-C, Chiao C-C (2017) Quantitative analysis of dynamic body patterning reveals the grammar of visual signals during the reproductive behavior of the oval squid Sepioteuthis lessoniana. Front Ecol Evol 5:30

    Article  Google Scholar 

  • Liscovitch-Brauer N, Alon S, Porath HT, Elstein B, Unger R, Ziv T, Admon A, Levanon EY, Rosenthal JJ, Eisenberg E (2017) Trade-off between transcriptome plasticity and genome evolution in cephalopods. Cell 169:191–202.e11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Locatello L, Fiorito G, Finos L, Rasotto MB (2013) Behavioural and immunological responses to an immune challenge in Octopus vulgaris. Physiol Behav 122:93–99. https://doi.org/10.1016/j.physbeh.2013.08.029

    Article  CAS  PubMed  Google Scholar 

  • MacCormack TJ, Callaghan NI, Sykes AV, Driedzic WR (2016) Taurine depresses cardiac contractility and enhances systemic heart glucose utilization in the cuttlefish, Sepia officinalis. J Comp Physiol B 186:215–227. https://doi.org/10.1007/s00360-015-0946-0

    Article  CAS  PubMed  Google Scholar 

  • Margheri L, Ponte G, Mazzolai B, Laschi C, Fiorito G (2011) Non-invasive study of Octopus vulgaris arm morphology using ultrasound. J Exp Biol 214:3727–3731

    Article  PubMed  Google Scholar 

  • Marini G, De Sio F, Ponte G, Fiorito G (2017) Behavioral analysis of learning and memory in cephalopods. In: Byrne JH (ed) Learning and memory: a comprehensive reference, 2nd edn. Academic, Amsterdam, pp 441–462

    Chapter  Google Scholar 

  • Mather JA (1991) Navigation by spatial memory and use of visual landmarks in octopuses. J Comp Physiol A 168:491–497

    Article  Google Scholar 

  • Mather JA (2001) Animal suffering: an invertebrate perspective. J Appl Anim Welf Sci 4:151–156. https://doi.org/10.1207/S15327604JAWS0402_9

    Article  Google Scholar 

  • Mather JA (2011) Philosophical background of attitudes toward and treatment of invertebrates. ILAR J 52:205–212

    Article  CAS  PubMed  Google Scholar 

  • Mather J (2017) Support for the precautionary principle. Anim Sentience 2:10

    Google Scholar 

  • Mather JA, Alupay JS (2016) An ethogram for benthic octopods (Cephalopoda: Octopodidae). J Comp Psychol 130:109

    Article  PubMed  Google Scholar 

  • Mather JA, Anderson RC (2007) Ethics and invertebrates: a cephalopod perspective. Dis Aquat Org 75:119–129

    Article  Google Scholar 

  • Mather JA, Kuba MJ (2013) The cephalopod specialties: complex nervous system, learning, and cognition. Can J Zool 91:431–449

    Article  Google Scholar 

  • Mather JA, Leite TS, Anderson RC, Wood JB (2014) Foraging and cognitive competence in octopuses. In: Darmaillacq A-S, Dickel L, Mather JA (eds) Cephalopod cognition. Cambridge University Press, Cambridge, p 125

    Chapter  Google Scholar 

  • Mellor DJ (2016) Updating animal welfare thinking: moving beyond the “Five Freedoms” towards “a life worth living”. Animals (Basel) 6:21

    Article  Google Scholar 

  • Mendl M, Paul ES (2004) Consciousness, emotion and animal welfare: insights from cognitive science. Anim Welf 13:17–25

    Google Scholar 

  • Merkin GV, Stien LH, Pittman K, Nortvedt R (2014) The effect of stunning methods and season on muscle texture hardness in Atlantic Salmon (Salmo salar L.). J Food Sci 79:E1137–E1141

    Article  CAS  PubMed  Google Scholar 

  • Mesa-Gresa P, Ramos-Campos M, Redolat R (2016) Corticosterone levels and behavioral changes induced by simultaneous exposure to chronic social stress and enriched environments in NMRI male mice. Physiol Behav 158:6–17

