Permanently Fused Setules Create Unusual Folding Fans Used for Swimming in Cyprid Larvae of Barnacles

Lamont, Eleanor I.; Emlet, Richard B.

doi:10.1086/700084

Cited by 7 publications

(5 citation statements)

References 29 publications

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“…Acartia's webbed thoracopod fan is strikingly similar to traits recently discovered in barnacle cyprids (6). Despite differences in anatomy, the apparent functions of setular linkage in swimming are the same.…”

Section: And Video 3)supporting

confidence: 63%

“…To confirm that the mesh represents physical linkage amongst setules, thoracopods were removed from anesthetized animals at or near the base with fine forceps, then spread on a slide in a small drop of water by application of a coverslip, as previously done with barnacle cyprids (6). In such preps, we could demonstrate linkage amongst all thoracopod setae in Acartia (Fig.…”

mentioning

confidence: 79%

“…This begs the question of how widespread a trait it might be. Lamont and Emlet (6) described it in all barnacle cyprids (including acrothoracicans, rhizocephalans, and thoracicans; no information is available for basal thecostracans), but not in nauplii. We have not detected linkage in any of several decapod zoeas, other small pelagic decapods, or harpactacoid copepods.…”

Section: And Video 3)mentioning

confidence: 99%

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Direct observation of the setular web that fuses thoracopodal setae of a calanoid copepod into a collapsible fan

Dassow

Emlet²

2019

Preprint

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Copepods are numerically dominant planktonic grazers throughout the waters of Earth, preyed upon in turn by a wide diversity of pelagic animals (1,2). Their feeding and swimming performance thus has global importance to aquatic food webs and oceanic carbon flux. These crustaceans swim and feed using cuticle-covered, segmented, muscular appendages whose reach is extended greatly by setae, extracellular chitinous extensions with diverse structure and function (3). Plumose setae, with subsidiary setules arranged like barbs on a feather, have well-documented roles in generating feeding and swimming currents (4,5). Recent work showed that plumose setae of barnacle cyprid thoracopods are permanently linked by setules into a single fan that opens and closes as one sheet during high-speed swimming (6).Intersetular linkage across cyprid thoracopods may greatly decrease leakage between extended setae, ensure even spread of setae within the fan, and promote ordered collapse of the fan to avoid entanglement of adjacent appendages. Here we demonstrate similar setular webbing amongst thoracopod setae in the calanoid copepod Acartia sp. High-speed video directly documents the existence of such links, and reveals that individuals experience apparently-irreparable degradation of the setal array due to de-linkage, with likely consequences for swimming performance.We caught calanoid copepods and copepodites in plankton samples from the Charleston marina, Oregon, USA (43˚ 20.682'N, 124˚ 19.236'W). Acartia sp. were most prevalent, and were first concentrated by attraction to light, then selected individually after anaesthetization in MgCl2 or tricaine. To record escape swimming, one or several animals were introduced into 0.3-0.5 ml clean natural seawater in a coverslip-bottomed 35 mm Petri dish (sometimes seeded with Nannochloropsis as a neutral, non-motile, non-aggregating particulate tracer), then covered with another coverslip supported by

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confidence: 63%

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confidence: 79%

Section: And Video 3)mentioning

confidence: 99%

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Direct observation of the setular web that fuses thoracopodal setae of a calanoid copepod into a collapsible fan

Dassow

Emlet²

2019

Preprint

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“…The structure and orientation of the appendices internae coupled with potential recoil or adhesive forces of the retinacula can serve as a passive mechanism in transition into the recovery stroke where less or little energy is required for pleopod retraction. This has also been proposed for a similar structure (fused setules) in barnacle larvae ( Lamont and Emlet 2018 ). Future studies are needed to determine the strength of retinacula and the function of detaching pleopod pairs in mantis shrimp locomotion.…”

Section: Discussionmentioning

confidence: 65%

Mantis Shrimp Locomotion: Coordination and Variation of Hybrid Metachronal Swimming

