Ultrastructural comparison of the midgut epithelia of fleas with different feeding behavior patterns (Xenopsylla cheopis, Echidnophaga gallinacea, Tunga penetrans, Siphonaptera, Pulicidae)

Abstract

This morphological study describes the ultrastructure of the midgut of three flea species, including temporary parasitic fleas (both sexes of Xenopsylla cheopis, males and immature females of Echidnophaga gallinacea and Tunga penetrans) and stationary parasitic fleas (mature females of E. gallinacea and T. penetrans). (1) Three cell types (a,b,c) constitute the midgut epithelium, each appearing in a characteristic and constant frequency along the whole midgut, a) The functional digestive cells form the main part of the epithelium as one layer of cylindric cells. Nuclear volume and nucleus/cytoplasm ratio have been estimated (with morphometric methods) to be the same in both sexes of E. gallinacea and T. penetrans. b) Some single regenerative cells or nests, containing 5-10 cells per section plane, lay at the base of the epithelium (2-3 cells or nests per cross section of a midgut). c) Secretory cells are characterized by their opaque cytoplasm which contains electron-dense vesicles. They have few microvilli and no basal labyrinth and are placed between digestive cells only as single cells (1-2 per cross section of a midgut). (2) After the first bloodmeal some ultrastructural changes occur in the midgut of all fleas. These changes are interpreted as a structural reflection of metabolic processes such as secretion of digestive enzymes, resorption, storage and transport of digested nutrients, and synthesis of digestive enzymes. (3) More conspicious changes occur in the midgut of the stationary parasitic and maturing females of E. gallinacea and T. penetrans. The nuclear volumes of the digestive cells reach the two-fold and eight-fold value, respectively. The nucleus/cytoplasm ratio decreases by half. The corresponding cytoplasmic growth of each cell is reflected in an enlargement of the whole midgut. The digestive cells form long apical cell extensions. The nucleus, basal labyrinth, rer, and golgi complex all change their morphology, and this can be interpreted as the result of a higher level of metabolic activity than during the first bloodmeal. (4) The midgut of the oviparous female of T. penetrans undergoes a process of compensatory hypertrophy which consists in the cellular hypertrophy of each digestive cell and in an extensive proliferation of the regenerative cells. A unique structure, called 'nuclear halo' appears within the process of cellular hypertrophy. This structure consists of a layer of 70-100 A thick filaments along the periphery of the nucleus. The nuclear halo contains few ribosomes and is screened from the cytoplasm by an rer cisterna. The filaments may contain RNA molecules which are on their way to the cytoplasm. It has been demonstrated that the structure of the midgut epithelium is influenced by the nutritive and parasitic behavior of the flea. The stationary and oviparous E. gallinacea and T. penetrans reveal an extensive and irreversible change of their midgut epithelium.