Cuvierian Tubules

Cuvierian tubules are peculiar organs found in several species of holothuroids (sea cucumbers), all belonging exclusively to the family Holothuriidae. Tubules (Fig. 4A) occurring in holothuroids of the genera Bohadschia, Holothuria and Pearsonothuria are expelled as sticky white threads that function as a defence mechanism against predators (Hamel and Mercier 2000; Flammang et al. 2002). Cuvierian tubule adhesion is a typical example of instantaneous adhesion, adhesion being achieved in a matter of seconds (less than 10 s; Zahn et al. 1973).

Cuvierian tubules occur in great numbers (between 200 and 600 in H. forskali; VandenSpiegel and Jangoux 1987) in the posterior part of the body cavity of the holothuroid. Proximally they are attached to the basal part of the

Fig. 4A, B. Morphology of Cuvierian tubules of Holothuria impatiens (originals). SEM photograph of a transversely sectioned tubule (A), and longitudinal histological section showing arrangement of tissue layers (B). CTL Connective tissue layer; IE inner epithelium; L lumen; ML muscle layer; M mesothelium

Fig. 4A, B. Morphology of Cuvierian tubules of Holothuria impatiens (originals). SEM photograph of a transversely sectioned tubule (A), and longitudinal histological section showing arrangement of tissue layers (B). CTL Connective tissue layer; IE inner epithelium; L lumen; ML muscle layer; M mesothelium left respiratory tree and their distal, blind ends float freely in the coelomic fluid. When disturbed, the sea cucumber directs its aboral end toward the stimulating source and undergoes a general body contraction. The anus opens, the wall of the cloaca tears, and the free ends of a few tubules (usually 10 to 20 in H. forskali; VandenSpiegel and Jangoux 1987), together with coelomic fluid, are expelled through the tear and the anus. As water from the respiratory tree is forcefully injected into their lumen, the emitted tubules elongate up to 20 times their original length (VandenSpiegel and Jangoux 1987). Upon contact with any surface, the elongated tubules become instantly sticky. The adhesiveness of Cuvierian tubules combined with their tensile strength make them very efficient for entangling and immobilizing most potential predators (VandenSpiegel and Jangoux 1987; Hamel and Mercier 2000). Finally, the expelled tubules autotomize at their attachment point on the left respiratory tree and are left behind as the holothuroid crawls away (VandenSpiegel and Jangoux 1987). After expulsion and autotomy, Cuvierian tubules are readily regenerated. Cuvierian tubules thus constitute an efficient defensive mechanism. Their large number, sparing use and regeneration dynamics make them a formidable line of defence (Hamel and Mercier 2000; VandenSpiegel et al. 2000).

Cuvierian tubule adhesive strength on glass has been measured in seven species of sea cucumbers belonging to the genera Bohadschia, Holothuria and Pearsonothuria (Flammang et al. 2002). The mean normal tenacities observed varied from about 30 to 135 kPa. These tenacities fall within the range of adhesive strengths described for marine organisms. They are, however, among the lowest observed values (Flammang 2003).

Cuvierian tubules consist, from the inside to the outside, of an epithelium surrounding the narrow lumen, a thick connective tissue layer and a mesothe-lium lining the surface of the tubule that is exposed to the coelomic cavity (Fig. 4). The mesothelium is responsible for adhesion. In quiescent tubules, it is a pseudostratified epithelium made up of two superposed cell layers, an outer layer of peritoneocytes and an inner layer of granular cells which is highly folded along the long axis of the tubule (Fig. 4B). Granular cells are filled with densely packed membrane-bound granules enclosing a proteina-ceous material (Endean 1957; VandenSpiegel and Jangoux 1987). During elongation, the structure of the mesothelium is modified: the protective outer layer of peritoneocytes disintegrates and the granular cell layer, now unfolded, thus becomes outermost on the tubule. Granular cells empty the contents of their granules when the elongated tubule comes into contact with a surface, resulting in adhesion (VandenSpiegel and Jangoux 1987; De Moor et al. 2003).

In H. forskali, tubule print material, i.e. the adhesive left on the substratum after mechanical detachment of the tubule, is composed of 60 % protein and 40 % neutral carbohydrate, a composition that is unique among the adhesive secretions of marine invertebrates (De Moor et al. 2003). The proteinaceous nature of the adhesive material is confirmed by the observation that prote-olytic enzymes reduce the adhesive strength of Cuvierian tubules in H. forskali (Zahn et al. 1973). The amino acid compositions of the protein fraction in H. forskali, H. leucospilota, B. subrubra and P.graeffei indicate that their adhesives are closely related. All are rich in small side-chain amino acids, especially glycine, and in charged and polar amino acids (Table 1). Their compositions differ, however, from those of every other marine bioadhesive (Flammang 2003). Only a small fraction of the Cuvierian tubule adhesive can be extracted using denaturing buffers. This soluble fraction contains several proteins with different molecular masses but with closely related amino acid compositions, resembling the one of the whole adhesive (De Moor et al. 2003). As for the tube foot adhesive, charged and polar amino acids are probably involved in adhesive interactions with the substratum through hydrogen and ionic bonding (Waite 1987). Small side-chain amino acids, on the other hand, are often found in large quantities in elastomeric proteins (Tatham and Shewry 2000). These proteins are able to withstand significant deformations without rupture before returning to their original state when stress is removed (Smith et al. 1999). The composition of Cuvierian tubule adhesive has therefore all the characteristics of a strong and resistant underwater adhesive.

Table 1. Amino acid compositions of adhesive prints from the Cuvierian tubules of several species of holothuroids (values in residues per thousand)

Amino acid

Holothuria

Holothuria

Bohadschia

Pearsonothuria

forskalia

leucospilotab

subrubrab

graeffeib

HYP

0

24

8

8

ASX

78

74

64

62

THR

87

69

65

80

SER

60

42

58

58

GLX

91

122

106

124

PRO

55

74

69

63

GLY

266

267

298

254

ALA

88

115

91

85

CYS/2

14

3

9

4

VAL

38

29

35

37

MET

10

9

1

9

ILE

28

24

25

32

LEU

37

31

37

38

TYR

20

14

17

17

PHE

20

16

20

20

HIS

26

13

8

20

HLYS

0

5

12

3

LYS

31

12

29

22

ARG

50

57

46

63

a De Moor et al. (2003) b Flammang and Waite (unpubl. data)

a De Moor et al. (2003) b Flammang and Waite (unpubl. data)

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