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

Abstract

Most species of octopus experience extreme physical decline after a single reproductive bout which extends over a period of days, weeks, or months before eventual death. Although outward indicators of senescence are widely recognized, comparatively little is known about physiological and neural changes accompanying terminal decline in octopuses. Here, we measured changes in behavioral response to nociceptive stimuli across the lifespan in giant Pacific octopus (GPO), Enteroctopus dofleini, held in public aquariums in the USA. Post-euthanasia, tissue was collected from arm tips, and neural and epithelial cell degeneration was quantified and compared with biopsies of arm tips from healthy, pre-reproductive GPOs. Behavioral assays showed significant changes both in low threshold mechanosensory responses and nociceptive behavioral responses beginning early in senescence and extending until euthanasia. Histology data showed that while the ratio of apoptotic cells to total cell number stayed constant between healthy and senescent GPOs, overall neural and epithelial cell density was significantly lower in terminally senescent octopuses compared with healthy controls. Our data provide new insight into the time-course and causes of sensory dysfunction in senescent cephalopods and suggest proactive welfare management should begin early in the senescence phase, well before animals enter terminal decline.