Push or Pull? The light‐weight architecture of the Daphnia pulex carapace is adapted to withstand tension, not compression

Abstract

Daphnia (Crustacea, Cladocera) are well known for their ability to form morphological adaptations to defend against predators. In addition to spines and helmets, the carapace itself is a protective structure encapsulating the main body, but not the head. It is formed by a double layer of the integument interconnected by small pillars and hemolymphatic space in between. A second function of the carapace is respiration, which is performed through its proximal integument. The interconnecting pillars were previously described as providing higher mechanical stability against compressive forces. Following this hypothesis, we analyzed the carapace structure of D. pulex using histochemistry in combination with light and electron microscopy. We found the distal integument of the carapace to be significantly thicker than the proximal. The pillars appear fibrous with slim waists and broad, sometimes branched bases where they meet the integument layers. The fibrous structure and the slim-waisted shape of the pillars indicate a high capacity for withstanding tensile rather than compressive forces. In conclusion they are more ligaments than pillars. Therefore, we measured the hemolymphatic gauge pressure in D. longicephala and indeed found the hemocoel to have a pressure above ambient. Our results offer a new mechanistic explanation of the high rigidity of the daphniid carapace, which is probably the result of a light-weight construction consisting of two integuments bound together by ligaments and inflated by a hydrostatic hyper-pressure in the hemocoel. J. Morphol. 277:1320-1328, 2016. © 2016 Wiley Periodicals, Inc.

Biomechanical analysis of prey capture in the carnivorous Southern bladderwort (Utricularia australis)

“…Indeed, in CE 08 where such temporary blockage can be noted, the duration of suction (i.e., the trapping duration) is even shortest (5.2 ms) among all CEs. It remains to be investigated if also a potential deformation of the C. dubia carapace during passage through the trap entrance region plays a role (see Kruppert and colleagues 28 for a biomechanical analysis of the Daphnia pulex carapace). It is supposable (but not observed in this study) that C. dubia individuals exist which are too big to get sucked into the trap, and that traps at early stages of deflation (with low underpressure values inside) cannot cope with prey blocking the entrances.…”

Carapace epithelia are rich in large filamentous actin bundles in Daphnia magna, Daphnia pulex, and Sida crystallina (Crustacea: Cladocera)

“…Ultrastructural observations of the Daphnia carapace integument have revealed fibers in the pillars that extend through the epithelia and anchor in the cuticle. Based on thickness, these fibers were predicted to be one of two cytoskeletal protein filaments: microtubules in Daphnia magna (Halcrow 1976), or intermediate filaments in D. pulex (Kruppert et al 2016). Although the pillars may contain these filaments, in the present study we show that the carapaces of three species of Cladocera, D. magna, D. pulex, and Sida crystallina, are rich in large F-actin bundles.…”

“…4,5), and within the pillars extends radially out from central foci into the deep and superficial epithelia (Figs. We present a model of the F-actin bundle structures in the pillars which draws from previously published ultrastructural observations (Halcrow 1976;Kruppert et al 2016), and incorporates our own observations that the filaments are arranged in bundles and extend into, but do not appear to completely transverse, the pillars (Fig. This arrangement is characteristic of stress fibers, which are F-actin bundles that are typically anchored on one end to another cell, or the extracellular matrix, at focal adhesions (for a review see Pellegrin & Mellor 2007).…”

“…1, March 2018 epithelium of land crab (Gecarcinus lateralis) and lobster (Homarus americanus) species, and the proteins were also present in isolated pockets in the cuticle (Mykles et al 2000). Ultrastructural analysis of the carapace of Daphnia species revealed filaments in the cuticle and pillars that, based on their observed size (15-36 nm and 15 nm, respectively), were predicted to be microtubules and intermediate filaments (Halcrow 1976;Kruppert et al 2016). Our results cannot rule out the presence of microtubules or intermediate filaments in these structures, but clearly demonstrate that F-actin is abundant in Cladocera pillars and extends radially into the deep and superficial epithelium (Figs.…”

“…Two roles have been proposed for the pillars in Daphnia, one in which the pillars resist compressive forces and can be induced to increase in diameter in the presence of predator kairomones (Laforsch et al 2004;Rabus et al 2013), and one in which the pillars serve a tensile role that antagonizes hydrostatic pressure in the hemolymphatic chamber (Kruppert et al 2016). Ultrastructural observations of the Daphnia carapace integument have revealed fibers in the pillars that extend through the epithelia and anchor in the cuticle.…”