Buoyancy control in ammonoid cephalopods refined by complex internal shell architecture

Abstract

The internal architecture of chambered ammonoid conchs profoundly increased in complexity through geologic time, but the adaptive value of these structures is disputed. Specifically, these cephalopods developed fractal-like folds along the edges of their internal divider walls (septa). Traditionally, functional explanations for septal complexity have largely focused on biomechanical stress resistance. However, the impact of these structures on buoyancy manipulation deserves fresh scrutiny. We propose increased septal complexity conveyed comparable shifts in fluid retention capacity within each chamber. We test this interpretation by measuring the liquid retained by septa, and within entire chambers, in several 3D-printed cephalopod shell archetypes, treated with (and without) biomimetic hydrophilic coatings. Results show that surface tension regulates water retention capacity in the chambers, which positively scales with septal complexity and membrane capillarity, and negatively scales with size. A greater capacity for liquid retention in ammonoids may have improved buoyancy regulation, or compensated for mass changes during life. Increased liquid retention in our experiments demonstrate an increase in areas of greater surface tension potential, supporting improved chamber refilling. These findings support interpretations that ammonoids with complex sutures may have had more active buoyancy regulation compared to other groups of ectocochleate cephalopods. Overall, the relationship between septal complexity and liquid retention capacity through surface tension presents a robust yet simple functional explanation for the mechanisms driving this global biotic pattern.

Resurrecting extinct cephalopods with biomimetic robots to explore hydrodynamic stability, maneuverability, and physical constraints on life habits

“…Rather than changing buoyancy for these behaviors, extant nautilids rely on active locomotion 61 . While extinct ectocochleates had disparate internal characteristics that could have influenced the function of their hydrostatic apparatus 62 , 63 (e.g., septal and siphuncular morphologies), it is parsimonious to suggest that extinct ectocochleates (including ammonoids) relied on active swimming as well for vertical movements. An investigation of the relationships between hydrostatic and hydrodynamic properties is necessary to fully understand the directional swimming capabilities of particular morphologies.…”

“…Equation 2 was used in the x, y, and z directions to compute the 3D coordinate position of the center of mass. The centers of mass for the chamber contents (liquid and gas) were set equal to the center of volume of all chambers, a minor assumption considering the capillary retention of liquid around the septal margins in the living animals 62 .…”

Is the relative thickness of ammonoid septa influenced by ocean acidification, phylogenetic relationships and palaeogeographic position?

“…The function of septal frilling and thus the factors causing a selection for ever more complex septal frilling has been widely discussed (e.g., Hewitt & Westermann, 1987 ; Klug & Hoffmann, 2015 ; Klug et al, 2008 ; Lemanis, 2020 ; Peterman et al, 2021 ). These authors suggested, among other things, that septal frilling served for purposes such as liquid retention, increased growth rates, improved resistance against point loads (predation), as well as resistance against hydrostatic pressure.…”

Vertical escape tactics and movement potential of orthoconic cephalopods

“…Full-size  DOI: 10.7717/peerj.11797/fig- 6 from efficiently directing a water jet upward, to counteract positive buoyancy, which may be problematic in the event of shell loss due to predation. This scenario may have been managed by ammonoid orthocones, if their complex septa improved buoyancy regulation (i.e., chamber refilling potential; Daniel et al, 1997;Peterman et al, 2021b). If complex ammonoid sutures (Peterman et al, 2021b) or larger siphuncles in some nautiloids (e.g., actinocerids, endocerids; Kröger, 2003) improved buoyancy management for these lifestyles, perhaps the magnitude of negative buoyancy could be adjusted for improved downward movement.…”

“…This scenario may have been managed by ammonoid orthocones, if their complex septa improved buoyancy regulation (i.e., chamber refilling potential; Daniel et al, 1997;Peterman et al, 2021b). If complex ammonoid sutures (Peterman et al, 2021b) or larger siphuncles in some nautiloids (e.g., actinocerids, endocerids; Kröger, 2003) improved buoyancy management for these lifestyles, perhaps the magnitude of negative buoyancy could be adjusted for improved downward movement. The low metabolic cost of upward movement from reduced hydrodynamic drag would apply to downward movement as well.…”