    Article  CAS  PubMed  Google Scholar 

  • Moltschaniwskyj NA, Hall K, Lipinski MR, Marian JEAR, Nishiguchi M, Sakai M, Shulman DJ, Sinclair B, Sinn DL, Staudinger M, Van Gelderen R, Villanueva R, Warnke K (2007) Ethical and welfare considerations when using cephalopods as experimental animals. Rev Fish Biol Fish 17:455–476

    Article  Google Scholar 

  • Mooney TA, Hanlon R, Madsen PT, Christensen-Dalsgaard J, Ketten DR, Nachtigall PE (2012) Potential for sound sensitivity in cephalopods. In: The effects of noise on aquatic life. Springer, New York, NY, pp 125–128

    Chapter  Google Scholar 

  • Moynihan MH (1997) Self-awareness, with specific references to coleoid cephalopods. In: Mitchell RW, Thompson NS, Miles HL (eds) Anthropomorphism, anecdotes and animals. Albany State University of NY Press, New York, NY, pp 213–219

    Google Scholar 

  • Moynihan M, Rodaniche AF (1982) The behavior and natural history of the Caribbean reef squid Sepioteuthis sepioidea. With a consideration of social, signal and defensive patterns for difficult and dangerous environments. Adv Ethol 25:1–150

    Google Scholar 

  • Nakajima R, Ikeda Y (2017) A catalog of the chromatic, postural, and locomotor behaviors of the pharaoh cuttlefish (Sepia pharaonis) from Okinawa Island, Japan. Mar Biodivers 47:735. https://doi.org/10.1007/s12526-017-0649-8

    Article  Google Scholar 

  • Nande M, Presa P, Roura Á, Andrews PL, Pérez M (2017) Prey capture, ingestion, and digestion dynamics of Octopus vulgaris paralarvae fed live zooplankton. Front Physiol 8:573

    Article  PubMed  PubMed Central  Google Scholar 

  • Nordgren A (2010) For our children: the ethics of animal experimentation in the age of genetic engineering. Rodopi, Amsterdam

    Google Scholar 

  • Nosengo N (2011) European directive gets its tentacles into octopus research. Nature 2011:229. https://doi.org/10.1038/news.2011.229

    Article  Google Scholar 

  • O’Brien CE, Mezrai N, Darmaillacq AS, Dickel L (2017) Behavioral development in embryonic and early juvenile cuttlefish (Sepia officinalis). Dev Psychobiol 59:145–160

    Article  PubMed  Google Scholar 

  • Ohl F, van der Staay FJ (2012) Animal welfare: at the interface between science and society. Vet J 192:13–19. https://doi.org/10.1016/j.tvjl.2011.05.019

    Article  CAS  PubMed  Google Scholar 

  • Oshima M, di Pauli von Treuheim T, Carroll J, Hanlon RT, Walters ET, Crook RJ (2016) Peripheral injury alters schooling behavior in squid, Doryteuthis pealeii. Behav Processes 128:89–95

    Article  PubMed  Google Scholar 

  • Otovic P, Hutchinson E (2015) Limits to using HPA axis activity as an indication of animal welfare. ALTEX 32:41–50

    Article  PubMed  Google Scholar 

  • Packard A (1972) Cephalopods and fish: the limits of convergence. Biol Rev 47:241–307

    Article  CAS  Google Scholar 

  • Perez PV, Butler-Struben HM, Crook RJ (2017) The selective serotonin reuptake inhibitor fluoxetine increases spontaneous afferent firing, but not mechanonociceptive sensitization, in octopus. Invertebr Neurosci 17:10. https://doi.org/10.1007/s10158-017-0203-1

    Article  CAS  Google Scholar 

  • Petrosino G (2015) The transcriptional landscape of the nervous system of Octopus vulgaris. Ph.D. thesis, Università degli Studi di Napoli Federico II, Napoli

    Google Scholar 

  • Ponder W, Lindberg DR (2008) Phylogeny and evolution of the Mollusca. Universisty of California Press, Berkeley, CA

    Book  Google Scholar 

  • Ponte G, Fiorito G (2015) Immunohistochemical analysis of neuronal networks in the nervous system of Octopus vulgaris. In: Merighi A, Lossi L (eds) Immunocytochemistry and related techniques. Springer, New York, NY, pp 63–79

