Ambient temperature shapes reproductive output during pregnancy and lactation in the common vole (Microtus arvalis)

a test of the heat dissipation limit theory

Mirre J. P. Simons, Inonge Reimert, Vincent van der Vinne, Catherine Hambly, Lobke M. Vaanholt, John R. Speakman, Menno P. Gerkema

Research output: Contribution to journalArticle

34 Citations (Scopus)

Abstract

The heat dissipation limit theory suggests that heat generated during metabolism limits energy intake and, thus, reproductive output. Experiments in laboratory strains of mice and rats, and also domestic livestock generally support this theory. Selection for many generations in the laboratory and in livestock has increased litter size or productivity in these animals. To test the wider validity of the heat dissipation limit theory, we studied common voles (Microtus arvalis), which have small litter sizes by comparison with mice and rats, and regular addition of wild-caught individuals of this species to our laboratory colony ensures a natural genetic background. A crossover design of ambient temperatures (21 and 30 degrees C) during pregnancy and lactation was used. High ambient temperature during lactation decreased milk production, slowing pup growth. The effect on pup growth was amplified when ambient temperature was also high during pregnancy. Shaving fur off dams at 30 degrees C resulted in faster growth of pups; however, no significant increase in food intake and or milk production was detected. With increasing litter size (natural and enlarged), asymptotic food intake during lactation levelled off in the largest litters at both 21 and 30 degrees C. Interestingly, the effects of lactation temperature on pup growth where also observed at smaller litter sizes. This suggests that vole dams trade-off costs associated with hyperthermia during lactation with the yield from investment in pup growth. Moreover, pup survival was higher at 30 degrees C, despite lower growth, probably owing to thermoregulatory benefits. It remains to be seen how the balance is established between the negative effect of high ambient temperature on maternal milk production and pup growth (and/or future reproduction of the dam) and the positive effect of high temperatures on pup survival. This balance ultimately determines the effect of different ambient temperatures on reproductive success.

Original languageEnglish
Pages (from-to)38-49
Number of pages12
JournalJournal of Experimental Biology
Volume214
Issue number1
DOIs
Publication statusPublished - Jan 2011

Keywords

  • heat dissipation
  • litter size enlargement
  • sustained energy intake
  • fur removal
  • ambient temperature
  • lactation
  • pup mortality
  • sustained energy-intake
  • doubly-labeled water
  • mouse mus-musculus
  • metabolic-rate
  • laboratory mice
  • milk-production
  • food-intake
  • field-vole
  • body-mass
  • lasiopodomys-brandtii

Cite this

Ambient temperature shapes reproductive output during pregnancy and lactation in the common vole (Microtus arvalis) : a test of the heat dissipation limit theory. / Simons, Mirre J. P.; Reimert, Inonge; van der Vinne, Vincent; Hambly, Catherine; Vaanholt, Lobke M.; Speakman, John R.; Gerkema, Menno P.

In: Journal of Experimental Biology, Vol. 214, No. 1, 01.2011, p. 38-49.

Research output: Contribution to journalArticle

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abstract = "The heat dissipation limit theory suggests that heat generated during metabolism limits energy intake and, thus, reproductive output. Experiments in laboratory strains of mice and rats, and also domestic livestock generally support this theory. Selection for many generations in the laboratory and in livestock has increased litter size or productivity in these animals. To test the wider validity of the heat dissipation limit theory, we studied common voles (Microtus arvalis), which have small litter sizes by comparison with mice and rats, and regular addition of wild-caught individuals of this species to our laboratory colony ensures a natural genetic background. A crossover design of ambient temperatures (21 and 30 degrees C) during pregnancy and lactation was used. High ambient temperature during lactation decreased milk production, slowing pup growth. The effect on pup growth was amplified when ambient temperature was also high during pregnancy. Shaving fur off dams at 30 degrees C resulted in faster growth of pups; however, no significant increase in food intake and or milk production was detected. With increasing litter size (natural and enlarged), asymptotic food intake during lactation levelled off in the largest litters at both 21 and 30 degrees C. Interestingly, the effects of lactation temperature on pup growth where also observed at smaller litter sizes. This suggests that vole dams trade-off costs associated with hyperthermia during lactation with the yield from investment in pup growth. Moreover, pup survival was higher at 30 degrees C, despite lower growth, probably owing to thermoregulatory benefits. It remains to be seen how the balance is established between the negative effect of high ambient temperature on maternal milk production and pup growth (and/or future reproduction of the dam) and the positive effect of high temperatures on pup survival. This balance ultimately determines the effect of different ambient temperatures on reproductive success.",
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