Conflict and Compromise: Using Reversible Remodeling to Manage Competing Physiological Demands at the Fish Gill

Abstract

The structural features of the fish gill necessary for oxygen uptake also favor undesirable, passive movements of ions and water. Reversible gill remodeling is one solution to this conflict. Cell masses that limit functional surface area are lost when oxygen availability decreases in hypoxia or oxygen demand increases with exercise or high temperature. However, much remains to be learned about how widespread reversible gill remodeling is among fish species, and how and why it occurs.

Morphopathology and gill recovery of Atlantic salmon during the parasitic detachment of Margaritifera margaritifera

“…In particular, apoptosis, phagocytosis and epithelial shedding mutually interplay to remove the cell excess, limit the detrimental effects of inflammation (AnvariFar et al., 2017) and preserve the branchial architecture during healing (Daoust & Ferguson, 1986). The presence of apoptotic hallmarks related to the more constricted peduncles and the remaining lesions after the detachment peak may indicate a regression of the hyperplastic tissue, as it was suggested during other gill proliferative diseases (Sales et al., 2017; Speare et al., 1999) and reversible gill remodelling (Gilmour & Perry, 2018; Sollid et al., 2003). On the contrary, the absence of apoptosis during the parasitism could be explained as a beneficial mechanism both to the parasite by preserving the hyperplastic covering around the larvae (Bienvenu et al., 2010) and to the host by minimizing the gill surface area exposed to the external environment (Nilsson, 2007).…”

What Is Gill Health and What Is Its Role in Marine Finfish Aquaculture in the Face of a Changing Climate?

“…Some species display a remarkable capacity to remodel key morphological traits that influence gill function, such as gill surface area and gas diffusion distance (i.e., the distance between water and blood sinus, Figure 2). A large gill surface area paired with a small gas diffusion distance is generally associated with enhanced diffusion of gas and ions across the branchial epithelium (Bindon et al, 1994;Lappivaara et al, 1995, reviewed in Sakuragui et al, 2003Gonzalez, 2011;Gilmour and Perry, 2018). Crucian carp (Carassius carassius), in particular, are well known to use the growth of epithelial cells to modify their gill surface area and gas diffusion distance to regulate gill function (Sollid et al, 2005).…”

“…Crucian carp (Carassius carassius), in particular, are well known to use the growth of epithelial cells to modify their gill surface area and gas diffusion distance to regulate gill function (Sollid et al, 2005). At low temperatures (10-20 • C), crucian carp grow an "inter-lamellar cell mass" in between their lamellae, leading to the fusion of adjacent lamellae, the reduction of gill surface area, and an increase in gas diffusion distance (Sollid et al, 2005;Gilmour and Perry, 2018). This reduction in surface area reduces diffusive ion loss across the branchial epithelium and allows crucian carp to reduce energetic costs associated with osmoregulation at times when oxygen demand is low (Sollid et al, 2005;Gilmour and Perry, 2018).…”

“…At low temperatures (10-20 • C), crucian carp grow an "inter-lamellar cell mass" in between their lamellae, leading to the fusion of adjacent lamellae, the reduction of gill surface area, and an increase in gas diffusion distance (Sollid et al, 2005;Gilmour and Perry, 2018). This reduction in surface area reduces diffusive ion loss across the branchial epithelium and allows crucian carp to reduce energetic costs associated with osmoregulation at times when oxygen demand is low (Sollid et al, 2005;Gilmour and Perry, 2018). This process can be reversed to where the inter-lamellar cell mass is rapidly shed in response to rising temperatures in the summer (>25 • C) thereby increasing gill surface area by up to 7.5-fold and enhancing oxygen uptake (Sollid et al, 2005).…”

“…The majority of studies, however, have focused on describing morphological changes observed in response to pollution (including toxins, heavy metals, and suspended particulate matter), parasites, and pathogens (e.g., Mueller et al, 1991;Ahmed et al, 2013;Zarha and Mobarak, 2015;Marcon et al, 2016), and little is known about whether gill remodeling may also occur in response to rising temperatures in these species. It is important to note, however, that modest changes in gill surface area or gas diffusion distances may not directly translate into changes in oxygen uptake and carbon dioxide excretion rates or other gill functions as these processes are influenced by numerous other factors as well (Robertson et al, 2015;Gilmour and Perry, 2018, see also Cumming and Herbert, 2016;Esbaugh et al, 2016;Hess et al, 2017). Findings in coral reef fish indicate that fish living at low latitudes and high average summer temperatures may generally have little capacity for gill remodeling in response to rising temperatures as many species already exhibit small gas diffusion distances, leaving little room for further decreases (Bowden et al, 2014).…”