Enormous gill chambers of deep-sea coffinfishes (Lophiiformes: Chaunacidae) support unique ventilatory specialisations such as breath holding and extreme inflation

Abstract

Deep sea habitats tend to favor species with low energetic demands, and therefore we predict that deep sea fishes will have behavioral and morphological specializations of the gill ventilatory system to reduce the energetic cost of pumping water across the gills. However, it is difficult to study functional morphology of deep sea fishes due the lack of ability to conduct laboratory experiments with living fishes. For this study, we combined analysis of publicly available video recorded by remote-operated vehicles (ROV) with detailed anatomical study of museum specimens to document the functional morphology of the massive gill chambers that are observed in coffinfishes (Lophiiformes: Chaunacidae). Chaunacids, like other lophiiforms, exhibit highly specialised ventilatory anatomy such as an enlarged branchiostegal apparatus and restricted gill openings, but videos show them using this anatomy in a new and unusual way. We observed eight individuals ventilating extremely slowly at rates of 0.03–0.004 Hz, during which the gill chambers were full yet we saw no inhalation or exhalation for periods of 26 to 245 s. This holding breath behaviour has not been observed in any other fishes and is probably highly energetically efficient. This inflation of the gill chambers also increases body volume by up to 30%, making them more globose and difficult to be taken as prey, much like stomach inflation in pufferfishes (Tetraodontidae). We also used micro computed-tomography (CT) scans to document the enormous branchiostegal rays and associated muscles that support this unique behaviour.