Intrinsic mechanical properties of the perfused armoured catfish heart with special reference to the effects of hypercapnic acidosis on maximum cardiac performance

Abstract

SUMMARYThe armoured catfish, Pterygoplichthys pardalis, is known to be extremely tolerant of environmental hypercarbia (elevated water CO 2 tensions), which occurs in their natural environment. In addition, previous studies have demonstrated that during exposure to hypercarbia, P. pardalis does not exhibit extracellular pH compensation and thus the heart and other organs must continue to function despite a severe extracellular acidosis. We used an in situ perfused heart preparation to determine the effects of an extracellular hypercapnic (elevated CO 2 in the animal) acidosis (1-7.5% CO 2 ) on heart function, specifically cardiac output, power output, heart rate and stroke volume. The present study is the first to comprehensively examine cardiac function in an acidosistolerant teleost. When compared with control conditions, maximum cardiac performance was unaffected at levels of CO 2 as high as 5%, far exceeding the hypercapnic tolerance of other teleosts. Moreover, P. pardalis exhibited only a moderate decrease (~35%) in cardiac performance when exposed to 7.5% CO 2 , and full cardiac performance was restored in six out of seven hearts upon return to control conditions. Myocardial intracellular pH (pH i ) was protected in situ, as has been found in vivo, and this protection extended to the highest level of CO 2 (7.5%) investigated. Thus, maintained heart function during a hypercapnic acidosis in P. pardalis is probably associated with preferential pH i regulation of the heart, but ultimately is not sufficient to prevent loss of cardiac function. Our findings suggest the need for further study to elucidate the mechanisms behind this remarkable cardiac hypercapnic tolerance.

Exceptional CO2Tolerance in White Sturgeon (Acipenser transmontanus) Is Associated with Protection of Maximum Cardiac Performance during Hypercapnia In Situ

“…The in situ heart preparation used in this study has been described in detail for different species, with a variety of minor modifications (Farrell et al 1983;Farrell and Milligan 1986;Hanson et al 2006Hanson et al , 2009. In brief, white sturgeon (300-1,300 g; relative ventricular weight ) were anesthe-0.096% ‫ע‬ 0.003% tized in buffered tricaine methane sulfonate (0.3 g L Ϫ1 of both MS-222 and NaHCO 3 ), weighed, and transferred to an operating table.…”

“…Consequently, data from hearts tested at a given CO 2 were pooled for all analyses. Multistep protocols have been used to assess maximum cardiac performance in other CO 2 -tolerant fishes (Hanson et al 2009). All perfusates contained 10 nmol L Ϫ1 [AD].…”

“…Correspondingly, ventricular strips from the eel recover contractility within 20 min after exposure to sustained severe hypercapnia (10-kPa Pco 2 ; Gesser et al 1982), while a similar treatment in rainbow trout results in a 20%-60% reduction in isometric force generation (Gesser et al 1982). The armored catfish heart also stands out for its high CO 2 tolerance, since a 6.5-kPa Pco 2 increase above control levels was required to decrease PO max and Q max by ∼50% in an isolated perfused (pericardium intact) heart preparation (Hanson et al 2009). …”

“…For example, some CO 2 -sensitive hearts show adrenergic cardiac protection (Gesser et al 1982;Farrell 1985) but not ventricular pHi regulation (Farrell and Milligan 1986). In contrast, armored catfish hearts at a higher Pco 2 and saturating levels of exogenous adrenaline exhibited reduced cardiac performance in situ, suggesting less cardiac protection through adrenergic pathways in CO 2 -tolerant fishes (Hanson et al 2009). These reductions were observed despite complete ventricular pHi compensation (Hanson et al 2009).…”

“…In contrast, armored catfish hearts at a higher Pco 2 and saturating levels of exogenous adrenaline exhibited reduced cardiac performance in situ, suggesting less cardiac protection through adrenergic pathways in CO 2 -tolerant fishes (Hanson et al 2009). These reductions were observed despite complete ventricular pHi compensation (Hanson et al 2009). White sturgeon hearts may also be CO 2 tolerant, as routine cardiac output was unchanged in vivo during short-term hypercarbia (Pco 2 of 22.5 mm Hg; Crocker et al 2000).…”