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Abstract AimCardiac fibrosis contributes to systolic and diastolic dysfunction and can disrupt electrical pathways in the heart. There are currently no therapies that prevent or reverse fibrosis in human cardiac disease. However, animals like freshwater turtles undergo seasonal remodeling of their hearts, demonstrating the plasticity of fibrotic remodeling. InTrachemys scripta, cold temperature affects cardiac load, suppresses metabolism, and triggers a cardiac remodeling response that includes fibrosis. MethodsWe investigated this remodeling using Fourier transform infrared (FTIR) imaging spectroscopy, together with functional assessment of muscle stiffness, and molecular, histological, and enzymatic analyses in control (25°C)T. scriptaand after 8 weeks of cold (5°C) acclimation. ResultsFTIR revealed an increase in absorption bands characteristic of protein, glycogen, and collagen following cold acclimation, with a corresponding decrease in bands characteristic of lipids and phosphates. Histology confirmed these responses. Functionally, micromechanical stiffness of the ventricle increased following cold exposure assessed via atomic force microscopy (AFM) and was associated with decreased activity of regulatory matrix metalloproteinases (MMPs) and increased expression of MMP inhibitors (TMPs) which regulate collagen deposition. ConclusionsBy defining the structural and metabolic underpinnings of the cold‐induced remodeling response in the turtle heart, we show commonalities between metabolic and fibrotic triggers of pathological remodeling in human cardiac disease. We propose the turtle ventricle as a novel model for studying the mechanisms underlying fibrotic and metabolic cardiac remodeling. 

Abstract Flat hydrodynamic shells likely represent an evolutionary trade-off between adaptation to an aquatic lifestyle and the instability of more rounded shells, thought beneficial for self-righting. Trade-offs often result in compromises, this is particularly true when freshwater turtles, with flatter shells, must self-right to avoid the negative effects of inverting. These turtles, theoretically, invest more biomechanical effort to achieve successful and timely self-righting when compared to turtles with rounded carapaces. This increase in effort places these hatchlings in a precarious position; prone to inversion and predation and with shells seemingly maladapted to the act of self-righting. Here, we examine hatchling self-righting performance in three morphologically distinct freshwater turtle species (Apalone spinifera,Chelydra serpentinaandTrachemys scripta scripta) that inhabit similar environmental niches. We demonstrate that these hatchlings were capable of rapid self-righting and used considerably less biomechanical effort relative to adult turtles. Despite differences in shell morphology the energetic efficiency of self-righting remained remarkably low and uniform between the three species. Our results confound theoretical predictions of self-righting ability based on shell shape metrics and indicate that other morphological characteristics like neck or tail morphology and shell material properties must be considered to better understand the biomechanical nuances of Testudine self-righting. 

ABSTRACT Animals at early life stages are generally more sensitive to environmental stress than adults. This is especially true of oviparous vertebrates that develop in variable environments with little or no parental care. These organisms regularly experience environmental fluctuations as part of their natural development, but climate change is increasing the frequency and intensity of these events. The developmental plasticity of oviparous vertebrates will therefore play a critical role in determining their future fitness and survival. In this Review, we discuss and compare the phenotypic consequences of chronic developmental hypoxia on the cardiovascular system of oviparous vertebrates. In particular, we focus on species-specific responses, critical windows, thresholds for responses and the interactive effects of other stressors, such as temperature and hypercapnia. Although important progress has been made, our Review identifies knowledge gaps that need to be addressed if we are to fully understand the impact of climate change on the developmental plasticity of the oviparous vertebrate cardiovascular system. 

ABSTRACT Vertebrates utilize various respiratory organs such as gills, lungs and skin in combination with diverse cardiovascular structures, including single-, three- and four-chambered hearts, to enable oxygen delivery and carbon dioxide removal. They also exhibit differences in aerobic and anaerobic metabolism during exertion, but the cardiorespiratory gas transport of all vertebrates is a four-step process governed by Fick's Principle and Fick's Law of Diffusion over the entire range of metabolic rates. Hillman et al. (2013) suggested that previous exercise studies have focused too narrowly on mammals and proposed that the cardiorespiratory system's excess capacity serves an evolutionary role in enhancing CO2 excretion in non-mammalian vertebrates. In contrast, an analysis by Hicks and Wang (2021) concluded that vertebrates maintain effective gas exchange even at peak activity, finding no evidence of arterial hypercapnia at maximal oxygen consumption and thus challenging the proposal of significant limitations to pulmonary or branchial CO2 efflux. In the present study, we investigated the limits for CO2 exchange in exercising American alligators (Alligator mississippiensis) and provide evidence that the cardiorespiratory system is adequately built to sustain CO2 excretion during strenuous exercise and maintain arterial PCO2, with no evidence of diffusion limitation for pulmonary CO2 excretion. 

