Limits to sustained energy intake VII: Milk energy output in laboratory mice at thermoneutralith

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Abstract

The limits to sustained energy intake at peak lactation could be imposed peripherally, by the capacity of the mammary glands, or centrally, by the capacity of the animal to dissipate body heat generated as a by-product of processing food and producing milk. To distinguish between the two hypotheses, we examined milk energy output at peak lactation in MF1 laboratory mice exposed to 30degreesC (N=12), 21degreesC (N=10; published data) and 8degreesC (N=10; published data). The peripheral limitation hypothesis predicts that milk energy output will remain constant at different temperatures, while the heat dissipation limit hypothesis predicts a decline in milk energy output as temperature increases. Since estimates of milk energy output in small mammals can vary depending on the calculation method used, we evaluated the milk energy output of mice (N=24) using four different methods: (1) as the difference between metabolizable energy intake and daily energy expenditure of the female, (2) from female water turnover, (3) from pup water turnover and (4) from the energy budget of the litter. We assessed these four methods by comparing their accuracy, precision and sensitivity to changes in parameters involved in the calculations. Methods 1, 3 and 4 produced similar estimates of milk energy output, while those derived from female water turnover were significantly lower and more variable. On average, mice at 30degreesC exported significantly less energy as milk (87.7 kJ day(-1)) than mice at 21degreesC (166.7 kJ day(-1)) and 8degreesC (288.0 kJ day(-1)). This reduction in milk energy output at 30degreesC was caused by a significant decline in both milk flow (20.0 g day(-1), 12.9 g day(-1) and 8.5 g day(-1) at 8degreesC, 21degreesC and 30degreesC, respectively) and gross energy content of milk (14.6 kJ g(-1), 13.1 kJ g(-1) and 10.5 kJ g(-1) at 8degreesC, 21degreesC and 30degreesC, respectively). Milk produced at 30'C contained significantly less total solids (34.4%) than milk at 21degreesC (40.9%) and 8degreesC (41.5%) and significantly less fat (20.0%) than milk at 21degreesC (26.4%) and 8degreesC (30.3%). The reduced milk energy output in mice exposed to 30degreesC, paralleled by their reduced food intake and low reproductive output, argues against the peripheral limitation hypothesis and provides strong support for the heat dissipation limit hypothesis.

Original languageEnglish
Pages (from-to)4267-4281
Number of pages14
JournalJournal of Experimental Biology
Volume206
Issue number23
DOIs
Publication statusPublished - 2003

Keywords

  • doubly labelled water
  • daily energy expenditure
  • water turnover
  • water balance
  • milk composition
  • peripheral limit
  • heat dissipation limit
  • laboratory mouse
  • Mus musculus
  • RATIO MASS-SPECTROMETRY
  • MOTHER-YOUNG CONTACT
  • MUS-MUSCULUS
  • LITTER SIZE
  • MATERNAL-BEHAVIOR
  • METABOLIC-RATE
  • CONCURRENT PREGNANCY
  • SIGMODON-HISPIDUS
  • TRITIATED-WATER
  • THERMAL CONTROL