    Chapter  Google Scholar 

  • Ponte G, Sykes AV, Cooke GM, Almansa E, Andrews PL (2017) The digestive tract of cephalopods: toward non-invasive in vivo monitoring of its physiology. Front Physiol 8:403

    Article  PubMed  PubMed Central  Google Scholar 

  • Pugliese C, Mazza R, Andrews PL, Cerra MC, Fiorito G, Gattuso A (2016) Effect of different formulations of magnesium chloride used as anesthetic agents on the performance of the isolated heart of Octopus vulgaris. Front Physiol 7:610

    Article  PubMed  PubMed Central  Google Scholar 

  • Rocha F, Guerra Á, González ÁF (2001) A review of reproductive strategies in cephalopods. Biol Rev 76:291–304

    Article  CAS  PubMed  Google Scholar 

  • Schnell AK, Smith CL, Hanlon RT, Hall KC, Harcourt R (2016) Cuttlefish perform multiple agonistic displays to communicate a hierarchy of threats. Behav Ecol Sociobiol 70:1643–1655

    Article  Google Scholar 

  • Seibel BA (2016) Cephalopod susceptibility to asphyxiation via ocean incalescence, deoxygenation, and acidification. Physiology 31:418–429

    Article  CAS  PubMed  Google Scholar 

  • Shigeno S, Parnaik R, Albertin CB, Ragsdale CW (2015) Evidence for a cordal, not ganglionic, pattern of cephalopod brain neurogenesis. Zool Lett 1:26

    Article  Google Scholar 

  • Shomrat T, Turchetti-Maia AL, Stern-Mentch N, Basil JA, Hochner B (2015) The vertical lobe of cephalopods: an attractive brain structure for understanding the evolution of advanced learning and memory systems. J Comp Physiol A 201:947–956

    Article  CAS  Google Scholar 

  • Sinn DL, Moltschaniwskyj NA (2005) Personality traits in Dumpling squid (Euprymna tasmanica): context-specific traits and their correlation with biological characteristics. J Comp Psychol 119:99–110

    Article  PubMed  Google Scholar 

  • Sinn DL, Perrin NA, Mather JA, Anderson RC (2001) Early temperamental traits in an octopus (Octopus bimaculoides). J Comp Psychol 115:351–364

    Article  CAS  PubMed  Google Scholar 

  • Smith JA, Andrews PLR, 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

    Article  Google Scholar 

  • Solé M, Lenoir M, Durfort M, López-Bejar M, Lombarte A, André M (2013) Ultrastructural damage of Loligo vulgaris and Illex coindetii statocysts after low frequency sound exposure. PLoS One 8:e78825

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sousounis K, Ogura A, Tsonis PA (2013) Transcriptome analysis of Nautilus and Pygmy squid developing eye provides insights in lens and eye evolution. PLoS One 8:e78054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Spangenberg EM, Keeling LJ (2016) Assessing the welfare of laboratory mice in their home environment using animal-based measures – a benchmarking tool. Lab Anim 50:30–38. https://doi.org/10.1177/0023677215577298

    Article  CAS  PubMed  Google Scholar 

  • Stokes WS (2002) Humane endpoints for laboratory animals used in regulatory testing. ILAR J 43:S31–SS8

    CAS  PubMed  Google Scholar 

  • Sweeney MJ, Roper CF (1998) Classification, type localities, and type repositories of recent cephalopoda. Smithson Contrib Zool 586:561–599

    Google Scholar 

  • Sykes AV, Domingues PM, Márquez L, Andrade JP (2011) The effects of tank colours on the growth and survival of cuttlefish (Sepia officinalis, Linnaeus 1758) hatchlings and juveniles. Aquac Res 42:441–449

    Article  Google Scholar 

  • Sykes AV, Baptista FD, Goncalves RA, Andrade JP (2012) Directive 2010/63/EU on animal welfare: a review on the existing scientific knowledge and implications in cephalopod aquaculture research. Rev Aquac 4:142–162

    Article  Google Scholar 

  • Sykes AV, Pereira D, Rodríguez C, Lorenzo A, Andrade JP (2013) Effects of increased tank bottom areas on cuttlefish (Sepia officinalis, L.) reproduction performance. Aquac Res 44:1017–1028