Hanson

Ray

Santhanakrishnan

et al. 2023

Integrative Organismal Biology

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Across countless marine invertebrates, coordination of closely spaced swimming appendages is key to producing diverse locomotory behaviors. Using a widespread mechanism termed hybrid metachronal propulsion, mantis shrimp swim by moving five paddle-like pleopods along their abdomen in a posterior to anterior sequence during the power stroke and a near-synchronous motion during the recovery stroke. Despite the ubiquity of this mechanism, it is not clear how hybrid metachronal swimmers coordinate and modify individual appendage movements to achieve a range of swimming capabilities. Using high speed imaging, we measured pleopod kinematics of mantis shrimp (Neogonodactylus bredini) while they performed two swimming behaviors: burst swimming and taking off from the substrate. By tracking each of the five pleopods, we tested how stroke kinematics vary across swimming speeds and the two swimming behaviors. We found that mantis shrimp achieve faster swimming speeds through a combination of higher beat frequencies, smaller stroke durations, and partially via larger stroke angles. The five pleopods exhibit non-uniform kinematics that contribute to the coordination and forward propulsion of the whole system. Micro-hook structures (retinacula) connect each of the five pleopod pairs and differ in their attachment across pleopods—possibly contributing to passive kinematic control. We compare our findings in N. bredini to previous studies to identify commonalities across hybrid metachronal swimmers at high Reynolds numbers and centimeter scales. Through our large experimental dataset and by tracking each pleopod's movements, our study reveals key parameters by which mantis shrimp adjust and control their swimming, yielding diverse locomotor abilities.

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“…Cyprids, therefore, need to meet strong swimming requirements. Indeed, recent observations of tethered barnacle cyprids of Balanus glandula highlighted specializations for swimming: the radial movement of the cyprid's thoracopods during the power stroke and the fused setules between these appendages [20]. While tethering allows for an excellent view of appendage movement, it prevents one from making a direct link between swimming kinematics to change in swimming performance and may introduce hydrodynamics artefacts [21,22].…”

Section: Introductionmentioning

confidence: 99%

Swimming kinematics and hydrodynamics of barnacle larvae throughout development

Wong

Chan

2020

Proc. R. Soc. B.

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Changes in size strongly influence organisms' ecological performances. For aquatic organisms, they can transition from viscosity- to inertia-dominated fluid regimes as they grow. Such transitions are often associated with changes in morphology, swimming speed and kinematics. Barnacles do not fit into this norm as they have two morphologically distinct planktonic larval phases that swim differently but are of comparable sizes and operate in the same fluid regime (Reynolds number 10 0 –10 1 ). We quantified the hydrodynamics of the rocky intertidal stalked barnacle Capitulum mitella from the nauplius II to cyprid stage and examined how kinematics and size increases affect its swimming performance. Cyprids beat their appendages in a metachronal wave to swim faster, more smoothly, and with less backwards slip per beat cycle than did all naupliar stages. Micro-particle image velocimetry showed that cyprids generated trailing viscous vortex rings that pushed water backwards for propulsion, contrary to the nauplii's forward suction current for particle capture. Our observations highlight that zooplankton swimming performance can shift via morphological and kinematic modifications without a significant size increase. The divergence in ecological functions through ontogeny in barnacles and the removal of feeding requirement likely contributed to the evolution of the specialized, taxonomically unique cyprid phase.

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Permanently Fused Setules Create Unusual Folding Fans Used for Swimming in Cyprid Larvae of Barnacles

Cited by 7 publications

References 29 publications

Direct observation of the setular web that fuses thoracopodal setae of a calanoid copepod into a collapsible fan

Direct observation of the setular web that fuses thoracopodal setae of a calanoid copepod into a collapsible fan

Mantis Shrimp Locomotion: Coordination and Variation of Hybrid Metachronal Swimming

Swimming kinematics and hydrodynamics of barnacle larvae throughout development

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