Morphology of reproductive accessory glands in female Sepia pharaonis (Cephalopoda: Sepiidae) sheds light on egg encapsulation

Abstract

The pharaoh cuttlefish, Sepia pharaonis, is an important cephalopod fishery species in southeastern Asia, with understudied reproductive physiology. The present study aimed to investigate the cellular characteristics of epithelial cells found in the nidamental glands (NGs) and accessory NGs (ANGs), as well as the structural connections between these two glands in mature female S. pharaonis. A histological analysis revealed two types of epithelial cells in NGs: Alcian blue‐positive, PAS‐negative mucosubstance‐secreting cells and eosinophilic, PAS‐positive granule‐secreting cells. Using transmission electron microscopy, three types of epithelial cells were identified: cells with electron‐dense granules, cells with electron‐lucent granules, and cells with both cilia and microvilli in the apex. Mature ANGs contain an abundance of tubular units composed of epithelial cells resting on a thin layer of basal lamina. Innervated muscle cells are tightly adhered to the basal lamina. In addition, we observed epithelial canalization of ANG tubules penetrating through the connective tissue linking NGs and the walls of the tubules in ANGs, which allows the contents of the ANG tubules to be transported to the NGs. Our results suggest that ANGs participate in the encapsulation of the ova via the same pathway as NGs, which provides an important basis for future studies on the mechanism of protection provided by NGs and ANGs during embryonic development in S. pharaonis.

Histological analysis of oogenesis and ovarian development of the pharaoh cuttlefish, Sepia pharaonis

“…The epithelial cells of the lumen of the accessory nidamental gland in S. pharaonis showed the uneven distribution of cilium. This was similar to the morphology described in the studies of Nair et al (2005) and Huang et al (2018) on the accessory nidamental gland. In addition, studies have found that the cephalopod accessory nidamental gland contains symbiotic bacteria.…”

“…Based on criteria used in fish descriptions, ovarian development and oogenesis have been characterized in a few cephalopod species, including Loligo vulgaris L amarck 1798 (Melo & Sauer, 1998), Octopus vulgaris C uvier 1797 (Di Cosmo et al, 2001), Octopus maya Voss & Solís 1966 (Avila‐Poveda et al, 2009), Amphioctopus fangsiao ( d'Orbigny [in A. Férussac & d'Orbigny], 1839–1841) (= Octopus ocellatus ) (Wang et al, 2015), Sepiella inermis (= maindroni ) ( Van Hasselt [in Férussac & d'Orbigny ] 1835) (Jiang et al, 2007), and Sepia esculenta H oyle 1885 (Yin et al, 2018). However, in S. pharaonis , the structure of the accessory nidamental gland is the only aspect of the reproductive system to have been studied (Huang et al, 2018; Nair et al, 2005).…”

“…Individuals can reach a weight of ≤2.2 kg when raised in cement ponds, and thus has become a commercially cultured cephalopod in coastal southeast China (Jiang, Peng, et al, 2019). Recent reports have focused on the development of fertilized eggs and embryos (Lee et al, 2016; Peng et al, 2017), environmental factors for the growth of juveniles (Jiang, Chen, et al, 2022), tissue nutrients, and development of the reproductive system (Gao et al, 2014; Huang et al, 2018; Nair et al, 2005). Given the difficulties in raising S. pharaonis in large‐scale aquaculture, our research group has conducted in‐depth research on the optimal food supply for hatchlings (Peng et al, 2015), the diet conversion strategy in the weaning period (Jiang et al, 2020, 2021), inking physiology (Jiang, Ye, et al, 2022; Jiang, Zhao, et al, 2019), nutritional requirements, and optimizing ecological factors for each growth stage (Jiang, Peng, et al, 2019).…”

The Characteristics and Expression Profile of Transferrin in the Accessory Nidamental Gland of the Bigfin Reef Squid during Bacteria Transmission

“…Antimicrobial activity is found in extracts of the ANG in squid 4,5 and cuttlefish 6 , which is interesting in light of the highly similar bacterial composition of the egg jelly coat and ANG in these cephalopods 7,8 . The ANG may play an important role in bacterial delivery from the parent to the egg capsule by preventing contamination from microorganisms in the benthic environment 9 . In squid and cuttlefish, at least some symbiotic bacteria are delivered from the marine environment and selected by the host 10 .…”

Transcriptomic profile of symbiotic accessory nidamental gland during female maturation in bigfin reef squid

“…Our previous study further suggested that the environment affects the microbial compositions of individuals, whereas maturity levels exert progressive effects on microbial dynamics over time (Yang et al, 2021). These host-selected bacteria are transmitted to the egg jelly coat in some squid and cuttlefish (Kerwin and Nyholm, 2017;Huang et al, 2018). Suppression of the bacteria deposited on the eggs by antibiotic treatment led to susceptibility to heavy biofouling and very low hatching rates compared with untreated eggs in Hawaiian bobtail squid (Kerwin et al, 2019).…”