Low Oxygen Consumption and High Body Content of Catch Connective Tissue Contribute to Low Metabolic Rate of Sea Cucumbers

Abstract

The energy consumption of echinoderms is low in comparison with that of other invertebrates. We demonstrated this by measuring the oxygen consumption rate per unit of body weight (VO2) of the sea cucumber Actinopyga mauritiana: VO2 was 1/8 that of the "standard" invertebrates. Low energy consumption in echinoderms has been attributed to their high skeletal content and to catch connective tissues (CCTs) that maintain body posture by altering their mechanical properties with little energy expenditure. The former is not applicable to holothurians, and the latter has not been proven experimentally. We postulated that the large content of dermal connective tissue, which maintaines posture economically, contributes to the low energy consumption in holothurians. Body-wall dermis occupied 53.5% of wet body weight, whereas body-wall muscles, including those of tube feet, occupied 5.1%. VO2 of the dermis in the stiff state (2.45 microl x g(-1) x h(-1)) was 1/10 that of the longitudinal body-wall muscle in contraction. the mechanical tests revealed that the stress at an imposed strain of 2% strain was 7 times greater in CCT than in muscles. These results showed that CCT could maintain posture more economically than muscles could. We concluded that the high content of connective tissue with energy-saving posture-maintenance activities contributed to the low energy consumption of holothurians.

Evaluation of the different forces brought into play during tube foot activities in sea stars

“…They were also in the range of what was observed for muscles of another sea cucumber, Actinopyga mauritiana (20kPa) (Takemae et al, 2009). The variation of the retractor muscle contraction with its extension ratio follows a typical bell-shaped length-tension curve that was identical in the two sea star species.…”

Interfibrillar stiffening of echinoderm mutable collagenous tissue demonstrated at the nanoscale

“…Specimens of the sea cucumbers (Holothuria leucospilota) were obtained from a commercial wholesaler (Marine Life) and delivered to the synchrotron SAXD beamline (in tanks of artificial sea water) a few hours before use. To prepare sea cucumber samples for the mechanical testing in different ionic solutions, we followed a protocol similar that used in previous studies of the mechanics of sea cucumber dermis (19,62). Specifically, after letting the sea cucumbers rest for 1 h in sea water, samples from the white central part of the body wall dermis (Fig.…”

“…Together with fibrillin-rich microfibrils (34) the fibrillar collagen network comprises the bulk of the extracellular matrix (ECM) of MCT. Dispersed in this ECM are clusters of juxtaligamental cells (JLCs) (12,15,19,24,28,29) (as seen from transmission electron and light microscopy), which are MCT-effector cells that are under neural control (12,15). Furthermore, it is the innervation of MCT that is a key distinction between echinoderm and vertebrate collagenous tissues (15).…”

“…Thus, MCT represents an evolutionary adaptation of collagenous tissue to change mechanical properties dynamically, whereas in other phyla collagenous tissues largely act as passive mechanical springs. The benefits of MCT also include a much lower energy expenditure (19) compared with muscle tissue and the presence of MCT is considered to have been a major factor in the evolutionary success and ecological diversity of echinoderms [reviewed in Barbaglio et al (20)]. …”

Coordination between catch connective tissue and muscles through nerves in the spine joint of the sea urchin Diadema setosum

“…It works as an effector that is responsible for posture maintenance. It stiffens to maintain the posture of animals with little energy consumption (Takemae et al, 2009;Motokawa et al, 2012); it softens to allow muscle to change the posture. It becomes very soft in autotomy and fission to allow animals to cast off their body parts (Motokawa and Tsuchi, 2003;Wilkie, 2005).…”