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.

Pelvic-Fan Flaring and Inflation in the Three-Tooth Puffer, Triodon macropterus (Tetraodontiformes: Triodontidae), with Additional Observations on Their Behavior in Captivity

“…comm., 18 December 2021). Long and Farina (2019) reported gill chamber (i.e., not the stomach) inflation in chaunacids during ventilation and suggested that such inflation may play a defensive role because it increases body size. Inflation may occur in frogfishes (Antennariidae; see Pietsch and Arnold, 2020: 452–454; also Ferreira et al, 2022), but the evidence and mechanism are unclear.…”

A survey of fish behaviour quantification indexes and methods in aquaculture

“…It is hard to calculate the area of opercular directly using machine vision. However, alternative characteristics can be measured, such as the time of each phase of ventilation (Zheng et al 2014;Farina & Bemis 2016;Long & Farina 2019). Conversely, ventilation activity has apparent external and internal changes.…”

A multi-tasking stomach: functional coexistence of acid–peptic digestion and defensive body inflation in three distantly related vertebrate lineages

“…Body inflation is an antipredator defensive mechanism [1]. Examples among vertebrates include amphibians and reptiles that use lung or buccal cavity inflation [2,3], the coffinfishes (Chaunacidae) that inflate by storing a substantial volume of water in their gill chambers [4], and notably within the stomach inflating pufferfishes and porcupine fishes (Tetraodontidae and Diodontidae sister families, respectively, Tetraodontiformes), herein referred to as 'pufferfishes', for simplicity. Pufferfishes can increase up to three times their body size by swallowing large amounts of water that is held within the stomach [5][6][7].…”

“…Pepsinogens are fundamental for acid-peptic digestion where the conversion from pepsinogen to pepsin (the active form) is promoted by both HCl and auto-catalysis [23,24]. In this way, gastric acidity promotes protein digestion and cell lysis, facilitating the release and absorption of nutrients [25], improving PO 4 3− and Ca 2+ uptake, and providing innate immune protection against pathogen entry into the intestine [19,22,26]. Surprisingly, despite the major advantages of a functional acid-peptic stomach, several secondary loss events of structure and function have occurred in the gnathostome lineage, most commonly in the Teleostei, but also in the Holocephali, dipnoids and monotremes [21, [27][28][29].…”