Comparative Respiratory Strategies of Subterranean and Fossorial Octodontid Rodents to Cope with Hypoxic and Hypercapnic Atmospheres
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J Comp Physiol B (2010) 180:877–884 DOI 10.1007/s00360-010-0465-y ORIGINAL PAPER Comparative respiratory strategies of subterranean and fossorial octodontid rodents to cope with hypoxic and hypercapnic atmospheres I. H. Tomasco • R. Del Rı´o • R. Iturriaga • F. Bozinovic Received: 8 October 2009 / Revised: 2 March 2010 / Accepted: 3 March 2010 / Published online: 30 March 2010 Ó Springer-Verlag 2010 Abstract Subterranean rodents construct large and com- Ventilatory tidal volume and respiratory frequency were plex burrows and spend most of their lives underground, measured in non-anaesthetized spontaneously breathing while fossorial species construct simpler burrows and are animals. Acute hypoxic challenges (O2 1–15%) and more active above ground. An important constraint faced by hypercapnia (CO2 10%) were induced to study respiratory subterranean mammals is the chronic hypoxia and hyper- strategies using non-invasive whole body pletismography capnia of the burrow atmosphere. The traits, regarded as techniques. Our results show that coruros have a larger ‘‘adaptations of rodents to hypoxia and hypercapnia’’, have ventilatory response to acute hypoxia as than degus. On the been evaluated in only a few subterranean species. In other hand, hypercapnic respiratory responses in coruros addition, well-studied subterranean taxa are very divergent seem to be attenuated when compared to those in degus. to their sister groups, making it difficult to assess the Our results suggest that coruros and degus have different adaptive path leading to subterranean life. The closely respiratory strategies to survive in the hypoxic and hyper- related sister genera Octodon and Spalacopus of Neotrop- capnic atmospheres present in their burrows. ical rodents offer a unique opportunity to trace the evolution of physiological mechanisms. We studied the ventilatory Keywords Ventilatory response Á Hypoxia Á responses of selected octodontid rodents to selective pres- Hypercapnia Á Octodontids Á Rodents sures imposed by the subterranean niche under the working hypothesis that life underground, in hypoxic and hyper- capnic conditions, promotes convergent physiological Introduction changes. To perform this study we used the following species: Spalacopus cyanus (the subterranean coruros) and The convergent evolution of subterranean mammals is one of Octodon degus (the fossorial degus) from central Chile. the most fascinating and puzzling evolutionary phenomena (Nevo 1999). Eight lineages of rodents have invaded the subterranean niche independently (Lacey et al. 2000); these Communicated by I. D. Hume. species live most of their lives underground in their usually closed burrows, and they are called collectively subterra- I. H. Tomasco (&) Laboratorio de Evolucio´n, Facultad de Ciencias, Universidad de nean. Other lineages have species that construct and use la Repu´blica, Igua´ 4225, 11400 Montevideo, Uruguay burrows, but are more active above ground, and they are e-mail: [email protected] called fossorial. Life underground imposes particular selective pressures, which have driven subterranean rodents R. Del Rı´o Á R. Iturriaga Laboratorio de Neurobiologı´a, Facultad de Ciencias Biolo´gicas, to develop convergent morphological and physiological P. Universidad Cato´lica de Chile, Santiago, Chile features (Nevo 1999). In comparison, fossorial rodents are much less specialized than subterranean species. F. Bozinovic An important constraint faced by subterranean mammals Departamento de Ecologı´a, Centro de Estudios Avanzados en Ecologı´a y Biodiversidad, Facultad de Ciencias Biolo´gicas, is the low availability of O2 (hypoxia) and the excess of CO2 P. Universidad Cato´lica de Chile, Santiago, Chile (hypercapnia) in the subterranean environment (Darden 123 878 J Comp Physiol B (2010) 180:877–884 1972; Arieli 1990; Shams et al. 2005). Maximal CO2 levels fluctuating O2 and CO2 levels by increasing the activity (6.1%) and minimal O2 levels (7.2%) were recorded in levels of antioxidant enzymes, such as superoxide dismu- northern Israel in the breeding mounds of Spalax carmeli in tase (Caballero et al. 2006). Recent studies have also found a flooded, poorly drained field of heavy clay soil with high differences in gene expression among subterranean species water content (Shams et al. 2005). Gas interchange between with different critical pO2 (Avivi et al. 2006; Nasser et al. burrows and atmosphere depends on the gas permeability 2005; Polyakov et al. 2004). However, these mechanisms properties of the soil, which is affected by such factors as have been evaluated in only a few subterranean species temperature and humidity (Arieli 1979), and the limited from the genera