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Journal of Comparative Physiology B

, Volume 180, Issue 6, pp 877–884 | Cite as

Comparative respiratory strategies of subterranean and fossorial octodontid rodents to cope with hypoxic and hypercapnic atmospheres

  • I. H. TomascoEmail author
  • R. Del Río
  • R. Iturriaga
  • F. Bozinovic
Original Paper

Abstract

Subterranean rodents construct large and complex burrows and spend most of their lives underground, while fossorial species construct simpler burrows and are more active above ground. An important constraint faced by subterranean mammals is the chronic hypoxia and hypercapnia of the burrow atmosphere. The traits, regarded as “adaptations of rodents to hypoxia and hypercapnia”, have been evaluated in only a few subterranean species. In addition, well-studied subterranean taxa are very divergent to their sister groups, making it difficult to assess the adaptive path leading to subterranean life. The closely related sister genera Octodon and Spalacopus of Neotropical rodents offer a unique opportunity to trace the evolution of physiological mechanisms. We studied the ventilatory responses of selected octodontid rodents to selective pressures imposed by the subterranean niche under the working hypothesis that life underground, in hypoxic and hypercapnic conditions, promotes convergent physiological changes. To perform this study we used the following species: Spalacopus cyanus (the subterranean coruros) and Octodon degus (the fossorial degus) from central Chile. Ventilatory tidal volume and respiratory frequency were measured in non-anaesthetized spontaneously breathing animals. Acute hypoxic challenges (O2 1–15%) and hypercapnia (CO2 10%) were induced to study respiratory strategies using non-invasive whole body pletismography techniques. Our results show that coruros have a larger ventilatory response to acute hypoxia as than degus. On the other hand, hypercapnic respiratory responses in coruros seem to be attenuated when compared to those in degus. Our results suggest that coruros and degus have different respiratory strategies to survive in the hypoxic and hypercapnic atmospheres present in their burrows.

Keywords

Ventilatory response Hypoxia Hypercapnia Octodontids Rodents 

Notes

Acknowledgments

This study was supported by PEDECIBA (Programa de Desarrollo de las Ciencias Básicas), ANII (Agencia Nacional de Innovación e Investigación), PDT (Programa de Desarrollo tecnológico) from Uruguay, ASM (American Society of Mammologists) from USA, and CONICYT (Comisión Nacional de Investigación Científica y Tecnológica) from Chile. We thank Dr. Lessa for the idea and encouragement, Alejandra Chiesa and Carolina Abud for a revision of the manuscript, and two anonymous reviewers for constructive criticisms.

