Development and sexual dimorphism of the sonic system in three deep-sea neobythitine fishes and comparisons between upper mid and lower continental slope

Abstract

Based on morphology, NB Marshall identified cusk-eels (family Ophidiidae) as one of the chief sound-producing groups on the continental slope. Due to food scarcity, we hypothesized that sonic systems will be reduced at great depths despite their potential importance in sexual reproduction. We examined this hypothesis in the cuskeel subfamily Neobythitinae by comparing sonic morphology in Atlantic species from the upper-mid (Dicrolene intronigra) and deeper continental slope (Porogadus miles and Bathyonus pectoralis) with three Taiwanese species previously described from the upper slope (Hoplobrotula armatus, Neobythites longipes and N. unimaculatus). In all six species, medial muscles are heavier in males than in females. Dicrolene has four pairs of sonic muscles similar to the shallow Pacific species, suggesting neobythitine sonic anatomy is conservative and sufficient food exists to maintain a well-developed system at depths exceeding 1 km. The sonic system in Porogadus and Bathyonus was reduced to a single pair of ventral medial muscles that connects to a smaller and thinner swimbladder via a long tendon. Small muscle fiber diameters, a likely indicator of rapid contraction, were present in males of five of the species. However, in Bathyonus, the deepest species (pale coloration, reduced eye size, shorter sonic muscles and longer tendons), muscle fibers were larger suggesting an adaptation to facilitate rapid bladder movement for sound production while using slower contractions and less metabolic energy. The six species separate into three groups in length-weight regressions: the three upper slope species have the greatest weights per unit length, Dicrolene is lower, and the two deep species are further reduced consistent with the hypothesis that food limitation affects sonic anatomy at great depths.

Sexual dimorphism in the sonic system and otolith morphology of Neobythites gilli (Ophidiiformes)

“…Although in many Ophidiiforms it is not possible to externally distinguish males from females, there is growing evidence that sexual dimorphism in the sound‐producing apparatus is important in this taxa. This has been shown in some Carapinae (Parmentier & Vandewalle, ; Kéver et al ., ), Ophidiidae (Courtenay, ; Casadevall et al ., ; Nguyen et al ., ; Kéver et al ., ) and Neobythitinae (Carter & Musick, ; Ali et al ., ; Fine et al ., ). Due to their way of life in darker or deep waters, the environmental pressures on external features is probably more limited, which may help to explain the lack of differences between male and female phenotypes.…”

“…The same kind of difference in muscle size between males and females was also recently reported in the sonic ventral muscles of sister taxa N. unimaculatus and N. longipes (Ali et al ., ). Moreover, this sonic dimorphism in muscle size (weight) was already shown in different Ophidiiform species (Fine et al ., , ; Parmentier et al ., ; Kéver et al ., ). This difference is well marked in the ventral muscle, most probably because this muscle provides the power required for sound production, whereas the intermediate muscle appears to be confined to a preparation or support function (Parmentier et al ., , ; Kéver et al ., ).…”

“…Because many species live in deep water, sound recordings are difficult to make and apply to only a few species from the carapid (Parmentier, Vandewalle & Lagard ere, 2003;K ever et al, 2014d) and ophidiid genera (Rountree & Bowers-Altman, 2002;K ever et al, 2014a). These studies have also underlined the required morphological adaptations related to this way of communication: Ophidiiforms have a high diversity of sound-producing mechanisms (Howes, 1992;Parmentier et al, 2006a;Nguyen et al, 2008;Fine et al, 2018).…”

Sound production and sonic apparatus in deep-living cusk-eels (Genypterus chilensis and Genypterus maculatus)

“…Sound-producing mechanisms 1) are found in all but one species examined to date (Howes, 1992;Marshall, 1967), 2) are quite complex with up to 6 sonic muscles (3 pairs) in some species and deep modifications of the swimbladder, rostral vertebral bodies and associated epineurals (Parmentier et al, 2010(Parmentier et al, , 2008a(Parmentier et al, , 2006aRose, 1961), 3) are able to produce different sounds (Mann et al, 1997;Parmentier et al, 2016aParmentier et al, , 2016bParmentier et al, , 2018bParmentier et al, , 2008bSprague and Luczkovich, 2001) and have sexually dimorphic sonic systems (Ali et al, 2016;Casadevall et al, 1996;Kéver et al, 2014aKéver et al, , 2014cNguyen et al, 2008;Rose, 1961). These features clearly support the importance of sonic communication in the Ophidiiformes (Fine et al, 2018(Fine et al, , 2007Nguyen et al, 2008). Since many species live in deep water (Nielsen et al, 1999) sound recordings have only been made for a few shallow species from the Carapidae (Kéver et al, 2014c;Parmentier et al, 2016aParmentier et al, , 2016bParmentier et al, , 2018bParmentier et al, , 2003 and Ophidiidae (Kéver et al, 2016Mooney et al, 2016;Rountree and Bowers-Altman, 2002).…”

“…Fish recordings were already realized around 120 m (Ruppé et al, 2015), but potential fish sounds are also reported deeper, from 700 m to 1800 m (Mann and Jarvis, 2004;Rountree et al, 2012;Wall et al, 2014). The absence of recordings is frustrating since inner anatomy of many deep species clearly indicates they possess muscles attached to the swimbladder (Fine et al, 2018;Howes, 1992;Marshall, 1967;Nguyen et al, 2008), a feature well known to evoke sound production (Fine and Parmentier, 2015). Although sounds may be the best mode of communication for fish active at night (Ruppé et al, 2015) and/or in a large dark environment like the deep-sea (Mann and Jarvis, 2004), the lack of data could be due to different factors such as being at the right place at the right moment, technical limitations or the fact deep-sea fish produce only low amplitude sounds (Wall et al, 2014).…”