Behavioral changes in senescent giant Pacific octopus (Enteroctopus dofleini) are associated with peripheral neural degeneration and loss of epithelial tissue

Holst, Meghan M; Hauver, Camille M; Stein, Rachel S; Milano, Bianca L; Levine, Lindsey H; Zink, Andrew G.; Watters, Jason V.; Crook, Robyn J.

doi:10.1016/j.cbpa.2022.111263

Cited by 8 publications

(3 citation statements)

References 34 publications

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“…Alternatively, during senescence, octopuses undergo degeneration of body and nervous system function and cognitive declines that could contribute to disturbed sleep (Anderson et al, 2002;Halm et al, 2000;Holst & Miller-Morgan, 2020). Early in senescence, captive giant Pacific octopuses (Enteroctopus dofleini) display a behavioral hypersensitivity in which mild dermal stimulation could be perceived as aversive (Holst et al, 2022). Given our octopus had the most episodes and most severe episode (Episode 3) nearly 6 weeks prior to its death, these behaviors could indicate it was experiencing effects of senescence yet to be detected in cephalopods.…”

Section: Discussionmentioning

confidence: 99%

Abnormal behavioral episodes associated with sleep and quiescence in Octopusinsularis: Possible nightmares in a cephalopod?

Ramos,

Steinblatt,

Demsey

et al. 2023

Preprint

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This paper presents some unusual behaviors observed in one single specimen of O. insularis. While nothing can be concluded rigorously from such data, we share the data and our analysis with the community, in the hope that others will be on the lookout for such rare events. Sleep is a fundamental biological function that is present in all tested vertebrates and most invertebrates. Cephalopods, such as octopuses, are cognitively complex animals that display active and inactive sleep states similar to those of vertebrates. In particular, octopuses have active sleep states during which they display sequences of camouflage patterns and modulation of basal rhythms, while remaining relatively unresponsive to outside stimuli. Some scientists have speculated that these states could be analogous to dreaming in mammals, involving episodic recall with a narrative structure. The convergent evolution of sleep in neurologically complex animals is a striking possibility, but its demonstration requires overcoming significant challenges. Towards this end, capturing abnormal sleep-associated episodes and other parasomnias in cephalopods can provide further insight into the biology of their sleep. This study reports abnormal behavioral episodes associated with transitions between activity states and sleep states observed in a male Octopus insularis. The study used continuous video monitoring to characterize the animal's activity patterns and detect rare behavioral episodes. Over the course of a month, four brief episodes (duration range: 44-290 seconds) were identified during which the octopus abruptly emerged from quiescent or active sleep, detached itself from its sleep position, and engaged in antipredator and predatory behaviors (with no predator present). The longest of these episodes resembled the species-typical response to a predatory attack, suggesting that the animal may have been responding to a negative episodic memory or exhibiting a form of parasomnia. These findings, in conjunction with recent evidence for sleep in octopuses, highlight the complexity of possible sleep-associated behavioral episodes. Investigating sleep in invertebrates is crucial to understanding the evolution of sleep across distantly related species.

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Section: Discussionmentioning

confidence: 99%

Abnormal behavioral episodes associated with sleep and quiescence in Octopusinsularis: Possible nightmares in a cephalopod?

Ramos,

Steinblatt,

Demsey

et al. 2023

Preprint

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“…A 2022 study comparing post-euthanasia arm tip tissue demonstrated differences between healthy and senescent GPOs. This suggests that proactive welfare management should begin earlier in senescence due to neural degeneration and the loss of epithelial tissue [ 39 ]. Additional studies of anesthesia and analgesia are critical to determining which techniques may best decrease pain, discomfort, and distress.…”

Section: Discussionmentioning

confidence: 99%

Characterization of Current Husbandry and Veterinary Care Practices of the Giant Pacific Octopus (Enteroctopus dofleini) Using an Online Survey

Kirby

Balko

Goertz

et al. 2023

Veterinary Sciences

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Giant Pacific octopuses (Enteroctopus dofleini) (GPOs) are commonly housed in zoos or aquaria, and sedation, anesthesia, and/or euthanasia may be indicated for a variety of reasons. Despite this need, evidence-based data on best practices is limited and focuses on smaller or more tropical species. The objectives of this study were to survey the aquatic community regarding the husbandry and veterinary care of GPOs, with a specific focus on anesthetic and euthanasia protocols. A two-part web-based survey was distributed to four aquatic and/or veterinary email listservs. Individuals from fifty-two institutions participated in phase one. Results documented that 40 (78 percent) participating institutions currently house GPOs, with most housing one and nine institutions housing two to three GPOs. The median (range) habitat volume is 5405 (1893–16,465) L, and 78 percent of systems are closed. Of the institutions surveyed, 23 have anesthetized or sedated a GPO for nonterminal procedures, including wound care, biopsies, and hemolymph collection. Reported methods of sedation or anesthesia include magnesium chloride, ethanol, isoflurane, tricaine methanesulfonate (MS-222), magnesium sulfate, benzocaine, and dexmedetomidine. Drugs or methods used for euthanasia include magnesium chloride, ethanol, mechanical decerebration, pentobarbital, isoflurane, MS-222, magnesium sulfate, benzocaine, potassium chloride, dexmedetomidine, and freezing. Reported observed side effects include ineffectiveness or inadequate sedation, inking, prolonged drug effects, and behavior changes. Survey data have the potential to guide the husbandry and veterinary care of GPOs and build the framework for future prospective studies on GPO sedation and anesthesia.

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“…This abnormal motor coordination compromises welfare, as it negatively affects the ability to perform basic maintenance behaviors such as grooming, which may lead to the accumulation of parasites on the skin. In the laboratory, abnormal motor behavior is often associated with imminent death [61].…”

Section: Discussionmentioning

confidence: 99%

Assessing Negative Welfare Measures for Wild Invertebrates: The Case for Octopuses

Andrade,

Santos,

De Paiva

et al. 2023

Animals

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Welfare metrics have been established for octopuses in the laboratory, but not for octopuses living in the wild. Wild octopuses are constantly exposed to potentially harmful situations, and the ability to assess the welfare status of wild octopuses could provide pertinent information about individuals’ health and species’ resilience to stressors. Here, we used underwater photos and videos to identify injuries and stress-related behaviors in wild Octopus insularis in a variety of contexts, including interacting with fishermen, interacting with other octopuses and fish, proximity to predators, in den, foraging, and in senescence. We adapted established metrics of octopus welfare from the laboratory to these wild octopuses. In addition to observing all of the stress measures, we also identified two previously unknown measures associated with decreased welfare: (1) a half white eye flash and (2) a half-and-half blotch body pattern. More than half of the individuals analyzed had arm loss, and almost half of the individuals had skin injuries. We also observed that irregular chromatophore expression and abnormal motor coordination were associated with interactions with fishermen. This is the first study to apply measures of welfare from the laboratory to wild octopuses. Our results may also aid in the identification of welfare measures for other wild invertebrates.

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Behavioral changes in senescent giant Pacific octopus (Enteroctopus dofleini) are associated with peripheral neural degeneration and loss of epithelial tissue

Cited by 8 publications

References 34 publications

Abnormal behavioral episodes associated with sleep and quiescence in Octopusinsularis: Possible nightmares in a cephalopod?

Abnormal behavioral episodes associated with sleep and quiescence in Octopusinsularis: Possible nightmares in a cephalopod?

Characterization of Current Husbandry and Veterinary Care Practices of the Giant Pacific Octopus (Enteroctopus dofleini) Using an Online Survey

Assessing Negative Welfare Measures for Wild Invertebrates: The Case for Octopuses

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