References

  1. Arieli R (1979) The atmospheric environment of the fossorial mole rat (Spalax ehrenbergi): effects of season, soil texture, rain, temperature and activity. Comp Biochem Physiol 63A:569–575Google Scholar
  2. Arieli R (1990) Adaptation of the mammalian gas transport system to subterranean life. In: Nevo E, Reig OA (eds) Evolution of subterranean mammals at the organismal and molecular levels. Wiley-Liss, New York, pp 251–268Google Scholar
  3. Arieli R, Ar A (1979) Ventilation of a fossorial mammal (Spalax ehrenbergi) in hypoxic and hypercapnic conditions. J Appl Physiol 47:1011–1017PubMedGoogle Scholar
  4. Arieli R, Nevo E (1991) Hypoxic survival differs between two mole rat species (Spalax ehrenbergi) of humid and arid habitats. Comp Biochem Physiol A 100:543–545CrossRefPubMedGoogle Scholar
  5. Arieli R, Heth G, Nevo E, Zamir Y, Neutra O (1986) Adaptive heart and breathing frequencies in 4 ecologically differentiating chromosomal species of mole rats in Israel. Experientia 42:131–133CrossRefGoogle Scholar
  6. Avivi A, Brodsky L, Nevo E, Band MR (2006) Differential expression profiling of the blind subterranean mole rat Spalax ehrenbergi superspecies: bio-prospecting for hypoxia tolerance. Physiol Genomics 27:54–64CrossRefPubMedGoogle Scholar
  7. Barros RC, Oliveira ES, Rocha PL, Branco LG (1998) Respiratory and metabolic responses of the spiny rats Proechimys yonenagae and P. iheringi to CO2. Respir Physiol 111:223–231CrossRefPubMedGoogle Scholar
  8. Barros RC, Zimmer ME, Branco LG, Milsom WK (2001) Hypoxic metabolic response of the golden-mantled ground squirrel. J Appl Physiol 91:603–612PubMedGoogle Scholar
  9. Boggs DF (1992) Comparative control of respiration. In: Parent RA (ed) Comparative biology of the normal lung. CRC Press, Boca Raton, pp 309–350Google Scholar
  10. Boggs DF, Birchard GF (1989) Cardio-respiratory responses of the woodchuck and porcupine to CO2 and hypoxia. J Comp Physiol 159B:641–648Google Scholar
  11. Boggs DF, Kilgore DL, Birchard GF (1984) Respiratory physiology of burrowing mammals and birds. Comp Biochem Physiol A 77:239–245CrossRefGoogle Scholar
  12. Boggs DF, Frappell PB, Kilgore DL Jr (1998) Ventilatory, cardiovascular and metabolic responses to hypoxia and hypercapnia in the armadillo. Respir Physiol 113:101–109CrossRefPubMedGoogle Scholar
  13. Buffenstein R (2000) Ecophysiological responses of subterranean rodents to underground habitats. In: Lacey EA, Patton JL, Cameron GN (eds) Life underground: the biology of subterranean rodents. University of Chicago Press, Chicago, pp 62–110Google Scholar
  14. Caballero B, Tomas-Zapico C, Vega-Naredo I, Sierra V, Tolivia D, Hardeland R, Rodriguez-Colunga MJ, Joel A, Nevo E, Avivi A, Coto-Montes A (2006) Antioxidant activity in Spalax ehrenbergi: a possible adaptation to underground stress. J Comp Physiol A 192:753–759CrossRefGoogle Scholar
  15. Contreras LC (1986) Bioenergetics and distribution of fossorial Spalacopus cyanus (Rodentia): thermal stress, or cost of burrowing. Physiol Zool 59:20–28Google Scholar
  16. Contreras LC, McNab BK (1990) Thermoregulation and energetics in subterranean mammals. Prog Clin Biol 35:231–250Google Scholar
  17. Darden TR (1972) Respiratory adaptations of fossorial mammal, the pocket gopher (Thomomys bottae). J Comp Physiol 78:121–137CrossRefGoogle Scholar
  18. Dejours P (1962) Chemoreflexes in breathing. Physiol Rev 42:335–358PubMedGoogle Scholar
  19. Dwinell MR, Powell FL (1999) Chronic hypoxia enhances the phrenic nerve response to arterial chemoreceptor stimulation in anesthetized rats. J Appl Physiol 87:817–823PubMedGoogle Scholar
  20. Frappell PB, Franklin CE, Grigg GC (1994) Ventilatory and metabolic responses to hypoxia in the echidna, Tachyglossus aculeatus. Am J Physiol 267:R1510–R1515PubMedGoogle Scholar
  21. Frappell PB, Baudinette RV, MacFarlane PM, Wiggins PR, Shimmin G (2002) Ventilation and metabolism in a large semifossorial marsupial: the effect of graded hypoxia and hypercapnia. Physiol Biochem Zool 75:77–82CrossRefPubMedGoogle Scholar
  22. Garland RJ, Kinkead R, Milsom WK (1994) The ventilatory response of rodents to changes in arterial oxygen content. Respir Physiol 96:199–211CrossRefPubMedGoogle Scholar
  23. Lacey EA, Patton JL, Cameron GN (2000) Life underground: the biology of subterranean rodents. University of Chicago Press, ChicagoGoogle Scholar
  24. Lechner AJ (1977) Metabolic performance during hypoxia in native and acclimated pocket gophers. J Appl Physiol 43:965–970PubMedGoogle Scholar
  25. Lessa EP, Vassallo AI, Verzi DH, Mora MS (2008) Evolution of morphological adaptations for digging in living and extinct ctenomyid and octodontid rodents. Biol J Linn Soc Lond 95:267–283CrossRefGoogle Scholar
  26. Ling L, Fuller DD, Bach KB, Kinkead R, Olson EB Jr, Mitchell GS (2001) Chronic intermittent hypoxia elicits serotonin dependent plasticity in the central neural control of breathing. J Neurosci 21:5381–5388PubMedGoogle Scholar
  27. Lovegrove BG (1989) The cost of burrowing of the social mole rats (Bathyergidae) Cryptomys damarensis and Heterocephalus glaber: the role of soil moisture. Physiol Zool 62:449–469Google Scholar
  28. MacLean GS (1981) Factor influencing the composition of respiratory gases in mammals burrows. Comp Biochem Physiol 69:373–383Google Scholar
