Abstract
BackgroundOctopoda utilise their arms for a diverse range of functions, including locomotion, hunting, defence, exploration, reproduction, and grooming. However the natural environment contains numerous threats to the integrity of arms, including predators and prey during capture. Impressively, octopoda are able to close open wounds in an aquatic environment and can fully regenerate arms. The regrowth phase of cephalopod arm regeneration has been grossly described; however, there is little information about the acute local response that occurs following an amputation injury comparable to that which frequently occurs in the wild.MethodsAdult Octopus vulgaris caught in the Bay of Naples were anaesthetised, the distal 10 % of an arm was surgically amputated, and wounded tissue was harvested from animals sacrificed at 2, 6, and 24 h post-amputation. The extent of wound closure was quantified, and the cell and tissue dynamics were observed histologically, by electron microscopy, as well as using ultrasound.ResultsMacroscopic, ultrasonic and ultrastructural analyses showed extensive and significant contraction of the wound margins from the earliest time-point, evidenced by tissue puckering. By 6 h post amputation, the wound was 64.0 ± 17.2 % closed compared to 0 h wound area. Wound edge epithelial cells were also seen to be migrating over the wound bed, thus contributing to tissue repair. Temporary protection of the exposed tip in the form of a cellular, non-mucus plug was observed, and cell death was apparent within two hours of injury. At earlier time-points this was apparent in the skin and deeper muscle layers, but ultimately extended to the nerve cord by 24 h.ConclusionsThis work has revealed that O. vulgaris ecologically relevant amputation wounds are rapidly repaired via numerous mechanisms that are evolutionarily conserved. The findings provide insights into the early processes of repair preparatory to regeneration. The presence of epithelial, chromatophore, vascular, muscle and neural tissue in the arms makes this a particularly interesting system in which to study acute responses to injury and subsequent regeneration.Electronic supplementary materialThe online version of this article (doi:10.1186/s40851-016-0044-5) contains supplementary material, which is available to authorized users.
Highlights
Octopoda utilise their arms for a diverse range of functions, including locomotion, hunting, defence, exploration, reproduction, and grooming
Limb regeneration is a well-established phenomenon in members of all four orders of coleoid cephalopod (e.g. S. officinalis [9], Sepioteuthis lessoniana [10]; squid, Omnastrephes bartrami [11], Octopoteuthis deletron [12]; O. vulgaris [13]; and deep sea octopus, Vampyroteuthis infernalis [14]), it is rarely mentioned in reviews of comparative aspects of regeneration, despite the broad acknowledgment that knowledge of the underlying evolutionary processes would better inform our understanding of the fundamental mechanisms of regeneration [8, 15]
There was no arm withdrawal in response to the transection, but the proximal arm recoiled from the transected distal tip by a few millimetres, indicating that the arm was under some longitudinal tension
Summary
Octopoda utilise their arms for a diverse range of functions, including locomotion, hunting, defence, exploration, reproduction, and grooming. The limbs (arms and tentacles) are one of the most striking external features of the approximately 700 known extant species of cephalopods ranging from the numerous tentacles of nautiloids (e.g. Nautilus pompilius) to the eight arms and two tentacles of cuttlefish (e.g. Sepia officinalis) and squid (e.g. Loligo pealii) and the eight arms of octopoda (e.g. Octopus vulgaris, [1]). Limb regeneration is a well-established phenomenon in members of all four orders of coleoid cephalopod (e.g. S_officinalis [9], Sepioteuthis lessoniana [10]; squid, Omnastrephes bartrami [11], Octopoteuthis deletron [12]; O. vulgaris [13]; and deep sea octopus, Vampyroteuthis infernalis [14]), it is rarely mentioned in reviews of comparative aspects of regeneration, despite the broad acknowledgment that knowledge of the underlying evolutionary processes would better inform our understanding of the fundamental mechanisms of regeneration [8, 15]
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