Cite this

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title = "Limits to sustained energy intake VII: Milk energy output in laboratory mice at thermoneutralith",
abstract = "The limits to sustained energy intake at peak lactation could be imposed peripherally, by the capacity of the mammary glands, or centrally, by the capacity of the animal to dissipate body heat generated as a by-product of processing food and producing milk. To distinguish between the two hypotheses, we examined milk energy output at peak lactation in MF1 laboratory mice exposed to 30degreesC (N=12), 21degreesC (N=10; published data) and 8degreesC (N=10; published data). The peripheral limitation hypothesis predicts that milk energy output will remain constant at different temperatures, while the heat dissipation limit hypothesis predicts a decline in milk energy output as temperature increases. Since estimates of milk energy output in small mammals can vary depending on the calculation method used, we evaluated the milk energy output of mice (N=24) using four different methods: (1) as the difference between metabolizable energy intake and daily energy expenditure of the female, (2) from female water turnover, (3) from pup water turnover and (4) from the energy budget of the litter. We assessed these four methods by comparing their accuracy, precision and sensitivity to changes in parameters involved in the calculations. Methods 1, 3 and 4 produced similar estimates of milk energy output, while those derived from female water turnover were significantly lower and more variable. On average, mice at 30degreesC exported significantly less energy as milk (87.7 kJ day(-1)) than mice at 21degreesC (166.7 kJ day(-1)) and 8degreesC (288.0 kJ day(-1)). This reduction in milk energy output at 30degreesC was caused by a significant decline in both milk flow (20.0 g day(-1), 12.9 g day(-1) and 8.5 g day(-1) at 8degreesC, 21degreesC and 30degreesC, respectively) and gross energy content of milk (14.6 kJ g(-1), 13.1 kJ g(-1) and 10.5 kJ g(-1) at 8degreesC, 21degreesC and 30degreesC, respectively). Milk produced at 30'C contained significantly less total solids (34.4{\%}) than milk at 21degreesC (40.9{\%}) and 8degreesC (41.5{\%}) and significantly less fat (20.0{\%}) than milk at 21degreesC (26.4{\%}) and 8degreesC (30.3{\%}). The reduced milk energy output in mice exposed to 30degreesC, paralleled by their reduced food intake and low reproductive output, argues against the peripheral limitation hypothesis and provides strong support for the heat dissipation limit hypothesis.",
keywords = "doubly labelled water, daily energy expenditure, water turnover, water balance, milk composition, peripheral limit, heat dissipation limit, laboratory mouse, Mus musculus, RATIO MASS-SPECTROMETRY, MOTHER-YOUNG CONTACT, MUS-MUSCULUS, LITTER SIZE, MATERNAL-BEHAVIOR, METABOLIC-RATE, CONCURRENT PREGNANCY, SIGMODON-HISPIDUS, TRITIATED-WATER, THERMAL CONTROL",
author = "Krol, {Elzbieta Barbara} and Speakman, {John Roger}",
year = "2003",
doi = "10.1242/jeb.00675",
language = "English",
volume = "206",
pages = "4267--4281",
journal = "Journal of Experimental Biology",
issn = "0022-0949",
publisher = "Company of Biologists Ltd",
number = "23",

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TY - JOUR

T1 - Limits to sustained energy intake VII: Milk energy output in laboratory mice at thermoneutralith

AU - Krol, Elzbieta Barbara

AU - Speakman, John Roger

PY - 2003

Y1 - 2003

N2 - The limits to sustained energy intake at peak lactation could be imposed peripherally, by the capacity of the mammary glands, or centrally, by the capacity of the animal to dissipate body heat generated as a by-product of processing food and producing milk. To distinguish between the two hypotheses, we examined milk energy output at peak lactation in MF1 laboratory mice exposed to 30degreesC (N=12), 21degreesC (N=10; published data) and 8degreesC (N=10; published data). The peripheral limitation hypothesis predicts that milk energy output will remain constant at different temperatures, while the heat dissipation limit hypothesis predicts a decline in milk energy output as temperature increases. Since estimates of milk energy output in small mammals can vary depending on the calculation method used, we evaluated the milk energy output of mice (N=24) using four different methods: (1) as the difference between metabolizable energy intake and daily energy expenditure of the female, (2) from female water turnover, (3) from pup water turnover and (4) from the energy budget of the litter. We assessed these four methods by comparing their accuracy, precision and sensitivity to changes in parameters involved in the calculations. Methods 1, 3 and 4 produced similar estimates of milk energy output, while those derived from female water turnover were significantly lower and more variable. On average, mice at 30degreesC exported significantly less energy as milk (87.7 kJ day(-1)) than mice at 21degreesC (166.7 kJ day(-1)) and 8degreesC (288.0 kJ day(-1)). This reduction in milk energy output at 30degreesC was caused by a significant decline in both milk flow (20.0 g day(-1), 12.9 g day(-1) and 8.5 g day(-1) at 8degreesC, 21degreesC and 30degreesC, respectively) and gross energy content of milk (14.6 kJ g(-1), 13.1 kJ g(-1) and 10.5 kJ g(-1) at 8degreesC, 21degreesC and 30degreesC, respectively). Milk produced at 30'C contained significantly less total solids (34.4%) than milk at 21degreesC (40.9%) and 8degreesC (41.5%) and significantly less fat (20.0%) than milk at 21degreesC (26.4%) and 8degreesC (30.3%). The reduced milk energy output in mice exposed to 30degreesC, paralleled by their reduced food intake and low reproductive output, argues against the peripheral limitation hypothesis and provides strong support for the heat dissipation limit hypothesis.