  29. Milsom WK, McArthur MD, Webb CL (1986) Control of breathing in hibernating ground squirrels. In: Heller HC, Musacchia XJ, Wang LCH (eds) Living in the cold: physiological and biochemical adaptations. Elsevier, New York, pp 469–475Google Scholar
  30. Mitchell GS, Johnson SM (2003) Plasticity in respiratory motor control. Invited review: neuroplasticity in respiratory motor control. J Appl Physiol 94:358–374PubMedGoogle Scholar
  31. Morrison P, Rosenmann M (1975) Metabolic level and limiting hypoxia in rodents. Comp Biochem Physiol A Comp Physiol 51:881–885CrossRefPubMedGoogle Scholar
  32. Morrison P, Kerst K, Rosenmann M (1963) Hematocrit and hemoglobin levels in some Chilean rodents from high and low altitude. Int J Biometeor 7:45–50CrossRefGoogle Scholar
  33. Mortola JP (2004) Implications of hypoxic hypometabolism during mammalian ontogenesis. Mortola Respir Physiol Neurobiol 141:345–356CrossRefGoogle Scholar
  34. Nasser NJ, Nevo E, Shafat I, Ilan N, Vlodavsky I, Avivi A (2005) Adaptive evolution of heparanase in hypoxia-tolerant Spalax: gene cloning and identification of a unique splice variant. Proc Natl Acad Sci USA 102:15161–15166CrossRefPubMedGoogle Scholar
  35. Nevo E (1999) Mosaic evolution of subterranean mammals: regression, progression, and global convergence. Oxford University Press, OxfordGoogle Scholar
  36. Okubo S, Mortola JP (1990) Control of ventilation in adult rats hypoxic in the neonatal period. Am J Physiol Regul Integr Comp Physiol 259:R836–R841Google Scholar
  37. Opazo JC (2005) A molecular timescale for caviomorph rodents (Mammalia, Hystricognathi). Mol Phyl Evol 37:932–937CrossRefGoogle Scholar
  38. Polyakov A, Beharav A, Avivi A, Nevo E (2004) Mammalian microevolution in action: adaptive edaphic genomic divergence in blind subterranean mole-rats. Proc Biol Sci 271(Suppl 4):S156–S159CrossRefPubMedGoogle Scholar
  39. Powell FL, Milsom WK, Mitchell GS (1998) Time domains of the hypoxic ventilatory response. Respir Physiol 112:123–134CrossRefPubMedGoogle Scholar
  40. Prabhakar NR (2001) Oxygen sensing during intermittent hypoxia: cellular and molecular mechanisms. J Appl Physiol 90:1986–1994CrossRefPubMedGoogle Scholar
  41. Quilliam TA, Clarke JA, Salsbury AJ (1971) The ecological significance of certain new haematological findings in the mole and hedgehog. Comp Biochem Physiol A 40:89–102CrossRefPubMedGoogle Scholar
  42. Ramírez JM, Folkow LP, Blix AS (2007) Hypoxia tolerance in mammals and birds: from the wilderness to the clinic. Annu Rev Physiol 69:113–143CrossRefPubMedGoogle Scholar
  43. Rey S, Del Río R, Alcayaga J, Iturriaga R (2004) Chronic intermittent hypoxia enhances cat chemosensory and ventilatory responses to hypoxia. J Physiol 560:577–586CrossRefPubMedGoogle Scholar
  44. Rosenmann M, Morrison PR (1975) Metabolic response of highland and lowland rodents to simulated high altitudes and cold. Comp Biochem Physiol A Comp Physiol 51:523–530CrossRefPubMedGoogle Scholar
  45. Shams I, Avivi A, Nevo E (2005) Oxygen and carbon dioxide fluctuations in burrows of subterranean blind mole rats indicate tolerance to hypoxic-hypercapnic stresses. Comp Biochem Physiol A Mol Integr Physiol 142:376–382CrossRefPubMedGoogle Scholar
  46. Stahl WR (1967) Scaling of respiratory variables in mammals. J Appl Physiol 22:453–460PubMedGoogle Scholar
  47. Tenney SM, Boggs DF (1986) Comparative mammalian respiratory control. In: Geiger SR (ed) Handbook of physiology: a critical, comprehensive presentation of physiological knowledge and concepts, sect 3, The respiratory system, Vol 2, Control of breathing. American Physiological Society, Bethesda, pp 833–855Google Scholar
  48. Vásquez RA, Ebensperger LA, Bozinovic F (2002) The effect of microhabitat on running velocity, intermittent locomotion, and vigilance in a diurnal rodent. Behav Ecol 13:182–187CrossRefGoogle Scholar
  49. Vleck D (1979) The energy cost of burrowing in the pocket gopher Thomomys bottae. Physiol Zool 64:871–884Google Scholar
  50. Walker BR, Adams EM, Voelkel NF (1985) Ventilatory responses of hamsters and rats to hypoxia and hypercapnia. J Appl Physiol 59:1955–1960PubMedGoogle Scholar
  51. Walsh JP, Boggs DF, Kilgore DL Jr (1996) Ventilatory and metabolic responses of a bat, Phyllostomus discolor, to hypoxia and CO2: implications for the allometry of respiratory control. J Comp Physiol B 166:351–358CrossRefPubMedGoogle Scholar
  52. Wang T, Warburton SJ (1995) Breathing pattern and cost of ventilation in the American alligator. Respir Physiol 102:29–37CrossRefPubMedGoogle Scholar
  53. Widmer HR, Hoppeler H, Nevo E, Taylor CR, Weibel ER (1997) Working underground: respiratory adaptations in the blind mole rat. Proc Natl Acad Sci USA 94:2062–2067CrossRefPubMedGoogle Scholar
  54. Withers PC (1978) Models of diffusion mediated gas exchange in animal burrows. Am Nat 112:1101–1167CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • I. H. Tomasco
    • 1
    Email author
  • R. Del Río
    • 2
  • R. Iturriaga
    • 2
  • F. Bozinovic
    • 3
  1. 1.Laboratorio de Evolución, Facultad de CienciasUniversidad de la RepúblicaMontevideoUruguay
  2. 2.Laboratorio de Neurobiología, Facultad de Ciencias BiológicasP. Universidad Católica de ChileSantiagoChile
  3. 3.Departamento de Ecología, Centro de Estudios Avanzados en Ecología y Biodiversidad, Facultad de Ciencias BiológicasP. Universidad Católica de ChileSantiagoChile

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