Spalax (Mediterranean), Heterocephalus ventilation is the result primarily of animal movements (African), and Thomomys (North American), and there are (Buffenstein 2000). These factors make burrow gas com- no comparative studies including several species. Besides, position to differ considerably from atmospheric air, and well-studied subterranean taxa are very divergent from their any activity of the inhabitants increases such difference. sister groups (if known), making it difficult to assess the Models of diffusion gas exchange (Withers 1978) and adaptive path leading to subterranean life. experimental data (MacLean 1981) show that, unless the To understand the physiological strategies of subterra- soil is completely devoid of biotic substances, burrow nean mammals for coping with subterranean atmospheric atmospheres will always be hypoxic and hypercapnic rela- conditions in comparison to less specialized forms, we tive to the surface atmosphere (Buffenstein 2000). examined the influence of experimental variations in hyp- Under low O2 partial pressure (pO2) in the burrow oxic and hypercapnic conditions on respiratory tidal volume atmosphere and facing the potential CO2 perturbation of and respiratory frequency in response to different values of their blood acid–base balance, subterranean mammals are pO2 and pCO2, of the fully subterranean coruro Spalacopus expected to show certain physiological mechanisms to cyanus (Rodentia: Octodontidae) and the fossorial degu avoid excessive energy expenditure in respiratory work. Octodon degus (Rodentia: Octodontidae). Coruros are dis- These mechanisms are not fully understood, but include tributed from 30 to 37°S along the coast of Chile and also several physiological adjustments in relation to the pre- above 2,000 m sea level in the Andes range. Degus are dicted values of mammals of similar body mass (predicted diurnal rodents inhabiting the semiarid and Mediterranean by Stahl 1967) and at different levels (reviewed by Boggs environments of northern and central Chile to 2,000 m above et al. 1984; Buffenstein 2000; Nevo 1999). For example, sea level. In many areas of their range of distribution, both the critical pO2 levels in these mammals are lower (Arieli species overlap and are sympatric, but one inhabits above 1990; Arieli and Nevo 1991; Lechner 1977), and metabolic (degus) and the other below (coruros) the surface. We rates can be maintained at low pO2 (Lovegrove 1989; hypothesized that coruros show an attenuated response to Vleck 1979). Besides, ventilation in normoxia is lower hypercapnia and hyperoxia compared with the related degus, (Arieli 1990; Boggs et al. 1998), and ventilatory response whereas the response to hypoxia is depressed in the latter. to hypoxia, hypercapnia, or both is attenuated (Arieli 1990; The closely related sister genera Octodon and Spalac- Boggs et al. 1998; Buffenstein 2000). Cardiac output and opus of Neotropical endemic rodents offer an opportunity heart frequency are also lower in normoxia (Arieli 1990), to trace the evolution of physiological traits. The mono- and show a twofold increased response to hypoxia even at typic genus Spalacopus is strictly subterranean and shares low temperatures (Arieli et al. 1986). Moreover, oxygen convergent adaptations to underground life, while the carrying capacity is increased, facilitated by elevated genus Octodon has three burrowing species. Moreover, the hemoglobin concentrations, high intrinsic affinity for phylogenetic relationships and estimations of divergence oxygen and more red blood cells (reviewed by Buffenstein times are well established as relatively recent (reviewed by 2000). Furthermore, their myoglobin concentration is Opazo 2005), which would allow tracing the changes higher in blood and skeletal muscles; the capillary density associated with the acquisition of subterranean adaptations in myocardium, skeletal muscles, and lungs is elevated along a known phylogeny, as well as identifying and dis- (Arieli 1990), and they have a high relative amount of criminating such adaptations from more general ones mitochondria in skeletal muscles (Widmer et al. 1997). associated with fossoriality. Finally, they have high arterial and tissue pCO2 (Arieli 1990), and they cope with it without altering the blood acid–base equilibrium by at least two known different Methods mechanisms (Buffenstein 2000; Quilliam et al. 1971). Other mechanisms are known only for species of the Animals studied genus Spalax and are related to shortening of the diffusion distance, increase of the O2 permeability constant (reviewed Experiments were performed on five adults of the fossorial by Arieli 1990), and avoidance of oxidative damage under species Octodon degus (‘‘degus’’; all males between 194.4 123 J Comp Physiol B (2010) 180:877–884 879 and 217.8 g) and four adults of the subterranean species (100% O2) stimuli