Bite force is limited by the force-length relationship of skeletal muscle in black carp, Mylopharyngodon piceus

Abstract

Bite force is critical to feeding success, especially in animals that crush strong, brittle foods. Maximum bite force is typically measured as one value per individual, but the force-length relationship of skeletal muscle suggests that each individual should possess a range of gape height-specific, and, therefore, prey size-specific, bite forces. We characterized the influence of prey size on pharyngeal jaw bite force in the snail-eating black carp (Mylopharyngodon piceus, family Cyprinidae), using feeding trials on artificial prey that varied independently in size and strength. We then measured jaw-closing muscle lengths in vivo for each prey size, and then determined the force-length relationship of the same muscle in situ using tetanic stimulations. Maximum bite force was surprisingly high: the largest individual produced nearly 700 N at optimal muscle length. Bite force decreased on large and small prey, which elicited long and short muscle lengths, respectively, demonstrating that the force-length relationship of skeletal muscle results in prey size-specific bite force.

Figure 1.

Prey strength, prey size and individual success. (a) Size and strength (mean±1 s.d.) of manufactured prey items. Grey level reflects tube size. (b–d) Prey crushing performance by each of the three individuals: 106, 81 and 75 mm head length, respectively. Crushing success spans 100% (black) to 0% (white).

Figure 2.

Anatomy and performance of black carp pharyngeal jaws. (a) Left lateral view of the bones associated with the pharyngeal jaw. (b) Lateral view, parasagittal cut-away, showing a schematic of the jaw-closing muscle and individual fibres tracked using XROMM. Note that muscle fibre orientations converge near the bite point, so little or no musculoskeletal leverage amplifies muscle force. (c) In situ force–length relationships (light grey) and in vivo tube-crushing performance (black triangles), normalized to L/L₀ and P/P₀. Each grey symbol represents a single in situ contraction in one individual (head lengths: circle, 106 mm; square, 81 mm; diamond, 75 mm). Up-pointing triangles indicate strongest crushable prey item in vivo, and down-pointing triangles indicate weakest uncrushable prey item; x-axis error bars denote ±1 s.d. of in vivo muscle lengths, y-axis error bars denote ±1 s.d. of prey strength determined via materials testing. All in vivo data are pooled in this figure; see electronic supplementary material, figure S1 for in vivo muscle length and performance data by individual.