Postembryonic development and differentiation of the midgut in the freshwater shrimp Neocaridina davidi (Crustacea, Malacostraca, Decapoda) larvae

Abstract

Neocaridina davidi is a freshwater shrimp that originates from Taiwan and is commonly bred all over the word. Like all decapods, which develop indirectly, this species has pelagic larvae that may differ entirely in their morphology and habits from adult specimens. To fill a gap of knowledge about the developmental biology of freshwater shrimps we decided to document the 3D-localization of the midgut inside the body cavity of larval stages of N. davidi using X-ray microtomography, and to describe all structural and ultrastructural changes of the midgut epithelium (intestine and hepatopancreas) which occur during postembryonic development of N. davidi using light and transmission electron microscopy. We laid emphasis on stem cell functioning and cell death processes connected with differentiation. Our study revealed that while the intestine in both larval stages of N. davidi has the form of a fully developed organ, which resembles that of adult specimens, the hepatopancreas undergoes elongation and differentiation. E-cells, which are midgut stem cells, due to their proliferation and differentiation are responsible for the above-mentioned processes. Our study revealed that apoptosis is a common process in both larval stages of N. davidi in the intestine and proximal region of the hepatopancreas. In zoea III, autophagy as a survival factor is activated in order to protect cells against their death. However, when there are too many autophagic structures in epithelial cells, necrosis as passive cell death is activated. The presence of all types of cell death in the midgut in the zoea III stage confirms that this part of the digestive tract is fully developed and functional. Here, we present the first description of apoptosis, autophagy and necrosis in the digestive system of larval stages of Malacostraca and present the first description of their hepatopancreas elongation and differentiation due to midgut stem cell functioning.

Morphological description of the midgut tract and midgut–hindgut junction in the larvae of the spider crab Maja brachydactyla Balss, 1922 (Malacostraca: Decapoda)

“…Similarly as observed in this study, the midgut tract is a short tube in other brachyurans (Spitzner et al, 2018), and anomurans (Williams, 1944;Abrunhosa and Kittaka, 1997). On the contrary, it is a large tube reaching the sixth abdominal segment in clawed lobsters (Factor, 1981), and caridean shrimps (Tziouveli et al, 2011;Sonakowska-Czajka et al, 2021).…”

“…The secretory activity was identified as merocrine, consisting on releasing the electron-dense content of the vesicles located in the cell apex. Similarly, electron-dense vesicles sharing a similar location were also identified on the main epithelial cells of the midgut tract of adults of the dungeness crabs Metacarcinus magister and the clawed lobster Homarus americanus (Mykles, 1979), in adults of the ridgeback prawns Sicyonia ingentis (Martins et al, 2006); as well in the larvae of the freshwater shrimp Neocaridina davidi (Sonakowska-Czajka et al, 2021).…”

“…The midgut tract of the larval stages of the common spider crab M. brachydactyla is a short and simple tube positioned anteriorly, between the stomach and the hindgut tract, as observed in adults from the same species (Castejón et al, 2021). The midgut tract as a simple tube, internally lined by a simple columnar epithelium, is shared by the larvae of several decapod taxa, including other brachyuran species (Jantrarotai and Sawanyatiputi, 2005;Spitzner et al, 2018), anomurans (Williams, 1944;Abrunhosa and Kittaka, 1997), astacideans (Factor, 1981), achelatans (Mikami et al, 1994), and carideans (Tziouveli et al, 2011;Sonakowska-Czajka et al, 2021). Major differences were found on the relative length of the midgut tract.…”

“…However, in the larval stages the majority of the studies focused on the whole digestive system so the midgut tract received little attention (Schlegel, 1911;Talbot et al, 1972;Lovett and Felder, 1989;Mikami et al, 1994;Abrunhosa and Kittaka, 1997;Jantrarotai and Sawanyatiputi, 2005;Tziouveli et al, 2011). Recently, the midgut tract was described in the larvae of the freshwater shrimp Neocaridina davidi (Sonakowska-Czajka et al, 2021).…”

Cytology, function and dynamics of stem and progenitor cells in decapod crustaceans

“…Using the mitosis marker anti‐phosphohistone H3, Sonakowska‐Czajka et al . (2021) revealed numerous proliferating cells in the anterior section of the midgut of larval freshwater shrimp Neocaridina davidi but not in the other parts of the midgut tube.…”