Comparative ultrastructure of the root system in Rhizocephalan barnacles (Crustacea: Cirripedia: Rhizocephala)

Abstract

Rhizocephalan barnacles are parasites of Crustacea. They lack even the rudiments of an alimentary canal, but infiltrate their hosts with a nutrient-absorbing system of rootlets. We review the ultrastructure of the rootlets using light microscopy, SEM, and TEM in nine species from five families, representing both suborders of the Rhizocephala: from the Kentrogonida Peltogaster paguri, P. curvatus, Peltogasterella sulcata, Cyphosaccus norvegicus (Peltogastridae); Lernaeodiscus porcellanae (Lernaeodiscidae); and Sacculina carcini (Sacculinidae); and from the Akentrogonida Clistosaccus paguri (Clistosaccidae); Chthamalophilus delagei, and Boschmaella japonica (Chthamalophilidae). With the exception of Chthamalophilus delagei, the root system of the investigated species shares numerous apomorphies at the ultrastructural level and displays at all levels specializations that maximize the surface area. The rootlets consist of a cuticle, an epidermis and a subjacent layer of axial cells that often, but not always surround, a central lumen. The rootlets are at all times enclosed in a less than 0.5 microm thick cuticle, which is never molted. The cuticle consists of an inner homogeneous layer with a slightly fibrous structure and an outer, less than 15-nm thick electron-dense layer, from which numerous microcuticular projections extend into the hemolymphatic space of the host. The microcuticular projections consist of the outer electron-dense layer and sometimes a core of the more translucent homogeneous layer. They vary among the species from being simple in Sacculina carcini to exhibiting complex branching patterns in Peltogasterella sulcata and Cyphosaccus norvegicus. Beneath the cuticle the epidermal plasma membrane is thrown into irregularly shaped projections. The epidermal cells are joined by long septate junctions and exhibit the characteristics of a transporting epithelium. Experiments with acid phosphatase revealed activity both in the epidermis and among the microcuticular projections. The projections may therefore form a domain that is important in absorption and extracellular digestion of nutrients from the host. The axial cells contain abundant endoplasmic reticulum and seem to convert absorbed carbohydrates into lipid, which is stored in large droplets. Subepidermal muscle cells cause sinuous movements of the rootlets, but it remains unknown how nutrients are transported along the rootlets towards the external reproductive body. In C. delagei the single, bladder-shaped rootlet lacks both the apical projections in the epidermis, the electron-dense cuticle layer, and the microcuticular projections. We review previous studies on the rhizocephalan root system and discuss functional and phylogenetic aspects of the morphology.

Metabolic effects of parasitization by the barnacle Polyascus plana (Cirripedia: Rhizocephala: Sacculinidae) on a grapsid host, Metopograpsus thukuhar

“…Our data show that significant levels of glycogen and triacylglycerol were accumulated in the externae. Although the mechanism of longitudinal transport that delivers the absorbed nutrients from rootlets to the externae is not precisely known, externae rely on rootlets for the supply of nutrients (Bresciani & Høeg 2001). Indeed, histological and ultrastructural characteristics of rootlets suggest that the epidermal and axial cells are sites of synthesizing and storing nutrients and energy reserves (e.g.…”

“…Indeed, histological and ultrastructural characteristics of rootlets suggest that the epidermal and axial cells are sites of synthesizing and storing nutrients and energy reserves (e.g. lipids, glycogen; Payen et al 1983, Bresciani & Høeg 2001. Thus, one of the explanations for the increased levels of glycogen and triacylglycerol in the rootlet-infiltrated hepatopancreas may be the mobilization of resources by the parasites.…”

Inorganic carbon fixation by chemosynthetic ectosymbionts and nutritional transfers to the hydrothermal vent host-shrimp Rimicaris exoculata

“…By extension, they suggest that this process might exist in many crustacean species, which would derive their nourishment at least partly from dissolved organic matter or dissolved organic carbon, as is commonly accepted for many marine invertebrates: annelids (Richards and Arme, 1982;Ahearn et al, 2000;Peppler and Ahearn, 2003), molluscs (Wright and Secomb, 1986;Wright, 1988;Wright and Pajor, 1989;De Eguileor et al, 2000) and cuticle-lined parasitic organisms such as nematodes (Fleming and Fetterer, 1984;Gordon and Burford, 1984;Masood, 1984). Arbitrarily rejected for crustaceans (Stephens, 1988) and especially decapods, this idea is surprisingly accepted without demonstration for parasitic rhizocephalan barnacles such as Sacculina carcini (Bresciani and Høeg, 2001) and for parasitic copepods (Kannupandi, 1976;Poquet et al, 1994) with a modified cuticle. It is well known, furthermore, that in pre-ecdysis, crustaceans (and other arthropods) absorb soluble molecules (for example, sugars and amino acids) from their degrading old cuticle through the new cuticle and re-utilise them for its synthesis .…”

Tissue changes in the shore crab Carcinus maenas as a result of infection by the parasitic barnacle Sacculina carcini

“…This highly specialised cirripede consists of an extensive rootlet system (termed interna) that penetrates the haemocoele of the host. Histological analysis has demonstrated rootlet penetration of the host digestive system, allowing removal, sequestration and presumably utilisation of host metabolites (Bresciani & Hoeg 2001). On maturation, the parasite forms an external egg sac (externa), which protrudes from the abdomen of chronically infected crabs.…”