Vampire squid: detritivores in the oxygen minimum zone

Abstract

Vampire squid (Vampyroteuthis infernalis) are considered phylogenetic relics with cephalopod features of both octopods and squids. They lack feeding tentacles, but in addition to their eight arms, they have two retractile filaments, the exact functions of which have puzzled scientists for years. We present the results of investigations on the feeding ecology and behaviour of Vampyroteuthis, which include extensive in situ, deep-sea video recordings from MBARI's remotely operated vehicles (ROVs), laboratory feeding experiments, diet studies and morphological examinations of the retractile filaments, the arm suckers and cirri. Vampire squid were found to feed on detrital matter of various sizes, from small particles to larger marine aggregates. Ingested items included the remains of gelatinous zooplankton, discarded larvacean houses, crustacean remains, diatoms and faecal pellets. Both ROV observations and laboratory experiments led to the conclusion that vampire squid use their retractile filaments for the capture of food, supporting the hypothesis that the filaments are homologous to cephalopod arms. Vampyroteuthis' feeding behaviour is unlike any other cephalopod, and reveals a unique adaptation that allows these animals to spend most of their life at depths where oxygen concentrations are very low, but where predators are few and typical cephalopod food is scarce.

Oxygen, ecology, and the Cambrian radiation of animals

“…The pelagic realm of modern OMZs is characterized by a diversity of carnivores that, in the cores of OMZs, usually migrate to more oxygenated water to pay off this oxygen debt (42). Interestingly, however, some permanently pelagic OMZ residents such as the vampire squid have adapted to low-oxygen levels by losing the carnivorous feeding habit that is primitive for cephalopods and becoming detritivores (43). The inability to pay off an oxygen debt in the chronically low-oxygen benthos, where organisms are unable to migrate to higher-O 2 waters, represents the most likely explanation for the observation that polychaete carnivore species diversity and percentage of the total fauna correlate with oxygen level.…”

Vampire squid reproductive strategy is unique among coleoid cephalopods

“…Life history theory predicts that iteroparity is favoured when adult survival is increased [10]. With the ability to inhabit low oxygen environments, where predators are fewer [6], vampire squid may benefi t from increased adult survival rates, allowing for multiple reproductive cycles at low reproductive cost. …”

“…This coleoid cephalopod occurs at open ocean depths between 500 and 3000 m and is able to inhabit low oxygen environments [5]. Vampire squid feed opportunistically on zooplankton and detritus [6]. Young [7] observed that in adult females, developing eggs were present in various sizes (up to 3 mm), "indicating a lack of a development cycle and a lack of a restricted breeding period", but the exact reproductive strategy of vampire squid remained unknown.…”

“…The metabolic and trophic characteristics of the species suggest a slow pace of life [5,6], and they may not be able to take in enough energy to support the high, short-term fecundity characteristic of semelparity. We hypothesize that only iteroparity can yield a suffi ciently high lifetime reproductive output for this species.…”

“…The length of this resting period in vampire squid is unknown but it is not until a batch of eggs has been spawned, and post-ovulatory follicles degenerate to a quarter of their initial size, that a new batch of oocytes starts to develop. Given that vampire squid have low metabolic rates and ingest low calorie food [5,6], the time to accumulate enough resources for the next spawning episode may be substantial.…”