Evolution of Feeding Shapes Swimming Kinematics of Barnacle Naupliar Larvae: A Comparison between Trophic Modes.

J Y Wong,B K K Chan,K Y K Chan

doi:10.1093/iob/obaa011

Abstract

SynopsisA central goal in evolutionary biology is connecting morphological features with ecological functions. For marine invertebrate larvae, appendage movement determines locomotion, feeding, and predator avoidance ability. Barnacle larvae are morphologically diverse, and the morphology of non-feeding lecithotrophic nauplii are distinct from those that are planktotrophic. Lecithotrophic larvae have a more globular body shape and simplified appendages when compared with planktotrophs. However, little is known about whether and how such morphological changes affect kinematics, hydrodynamics, and ecological functions. Here, we compared the nauplii kinematics and hydrodynamics of a lecithotrophic Rhizocephalan species, Polyascus planus, against that of the planktotrophic nauplii of an intertidal barnacle, Tetraclita japonica. High-speed, micro-particle image velocimetry analysis showed that the Polyascus nauplii swam faster and had higher amplitude and more synchronous appendage beating than the Tetraclita nauplii. This fast swimming was accompanied by a faster attenuation of induced flow with distance, suggesting reduced predation risk. Tetraclita nauplii had more efficient per beat cycles with less backward displacement during the recovery stroke. This “anchoring effect” resulted from the anti-phase beating of appendages. This movement, together with a high-drag body form, likely helps direct the suction flow toward the ventral food capturing area. In sum, the tradeoff between swimming speed and predation risks may have been an important factor in the evolution of the observed larval forms.

Highlights

Nauplius is a homologous developmental stage shared by all crustaceans, and the free-living form of nauplius has persisted in most lineages (Williams 1994b) but see Scholtz (2000)
They are distinguished from other crustacean nauplii by the presence of a pair of frontal horns, which are unique for barnacles (Høeg and Møller 2006)
The swimming velocity difference is best explained by the large difference in beat frequency between the species. Polyascus nauplii beat their appendages at frequencies approximately three times that of Tetraclita nauplii (Table 1), which translates into higher angular speeds in all pairs of appendages (Table 1)

Summary

Introduction

Nauplius is a homologous developmental stage shared by all crustaceans, and the free-living form of nauplius has persisted in most lineages (Williams 1994b) but see Scholtz (2000). A striking example of diversity in naupliar forms can be found among barnacle (Cirripedia) nauplii. They are distinguished from other crustacean nauplii by the presence of a pair of frontal horns, which are unique for barnacles (Høeg and Møller 2006). The presence of frontal horns or the less streamlined overall naupliar forms of barnacles was thought to be costly for locomotion, but may be beneficial for suspension feeding (Moyse 1984; Emlet and Strathman 1985). Comparative study on barnacle naupliar forms supports this functional tradeoff: common planktotrophic nauplii have relatively longer frontal horns and tail spines than lecithotrophic nauplii that do not feed (Wong et al 2018). Without empirical data on how lecithotrophic nauplii perform, inference on such a morphology–function link still lacks mechanistic insight (Koehl 1996)

Methods

Results

Conclusion