Potentially handicapped but otherwise functional: Malformations in prey capture tools show no impacts on octopus life

Abstract Larval mortality is a keystone ecological factor for many benthic octopus since it mostly occurs before their settlement in the sea bottom as benthic juveniles. The literature had revealed that records of adult animals with morphological abnormalities (teratologies) are fewer in species with complex life cycle than in those with direct development. This is a direct consequence of the morphological, physiological, and development challenges that the transition from the larval to the adult morphology represents. During a routine fishing sample, we found an immature female horned octopus with additional buccal structures in two suckers of its ventral arms, likely rendering these suckers as inefficient. Based on the literature about the natural history of octopus, we provide evidence that these abnormalities were present at the moment of hatch. We evaluated the impact of the teratologies by comparing the shape of the buccal beaks and the trophic niche of the individual with five normal conspecifics. Although the beaks showed a different shape than normal individuals, the trophic niche was similar. Surprisingly, the teratological condition of the individual likely had no severe impacts on its life, even though it likely represents a handicap for its survival during its planktonic life. We also comment on other previous records from the literature of teratological adult octopus to highlight the amazing adaptive capacity of octopus to deal with challenging morphologies.

in the early phase of their life cycle (paralarval stage). Because these marine predators have a short lifespan (usually around one year) and die after a single reproductive event, early survival is crucial for the population dynamics of octopus species from the continental shelf.
For this reason, their population maintenance mainly depends on the survival of the planktonic paralarval cohorts.
Overall, the survival rate of individuals with teratologies (developmental malformations) is expected to be lower than normal conspecifics. This is especially true in species with complex life cycles.
Not surprisingly, teratologies are more frequently reported in the adults of animals with direct development than in those with complex life cycles involving metamorphoses (see Fernández-Álvarez et al., 2011 and references therein), indicating the lethality of some of those anomalies, especially during early developmental stages.
During a routine fish sampling using bottom trawling, we found a single-horned octopus (Eledone cirrhosa) displaying additional buccal pieces at the level of the first sucker of both ventral arms (see were three structures: The one closer to the mouth resembled the lower beak with irregular wings, the one placed distally resembled a very narrow upper beak, while the intermediate structure was comparatively smaller, poorly developed, and difficult to allocate to any known cephalopod beak shape but with an unmistakable developing rostrum. Horned octopus paralarvae hatch with 4.5 mm mantle length (ML) and eight small arms equipped with eight suckers each (Mangold et al., 1971). Since hatchling suckers are not replaced through its life, Given that the arms and the buccal mass have primary functions in the prey capture, handling, and feeding process of octopus, these teratologies could place constraints associated with its feeding behavior, perhaps limiting the consumption of similar prey compared to conspecifics without any teratological trait and, thus, negatively Octopus paralarvae feed on planktonic prey, which they capture with the aid of the suckers and arms, just before using their beaks to both wound the prey and inoculate its body with digestive enzymes and finally to suck-up the predigested content (Villanueva & Norman, 2008). The internal pressure reduction that enables an octopus sucker to function requires the strong action of its muscles coupled with an efficient seal against the surface of the prey (Kier & Smith, 2002), helped by the mucus film that covers the sucker surface in octopus paralarvae (Accogli et al., 2017). Thus, the presence of the extranumeral beaks in the suckers could not only compromise the tridimensional structure of the musculature, but it also could disable the sealing of the sucker against the prey surface, hindering prey capture, holding, and subduing and, consequently, rendering the affected suckers inefficient. Due to their position near the mouth, the basal suckers from each arm are paramount during feeding operations, since they keep the prey in the right position for killing and eating it. In addition, suckers have mechano-and chemoreceptors used to select the food quality ingested (Villanueva & Norman, 2008). Therefore, it seems logical to hypothesize that two malfunctional suckers in this position represent an important disadvantage in comparison with conspecifics, particularly during the delicate paralarval period.
Previous literature shows a few examples of teratological octopus which were able to reach adulthood even with characters that compromise their survival, such as the absence of a gill or with F I G U R E 2 Graph showing the length/ weight relationship for horned octopus based on the equation provided by Jereb et al. (2015); the red point signals the actual weight and length of the teratological individual. Abbreviations: TW, total weight; ML, mantle length F I G U R E 3 (a) Detail of the landmarks defined in this study for the upper (up) and lower (down) beaks. (b) Morphospaces of the upper (in shaded blue) and lower (in shaded green) beak shape and isotopic space (in shaded orange) of the analyzed horned octopus individuals, highlighting the position (colored points) of the teratological specimen in each space. Scale bar: 1 mm