AB - The limits to sustained energy intake at peak lactation could be imposed peripherally, by the capacity of the mammary glands, or centrally, by the capacity of the animal to dissipate body heat generated as a by-product of processing food and producing milk. To distinguish between the two hypotheses, we examined milk energy output at peak lactation in MF1 laboratory mice exposed to 30degreesC (N=12), 21degreesC (N=10; published data) and 8degreesC (N=10; published data). The peripheral limitation hypothesis predicts that milk energy output will remain constant at different temperatures, while the heat dissipation limit hypothesis predicts a decline in milk energy output as temperature increases. Since estimates of milk energy output in small mammals can vary depending on the calculation method used, we evaluated the milk energy output of mice (N=24) using four different methods: (1) as the difference between metabolizable energy intake and daily energy expenditure of the female, (2) from female water turnover, (3) from pup water turnover and (4) from the energy budget of the litter. We assessed these four methods by comparing their accuracy, precision and sensitivity to changes in parameters involved in the calculations. Methods 1, 3 and 4 produced similar estimates of milk energy output, while those derived from female water turnover were significantly lower and more variable. On average, mice at 30degreesC exported significantly less energy as milk (87.7 kJ day(-1)) than mice at 21degreesC (166.7 kJ day(-1)) and 8degreesC (288.0 kJ day(-1)). This reduction in milk energy output at 30degreesC was caused by a significant decline in both milk flow (20.0 g day(-1), 12.9 g day(-1) and 8.5 g day(-1) at 8degreesC, 21degreesC and 30degreesC, respectively) and gross energy content of milk (14.6 kJ g(-1), 13.1 kJ g(-1) and 10.5 kJ g(-1) at 8degreesC, 21degreesC and 30degreesC, respectively). Milk produced at 30'C contained significantly less total solids (34.4%) than milk at 21degreesC (40.9%) and 8degreesC (41.5%) and significantly less fat (20.0%) than milk at 21degreesC (26.4%) and 8degreesC (30.3%). The reduced milk energy output in mice exposed to 30degreesC, paralleled by their reduced food intake and low reproductive output, argues against the peripheral limitation hypothesis and provides strong support for the heat dissipation limit hypothesis.

KW - doubly labelled water

KW - daily energy expenditure

KW - water turnover

KW - water balance

KW - milk composition

KW - peripheral limit

KW - heat dissipation limit

KW - laboratory mouse

KW - Mus musculus

KW - RATIO MASS-SPECTROMETRY

KW - MOTHER-YOUNG CONTACT

KW - MUS-MUSCULUS

KW - LITTER SIZE

KW - MATERNAL-BEHAVIOR

KW - METABOLIC-RATE

KW - CONCURRENT PREGNANCY

KW - SIGMODON-HISPIDUS

KW - TRITIATED-WATER

KW - THERMAL CONTROL

U2 - 10.1242/jeb.00675

DO - 10.1242/jeb.00675

M3 - Article

VL - 206

SP - 4267

EP - 4281

JO - Journal of Experimental Biology

JF - Journal of Experimental Biology

SN - 0022-0949

IS - 23

ER -