School of Life Sciences, University of Nevada, Las Vegas, Las Vegas, NV, 89154, USA.
Department of Zoology, University of British Columbia, Vancouver, BC, V6T 1Z4, Canada.
J Comp Physiol B. 2024 Dec;194(6):869-885. doi: 10.1007/s00360-024-01587-9. Epub 2024 Oct 7.
Common tenrecs (Tenrec ecaudatus) are fossorial mammals that use burrows during both active and hibernating seasons in Madagascar and its neighboring islands. Prevailing thought was that tenrecs hibernate for 8-9 months individually, but 13 tenrecs were removed from the same sealed burrow 1 m deep from the surface. Such group hibernation in sealed burrows presumably creates a hypoxic and/or hypercapnic environment and suggests that this placental mammal may have an increased tolerance to hypoxia and hypercapnia. Higher tolerances to hypoxia and hypercapnia have been documented for other mammals capable of hibernation and to determine if this is the case for tenrecs, we exposed them to acute hypoxia (4 h of 16 or 7% O), progressive hypoxia (2 h of 16, 10 and 4% O), or progressive hypercapnia (2 h of 2, 5 and 10% CO) at cold (16 °C) or warm (28 °C) ambient temperatures (T). Oxygen equilibrium curves were also constructed on the whole blood of tenrecs at 10, 25, and 37 °C to determine if hemoglobin (Hb)-O affinity contributes to hypoxia tolerance. In animals held at 16 °C, normoxic and normocapnic levels of oxygen consumption rate ( ), body temperature (T), and heart rate (HR) were highly variable between individuals. This inter-individual variation was greatly reduced in animals held at 28 °C for oxygen consumption rate and body temperature. Both hypoxia (acute and progressive) and progressive hypercapnia led to decreases in as well as the variation in between animals held at 16 °C. The fall in oxygen consumption rate in 7% O independent of changes in body temperature in tenrecs held at 16 °C is unique and not consistent with the typical hypoxic metabolic response seen in other hibernating species that depends on concomitant falls in T. In animals held at 28 °C, exposure to O levels as low as 4% and CO levels as high as 10% had no significant effect on , HR, or T, indicative of high tolerance to both hypoxia and hypercapnia. High variation in heart rate remained between individuals in all gas compositions and at all temperatures. Tenrec Hb-O affinity was similar to other homeothermic placental mammals and likely does not contribute to the increased hypoxia tolerance. Ultimately, our results suggest changes in T dictate physiological responses to hypoxia or hypercapnia in tenrecs, responses more characteristic of reptiles than of most placental mammals. Given that numerous anatomical and physiological characteristics of tenrecs suggest that they may be representative of an ancestral placental mammal, our findings suggest the typical hypoxic metabolic response evolved later in mammalian evolution.
普通刺豚鼠(Tenrec ecaudatus)是一种穴居哺乳动物,在马达加斯加及其周边岛屿,无论是在活跃期还是冬眠期,它们都会使用洞穴。先前的观点认为,刺豚鼠会单独冬眠 8-9 个月,但在离地面 1 米深的同一个密封洞穴中,有 13 只刺豚鼠被取出。这种在密封洞穴中的群体冬眠可能会产生低氧和/或高碳酸环境,并表明这种胎盘哺乳动物可能对低氧和高碳酸有更高的耐受性。其他有冬眠能力的哺乳动物已经证明了对低氧和高碳酸的更高耐受性,为了确定刺豚鼠是否也如此,我们在冷(16°C)或暖(28°C)环境温度(T)下,让它们暴露于急性低氧(4 小时 16%或 7% O)、渐进性低氧(2 小时 16%、10%和 4% O)或渐进性高碳酸(2 小时 2%、5%和 10% CO)中。我们还在 10、25 和 37°C 下构建了刺豚鼠全血的氧平衡曲线,以确定血红蛋白(Hb)-O 亲和力是否有助于低氧耐受性。在以 16°C 饲养的动物中,个体间的正常氧消耗率(VO2)、体温(T)和心率(HR)的正常氧和正常碳酸水平的差异很大。在以 28°C 饲养的动物中,VO2 和 T 之间的个体差异大大减少。急性低氧和渐进性高碳酸都会导致 16°C 下饲养的动物的 VO2 降低,以及动物间 VO2 变异的减少。在以 16°C 饲养的刺豚鼠中,7% O 下的耗氧量下降与 T 无关,这是独特的,与其他依赖于 T 同时下降的冬眠物种的典型低氧代谢反应不一致。在以 28°C 饲养的动物中,暴露于低至 4%的 O 和高至 10%的 CO 水平对 VO2、HR 或 T 没有显著影响,表明对低氧和高碳酸有很高的耐受性。在所有气体组成和温度下,个体间的心率变化仍然很大。刺豚鼠的 Hb-O 亲和力与其他恒温胎盘哺乳动物相似,可能不会增加低氧耐受性。最终,我们的结果表明,T 的变化决定了刺豚鼠对低氧或高碳酸的生理反应,这种反应更符合爬行动物的特征,而不是大多数胎盘哺乳动物的特征。鉴于刺豚鼠的许多解剖和生理特征表明它们可能代表一种祖先胎盘哺乳动物,我们的研究结果表明,典型的低氧代谢反应是在哺乳动物进化的后期进化而来的。