The fish skin is a body integument that provides diverse barriers and chemical passages as follows: i) the maintenance of water- and ion-osmotic balance (Ghioni et al. 1997), ii) a physical barrier to prevent water loss (Sayer 2005) and entry of harmful substances (Shephard 1993) or potential infective pathogens (Benhamed et al. 2014), iii) outer region for color expression (Zarnescu 2017), iv) sensory reception of physical and chemical stimuli (Bleckmann and Zelick 2009), and v) cutaneous respiration in the case of some teleosts (Urbina et al. 2014). Considering the above reports, the skin of T. brevispinis contained SFCs, SPCs, SCCs, MCs, PCs, and TBs that may enable the maintenance of a stable skin structure (Roberts and Horsley 2014), improve tolerance to somewhat turbid water with high amounts of organic materials (Han and An 2013; Park and Gwak 2019), perceive chemical differences between sour, salty, sweet, and bitter foodstuffs, and adjust to environmental changes in its habitat (Morais 2017). Tridentiger brevispinis also shows significant characteristics for cutaneous respiration (Glover et al. 2013): 1) a thick epidermis (91.6 ± 31.0 µm, 35.4 − 150.0), 2) well-developed dermal vascularization (in the operculum, dorsal-caudal region, and lateral body), and 3) some blood capillaries with dermal collagen protruding slightly into the epidermis (only in the lateral body).
Underwater teleosts or amphibious species have large cells (club cells, mucous cells, swollen cells) that play a major role in absorbing dissolved gas in water and spreading supplemental oxygen to the blood capillary or connective tissue (Park et al. 2001; Lauriano et al. 2018). Among them, Korean underwater species that inhabit stream regions where water level variation happens frequently (Kim and Park 2002) commonly have a thicker epidermis as follows: 53.2 − 111.7 µm in the freshwater goby Rhinogobius brunneus (unpublished) with numerous MCs, 97.5 − 113.5 µm in the Chinese muddy loach Misgurnus mizolepis (Park et al. 2001), 87.8 − 137.1 µm in the Korean spined loach Iksookimia koreensis (Park 2002) with numerous MCs and club cells, and 59 − 297.0 µm in the Korean eel goby Odontamblyopus lacepedii (Park et al. 2003b) with abundant MCs and swollen cells. Tridentiger brevispinis has a thicker epidermis as well that is augmented by multi-layered the SPCs and the possession of abundant MCs to promote oxygen diffusion at about 70% of the absorption rate in water (Ultsch and Gross 1979). In addition, because a reduced diffusion distance facilitates a higher diffusion velocity of supplementary oxygen, a short length between the blood capillaries and skin surface in many teleosts has been suggested to facilitate cutaneous respiration (Kim and Park 2011; Glover et al. 2013). So, the reduced diffusion distance of the lateral body in T. brevispinis may be considered the most efficient spot for cutaneous respiration among the five regions studied.
In skin vascularization, highly dermal blood vessels are a histological modification for oxygen-carbon dioxide exchange in fish skin (Potter et al. 1995; Welsch and Potter 1998). In addition, intraepidermal blood capillaries or dermal capillaries near the epidermis allow fish more efficient oxygen absorption than those in the dermis due to the reduced distance between external gas and the blood capillary (Park et al. 2003a; Park and Kim 2007). So, teleosts living in poorly oxygenated water have been reported to exhibit thicker and wider vascularization and a well-developed dermal papillae of blood capillaries positioned closer to the epidermis. In the lungfish, Neoceratodus forsteri, which is extremely well-adapted to the aerial exposure, abundant blood vessels supplying the papilla and subepidermal capillary network occurs among the fibrous layer of the dermis (Bemis and Northcutt 1992). Blood capillaries distributed just below the basement membrane were revealed in M. mizolepis (Park et al. 2001)d koreensis (Park 2002). In addition to such positions of the stratum laxum, the Korean torrent catfish Liobagrus mediadiposalis (Park et al. 2003a) and the Korean stumpy bullhead Pseudobagrus brevicorpus (Park and Kim 2007) showed blood capillaries in the middle part of the epidermis. All of these examples are best suited to survival in a hypoxic wetland or pool of freshwater prone to drying due to the Korean climate (Kim and Park 2002). Tridentiger brevispinis has fine blood capillaries just below the basement membrane protruding into the epidermis and visible only in the lateral body. With this modification, the diffusion distance between blood capillary and surface in T. brevispinis is lowest in the lateral body (88.6 ± 19.0 µm), followed by the operculum (108.3 ± 16.7 µm). This suggests that the skin region of the lateral body of T. brevispinis is the most effective spot for cutaneous respiration. Moreover, well-developed vascularization and blood capillaries near the epidermis in T. brevispinis is a skin modification suitable for obtaining dissolved gas under hypoxic water conditions.
Consequently, T. brevispinis exhibits a thicker epidermis, a well-developed vascularization, a few blood capillaries protruding into the epidermis, and reduced diffusion distance in the lateral body, all of which are related to effective cutaneous respiration for survival in a hypoxic habitat during the dry season.