Research Article: Arms of larval seastars of Pisaster ochraceus provide versatility in muscular and ciliary swimming

Date Published: March 14, 2019

Publisher: Public Library of Science

Author(s): Sophie B. George, Richard R. Strathmann, Chung-Ping Lin.

http://doi.org/10.1371/journal.pone.0213803

Abstract

Larval swimming with cilia, unaided by muscles, is the presumed ancestral condition for echinoderms, but use of muscles in swimming has evolved several times. Ciliation and musculature of the arms of brachiolaria-stage larvae in the family Asteriidae provide unusual versatility in the use of muscles in swimming. The muscles affect swimming in two different ways. (1) Contraction of muscles moves the arms, propelling the larva. (2) Contraction of muscles changes orientation of the arms, thereby changing direction of ciliary currents and direction of swimming. New observations of the brachiolaria of the asteriid seastar Pisaster ochraceus demonstrate more versatility in both of these uses of muscles than had been previously described: the posterolateral arms stroke in more ways to propel the larva forward and to change the direction of swimming, and more pairs of the arms point ciliary currents in more directions for changes in direction of swimming. Morphology of brachiolariae suggests that these uses of muscles in swimming evolved before divergence of the families Stichasteridae and Asteriidae within forcipulate asteroids. This versatile use of muscles for swimming, both alone and in combination with ciliary currents, further distinguishes the swimming of these brachiolariae from swimming by larvae of other echinoderms and larvae of acorn worms in the sister phylum Hemichordata.

Partial Text

Ciliary swimming without the aid of muscles is the general and presumably ancestral case for the feeding larvae of echinoderms [1]. Use of muscles in larval swimming, known to occur in the seastar family Asteriidae, is striking because use of muscles in larval swimming evolved rarely in the phylum Echinodermata. Muscles of echinoderm larvae supplement swimming in two ways. One way is for muscles to create a current by moving part of the larval body. Another way is for muscles to redirect ciliary currents by changing the form of the larval body.

Swimming of larvae of asteroids and other echinoderms changes during development and differs with morphology [18,19]. The arms of brachiolariae of Pisaster ochraceus confer capabilities not present in the preceding bipinnaria stage or in the brachiolariae of other orders of asteroids. Advanced brachiolaria larvae of P. ochraceus have a suite of complex, precise, and well-coordinated swimming behaviors that aid directionality of swimming. Speed may be enhanced by currents generated by the arms as well as by use of arms in maintaining a direction. These larvae can turn and switch directions in a few seconds by strokes of the posterolateral arms or by pointing ciliary currents with either the posterolateral arms alone or with the postoral and posterodorsal arms in combination. The posterolateral arms can sweep through the water synchronously or asynchronously to complete turns in either the dorsal or ventral direction. The side-to-side movement of the very long posterolateral arms adds to ciliary beat as a means of forward swimming. The posterolateral arms can grow to be almost as long as the rest of the larval body. The larvae can also change direction by pointing the arms in different combinations to point the ciliary currents along the arms.

 

Source:

http://doi.org/10.1371/journal.pone.0213803

 

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