ABSTRACT Oxygen deprivation during embryonic development can permanently remodel the vertebrate heart, often causing cardiovascular abnormalities in adulthood. While this phenomenon is mostly damaging, recent evidence suggests developmental hypoxia produces stress-tolerant phenotypes in some ectothermic vertebrates. Embryonic common snapping turtles (Chelydra serpentina) subjected to chronic hypoxia display improved cardiac anoxia tolerance after hatching, which is associated with altered Ca2+ homeostasis in heart cells (cardiomyocytes). Here, we examined the possibility that changes in Ca2+ cycling, through the sarcoplasmic reticulum (SR), underlie the developmentally programmed cardiac phenotype of snapping turtles. We investigated this hypothesis by isolating cardiomyocytes from juvenile turtles that developed in either normoxia (21% O2; ‘N21’) or chronic hypoxia (10% O2; ‘H10’) and subjected the cells to anoxia/reoxygenation, in either the presence or absence of SR Ca2+-cycling inhibitors. We simultaneously measured cellular shortening, intracellular Ca2+ concentration ([Ca2+]i), and intracellular pH (pHi). Under normoxic conditions, N21 and H10 cardiomyocytes shortened equally, but H10 Ca2+ transients (Δ[Ca2+]i) were twofold smaller than those of N21 cells, and SR inhibition only decreased N21 shortening and Δ[Ca2+]i. Anoxia subsequently depressed shortening, Δ[Ca2+]i and pHi in control N21 and H10 cardiomyocytes, yet H10 shortening and Δ[Ca2+]i recovered to pre-anoxic levels, partly due to enhanced myofilament Ca2+ sensitivity. SR blockade abolished the recovery of anoxic H10 cardiomyocytes and potentiated decreases in shortening, Δ[Ca2+]i and pHi. Our novel results provide the first evidence of developmental programming of SR function and demonstrate that developmental hypoxia confers a long-lasting, superior anoxia-tolerant cardiac phenotype in snapping turtles, by modifying SR function and enhancing myofilament Ca2+ sensitivity. 

Abstract Armoured, rigid bodied animals, such as Testudines, must self-right should they find themselves in an inverted position. The ability to self-right is an essential biomechanical and physiological process that influences survival and ultimately fitness. Traits that enhance righting ability may consequently offer an evolutionary advantage. However, the energetic requirements of self-righting are unknown. Using respirometry and kinematic video analysis, we examined the metabolic cost of self-righting in the terrestrial Mediterranean spur-thighed tortoise and compared this to the metabolic cost of locomotion at a moderate, easily sustainable speed. We found that self-righting is, relatively, metabolically expensive and costs around two times the mass-specific power required to walk. Rapid movements of the limbs and head facilitate successful righting however, combined with the constraints of breathing whilst upside down, contribute a significant metabolic cost. Consequently, in the wild, these animals should favour environments or behaviours where the risk of becoming inverted is reduced. 

Abstract Quantitative functional anatomy of amniote thoracic and abdominal regions is crucial to understanding constraints on and adaptations for facilitating simultaneous breathing and locomotion. Crocodilians have diverse locomotor modes and variable breathing mechanics facilitated by basal and derived (accessory) muscles. However, the inherent flexibility of these systems is not well studied, and the functional specialisation of the crocodilian trunk is yet to be investigated. Increases in body size and trunk stiffness would be expected to cause a disproportionate increase in muscle force demands and therefore constrain the basal costal aspiration mechanism, necessitating changes in respiratory mechanics. Here, we describe the anatomy of the trunk muscles, their properties that determine muscle performance (mass, length and physiological cross‐sectional area [PCSA]) and investigate their scaling in juvenileAlligator mississippiensisspanning an order of magnitude in body mass (359 g–5.5 kg). Comparatively, the expiratory muscles (transversus abdominis,rectus abdominis,iliocostalis), which compress the trunk, have greater relative PCSA being specialised for greater force‐generating capacity, while the inspiratory muscles (diaphragmaticus,truncocaudalis ischiotruncus,ischiopubis), which create negative internal pressure, have greater relative fascicle lengths, being adapted for greater working range and contraction velocity. Fascicle lengths of the accessorydiaphragmaticusscaled with positive allometry in the alligators examined, enhancing contractile capacity, in line with this muscle's ability to modulate both tidal volume and breathing frequency in response to energetic demand during terrestrial locomotion. Theiliocostalis, an accessory expiratory muscle, also demonstrated positive allometry in fascicle lengths and mass. All accessory muscles of the infrapubic abdominal wall demonstrated positive allometry in PCSA, which would enhance their force‐generating capacity. Conversely, the basal tetrapod expiratory pump (transversus abdominis) scaled isometrically, which may indicate a decreased reliance on this muscle with ontogeny. Collectively, these findings would support existing anecdotal evidence that crocodilians shift their breathing mechanics as they increase in size. Furthermore, the functional specialisation of thediaphragmaticusand compliance of the body wall in the lumbar region against which it works may contribute to low‐cost breathing in crocodilians.