Cardiovascular function, compliance, and connective tissue remodeling in the turtle,Trachemys scripta, following thermal acclimation

Abstract

Low temperature directly alters cardiovascular physiology in freshwater turtles, causing bradycardia, arterial hypotension, and a reduction in systemic blood pressure. At the same time, blood viscosity and systemic resistance increase, as does sensitivity to cardiac preload (e.g., via the Frank-Starling response). However, the long-term effects of these seasonal responses on the cardiovascular system are unclear. We acclimated red-eared slider turtles to a control temperature (25°C) or to chronic cold (5°C). To differentiate the direct effects of temperature from a cold-induced remodeling response, all measurements were conducted at the control temperature (25°C). In anesthetized turtles, cold acclimation reduced systemic resistance by 1.8-fold and increased systemic blood flow by 1.4-fold, resulting in a 2.3-fold higher right to left (R-L; net systemic) cardiac shunt flow and a 1.8-fold greater shunt fraction. Following a volume load by bolus injection of saline (calculated to increase stroke volume by 5-fold, ∼2.2% of total blood volume), systemic resistance was reduced while pulmonary blood flow and systemic pressure increased. An increased systemic blood flow meant the R-L cardiac shunt was further pronounced. In the isolated ventricle, passive stiffness was increased following cold acclimation with 4.2-fold greater collagen deposition in the myocardium. Histological sections of the major outflow arteries revealed a 1.4-fold higher elastin content in cold-acclimated animals. These results suggest that cold acclimation alters cardiac shunting patterns with an increased R-L shunt flow, achieved through reducing systemic resistance and increasing systemic blood flow. Furthermore, our data suggests that cold-induced cardiac remodeling may reduce the stress of high cardiac preload by increasing compliance of the vasculature and decreasing compliance of the ventricle. Together, these responses could compensate for reduced systolic function at low temperatures in the slider turtle.

Embryonic hypoxia programmes postprandial cardiovascular function in adult common snapping turtles (Chelydra serpentina)

“…Prior studies have also reported a net systemic blood flow pattern [i.e. right-left (R-L) shunt] in T. scripta (Wang and Hicks, 1996a;Hicks and Wang, 1998;Crossley et al, 2000;Krosniunas and Hicks, 2003;Galli et al, 2004;Keen et al, 2016). However, we are among the first to assess intracardiac shunting in the snapping turtle (Steggerda and Essex, 1957), and it is unclear whether the direction of shunting is similarly variable in this species.…”

Embryonic Temperature Programs Phenotype in Reptiles

“…Together, these changes preserve whole organism performance across a broader range of temperatures than would otherwise be possible. Similar effects of cold acclimation on the cardiovascular system are observed in turtles (Risher and Claussen, 1987;Keen et al, 2016). Heat acclimation is also a well-established phenomenon in which exposure to elevated temperatures increases the critical thermal maximum of a broad range of organisms (Sinclair et al, 2016;Rohr et al, 2018), including lizards, snakes, and turtles (Murrish and Vance, 1968;Jacobson and Whitford, 1970;Williamson et al, 1989;Brown, 1996).…”

Regulation of collagen deposition in the trout heart during thermal acclimation

“…Recent work using comparative models, including zebrafish and rainbow trout, have been providing novel insight into how an increase in deposited collagen, permanent in the mammalian heart, may be reversible ( Klaiman et al, 2011 ; Johnson et al, 2014 ). This work has been examining the response of the fish heart, primarily the single cardiac ventricle, to thermal acclimation ( Klaiman et al, 2011 , 2014 ; Johnson et al, 2014 ; Keen et al, 2016a , 2017 , 2018 ; Ding et al, 2021 ). Fish are ectothermic and their physiological temperature is determined by that of their environment.…”

“…While there are some fish that significantly reduce physical activity with such a decrease in physiological temperature, salmonids, including rainbow trout, as well as zebrafish do not ( Klaiman et al, 2011 ; Anttila et al, 2014 ; Elliott and Elliott, 2010 ; Rodnick et al, 2004 ; Cortemeglia and Beitinger, 2005 ; Sundin et al, 2019 ). Previous work has demonstrated that the heart of these fish can undergo changes in form, composition and function to help compensate for this change in physiological temperature so as to maintain contractility, and therefore activity of the animal ( Klaiman et al, 2011 , 2014 ; Gamperl and Farrell, 2004 ; Aho and Vornanen, 1999 , 2001 ; Keen et al, 2016b ; Driedzic et al, 1996 ). Cold acclimation of rainbow trout has also been found to cause an increase in the collagen content of the myocardium while warm acclimation reduces collagen content ( Fig.…”