    Article  Google Scholar 

  • Sykes AV, Alves A, Capaz JC, Madeira C, Couto AT, Gonçalves RA, Frias PA, Leal I, Andrade JP (2017) Refining tools for studying cuttlefish (Sepia officinalis) reproduction in captivity: in vivo sexual determination, tagging and DNA collection. Aquaculture 479:13–16

    Article  CAS  Google Scholar 

  • Trueblood LA, Zylinski S, Robison BH, Seibel BA (2015) An ethogram of the Humboldt squid Dosidicus gigas Orbigny (1835) as observed from remotely operated vehicles. Behaviour 152:1911–1932

    Article  Google Scholar 

  • Vardanis G, Divanach P, Pavlidis M (2017) Comparison of alternative slaughter methods for sea bream, Sparus aurata with respect to stress response. 8ο Πανελλήνιο Συμποσιο Ωκεανογραφίας & Αλιείας:1113–1116

    Google Scholar 

  • Vidal EAG, Villanueva R, Andrade JP, GleadaIl IG, Iglesias J, Koueta N, Rosas C, Segawa S, Grasse B, Franco-Santos RM, Albertin CB, Caamal-Monsreal C, Chimal ME, Edsinger-Gonzales E, Gallardo P, Le Pabic C, Pascual C, Roumbedakis K, Wood J (2014) Cephalopod culture: current status of main biological models and research priorities. Adv Mar Biol 67:1–98. https://doi.org/10.1016/b978-0-12-800287-2.00001-9

    Article  PubMed  Google Scholar 

  • Villanueva R, Norman MD (2008) Biology of the planktonic stages of benthic octopuses. In: Gibson R, Atkinson R, Gordon J (eds) Oceanography and marine biology: an annual review. Taylor & Francis, Boca Raton, NY, pp 105–202

    Chapter  Google Scholar 

  • Villanueva R, Perricone V, Fiorito G (2017) Cephalopods as predators: a short journey among behavioral flexibilities, adaptions, and feeding habits. Front Physiol 8:598

    Article  PubMed  PubMed Central  Google Scholar 

  • Xavier JC, Allcock AL, Cherel Y, Lipinski MR, Pierce GJ, Rodhouse PG, Rosa R, Shea EK, Strugnell JM, Vidal EA (2015) Future challenges in cephalopod research. J Mar Biol Assoc U K 95:999–1015

    Article  Google Scholar 

  • Zepeda EA, Veline RJ, Crook RJ (2017) Rapid associative learning and stable long-term memory in the squid Euprymna scolopes. Biol Bull 232:212–218

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Biology and Evolution of Marine Organisms, Stazione Zoologica Anton Dohrn, Napoli, Italy

    Giovanna Ponte, Paul Andrews & Graziano Fiorito

  2. Association for Cephalopod Research ‘CephRes’ – a non-profit research organization, Napoli, Italy

    Giovanna Ponte, Paul Andrews, Viola Galligioni & Graziano Fiorito

  3. Comparative Medicine Unit, Trinity College Dublin, Dublin, Ireland

    Viola Galligioni

  4. Direcção-Geral dos Recursos Naturais, Segurança e Serviços Marítimos, DGRM/DRI, Lisbon, Portugal

    João Pereira

  5. Departamento do Mar e Recursos Marinhos, IPMA, Lisbon, Portugal

    João Pereira

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  1. Giovanna Ponte
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  2. Paul Andrews
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  3. Viola Galligioni
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  4. João Pereira
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  5. Graziano Fiorito
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Correspondence to Giovanna Ponte .

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  1. Department of Ecological and Biological Sciences, Ichthyogenic Experimental Marine Centre (CISMAR), University of Tuscia, Tarquinia, Viterbo, Italy

    Claudio Carere

  2. Department of Psychology, University of Lethbridge, Lethbridge, AB, Canada

    Jennifer Mather

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Ponte, G., Andrews, P., Galligioni, V., Pereira, J., Fiorito, G. (2019). Cephalopod Welfare, Biological and Regulatory Aspects: An EU Experience. In: Carere, C., Mather, J. (eds) The Welfare of Invertebrate Animals. Animal Welfare, vol 18. Springer, Cham. https://doi.org/10.1007/978-3-030-13947-6_9

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