Bifunctional Role of the Sternohyoideus Muscle During Suction Feeding in Striped Surfperch,Embiotoca lateralis

Autor: T F Martinson, J J Lomax, Elizabeth L. Brainerd, Yordano E. Jimenez
Rok vydání: 2020
Předmět:
Zdroj: Integrative Organismal Biology. 2
ISSN: 2517-4843
DOI: 10.1093/iob/obaa021
Popis: Suction feeding is a powerful and complex process of prey ingestion that relies on contributions from both head and body muscles in fishes. Whereas the cranial and hypobranchial muscles in the head region might intuitively be seen as the main drivers behind suction feeding, the axial muscles of the body have long been understood as necessary contributors to the process as well (Muller and Osse 1984; Westneat 1990; Van Wassenbergh et al. 2007). In many fishes, epaxial muscles contract to rotate and lift the neurocranium while the hypaxial muscles contribute to hyoid depression via pectoral girdle retraction (Lauder 1979, 1982; Liem 1980; Camp and Brainerd 2014). The sternohyoideus (SH) muscle serves as a bridge between the body and the head, transmitting hypaxial muscle power to the hyobranchial elements of the head yet still retaining the potential to act on these elements itself. Recent studies have shown that axial musculature provides a majority of the power for strikes in largemouth bass (Micropterus salmoides) and bluegill sunfish (Lepomis macrochirus; Camp et al. 2015; Camp et al. 2018). In both species, the SH muscle is the only muscle in the head that is large enough to contribute more than negligible power. In largemouth bass, however, the SH function has been found to vary, as the muscle sometimes shortens and other times lengthens around the time of peak gape (Carroll 2004). Peak suction power production occurs just before peak gape, and the SH was later determined to show little to no shortening during periods of peak power production in M. salmoides (Camp et al. 2015). This lack of shortening during peak power indicates that the largemouth bass SH contributes little to no positive work and power. In contrast, bluegill sunfish rapidly shorten the SH during suction feeding, contributing power for both hyoid depression and, by extension, suction expansion (Camp et al. 2018). However, the contribution of the SH is still small, likely providing less than 10% of overall power, though the constant shortening of the bluegill sternohyoid for all studied strikes suggest that 10% may be crucial to generating a successful strike in the bluegill. These muscle strain patterns indicate that in largemouth bass, the SH is active isometrically at the time of peak power production, effectively serving to transmit pectoral girdle rotation and hypaxial muscle power for hyoid depression (Carroll 2004; Carroll et al. 2004; Camp and Brainerd 2014; Camp et al. 2015), whereas in bluegill it serves a dual function both transmitting hypaxial power and contributing its own additional power for hyoid depression. In bluegill, the SH muscle is nearly twice the size of the SH in bass, when measured as a fraction of axial muscle mass (Camp et al. 2015; Camp et al. 2018). Clariid catfishes display this same relationship between SH muscle size and function. Of four species studied, the SH is largest in Gymnallabes typus, and this is the only species that showed SH shortening during suction feeding (Van Wassenbergh et al. 2007). In other studied clariid species, SH muscles were about half the size of G. typus and contracted isometrically during the first half of hyoid depression and then lengthened during the second half (Van Wassenbergh et al. 2007). The clariid catfish and centrarchid results together suggest that the SH may be more likely to shorten and contribute power to suction expansion when the SH is relatively large, whereas, in species in which it is smaller, the SH does not shorten but instead acts much like a stiff ligament to transmit force and power from the hypaxial musculature to the hyoid. If muscle size is to be considered an indicator of sternohyoid bifunctionality, as both a transmitter and contributor to suction power, then studies focused on testing this prediction in species that fit this emerging size-specific criterion are necessary. This study focuses on the suction feeding mechanism of the striped surfperch, Embiotoca lateralis, a species with a large SH muscle relative to M. salmoides and L. macrochirus (the mass of the SH is 8.8% of axial muscle mass in E. lateralis relative to 4.0% in L. macrochirus and 1.7% in M. salmoides; see “Materials and methods” and “Results” sections for more information on these masses). Does the surfperch SH shorten during suction expansion? We use a relatively new method, Video Reconstruction of Moving Morphology (VROMM) (Jimenez et al. 2018; Hoffmann et al. 2019) to track and animate the neurocranium, cleithrum, and a reference body plane, as well as a new method that employs external 3D marker tracking to estimate epaxial and SH muscle strain. As this particular application of external marker tracking is previously undescribed, we additionally present an experimental evaluation of the new method.
Databáze: OpenAIRE
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