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Energy Balance in Motion
Klaas R. Westerterp
Department of Human Biology
Maastricht University
Maastricht
The Netherlands
© The Author(s) 2013
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this book shows how energy balance has been in motion over the past four decades.
Preface
vii
Dr. Klaas R. Westerterp is professor of Human
Energetics in the Faculty of Health, Medicine and Life
Sciences at Maastricht University, The Netherlands.
His M.Sc in Biology at the University of Groningen
resulted in a thesis titled ‘The energy budget of the
nesting Starling, a field study’. He received a grant
from the Netherlands Organisation for Scientific
Research (FUNGO, NWO) for his doctorate research
in the Faculty of Mathematics and Natural Sciences
at the University of Groningen. His Ph.D. thesis was
titled ‘How rats economize, energy loss in starva-
tion’. Subsequently, he performed a three-year post-
doc at Stirling University in Scotland supported
by a grant from the Natural Environment Research
Council (NERC), and a two-year postdoc at the University of Groningen and the
Netherlands Institute of Ecology (NIOO, KNAW) with a grant from the Netherlands
Organisation for Scientific Research (BION, NWO) in order to work on flight ener-
getics in birds. In 1982, he became senior lecturer and subsequently full professor
at Maastricht University in the Department of Human Biology. Here, his field of
expertise is energy metabolism, physical activity, food intake and body composition
and energy balance under controlled conditions and in daily life. He was editor in
chief of the Proceedings of the Nutrition Society and he is currently a member of
the Editorial Board of the journal Nutrition and Metabolism (London) and of the
European Journal of Clinical Nutrition, and editor in chief of the European Journal
of Applied Physiology.
About the Author
ix

components like mineral mass
EE Energy expenditure
EG Energy deposited in the body during growth
EI Energy intake
FAO Food and agriculture organisation of the United Nations
FFM Fat-free body mass
FM Fat mass of the body
SMR Sleeping metabolic rate
TEE Total energy expenditure
Tracmor Triaxial accelerometer for movement registration
UNU United Nations University
WHO World Health Organization
Abbreviations
1
Abstract Man is an omnivore and originally met energy requirements by hunt-
ing and gathering. Man evolved in an environment of feast and famine: there were
periods with either a positive or negative energy balance. As an introduction to
human energetics, this book on energy balance in motion starts with a chapter on
animal energetics. How do animals survive and reproduce in an environment with
a variable food supply? The examples on animal energetics illustrate how animals
grow, reproduce and survive periods of starvation. It is an introduction to method-
ology and basic concepts in energetics. Growth efficiency of a wild bird in its nat-
ural environment, here the Starling, is similar to a farm animal like the Domestic
Fowl. Reproductive capacity is set by foraging capacity, determined by food avail-
ability and the capacity parents can produce food to the offspring. Birds feeding
nestlings reach an energy ceiling where daily energy expenditure is four times
resting energy expenditure. Starvation leads to a decrease in energy expenditure,
where the largest saving on energy expenditure can be ascribed to a decrease in
activity energy expenditure.
Keywords  Activity  factor  •  Body  temperature  •  Doubly  labelled  water  method  •

from hatching to fledging in 19–21 days. There is close synchrony in breeding
behaviour within the colony and the adults forage in the same general area allow-
ing several adults to be observed at the same time, thus duplicating observations.
Growth efficiency, the relation between energy intake and the energy deposited in
the body during growth, is assessed by measurement of the separate components of
Fig. 1.1 Five ‘Starling pots’, mounted against the front of a house or pub, with somebody
inspecting from the loft (Etching Claes Janz Visscher. The village party, 1617. With permission: 
Rijksmuseum, Amsterdam)
3
the energy budget: food intake, rejecta,  metabolizable energy, energy expenditure, 
and energy stored in growth (Fig. 1.2). Food provides the organism with energy
for maintenance, temperature regulation activity and growth. Of the total incoming
food energy or gross energy, a part is voided as rejecta including both faeces and
urine. The remainder is commonly termed metabolizable energy. Measurements of 
the separate components of the energy budget of the nestling Starling are described
to illustrate the methodology and general principles of energetics (Westerterp 1973).
Energy intake of the nestlings is measured by taking samples of the meals, and
by counting the total number of meals per day. Meals can be sampled by the col-
lar method. Nestlings are collared with a cotton thread around the neck preventing
swallowing of a meal after feeding. Meals are removed after each parental visit
for later analysis with regard to diet composition and energy content. Depending
on age, nestlings can be collared for periods of one to three hours, between some
hours after sunrise and before sunset so as not to interfere with the very first and
last feedings of the day. The feeding frequency can be determined by automatic
counting of parental visits with an electric contact in the nest entrance. Energy
output in rejecta is measured by taking samples of rejecta, and by observing the
production frequency of rejecta. Faeces and urine are excreted together in mem-
branous sacs, an adaptation enabling the parents to remove them and thus keeping
the nest clean. The collection of samples is a simple matter, especially after the
fifth day when the nestlings automatically produce a faecal sac when handled. The

total or gross energy intake. This is similar to that of 16 % for Domestic Fowl.
Growth efficiency, the relation between energy intake and the energy depos-
ited in the body during growth, does not depend on the pattern of ontogeny but
seems rather a function of the type of food. Higher figures are reported for fish-
eating birds.
Natural selection favours individuals producing the optimal number of fertile
offspring. Starlings habitually lay a clutch of three to seven eggs. The figures as
presented above were mainly from nests with four chicks. The question is whether
the production  of offspring is higher  for a larger brood  size. Is  the food  require-
ment of a chick in a larger brood lower than in a smaller brood? The higher
return in a larger brood could be a reflection of the reduced energy requirement
for maintaining body temperature through huddling. Comparative observations in
broods ranging in size from three to seven chicks showed food intake per gram of 
growth to be optimal for a brood of five (Fig. 1.3). A chick in a brood of five needs
10–20 % less energy to reach a given body weight at fledging than in a brood of
three, a saving probably mainly based on huddling behaviour. This trend does not
continue with a further increase to brood size seven. Here a chick needed 5–10 % 
more energy. Deterioration of the insulative properties of the nest in the big-
gest broods might explain this. Additionally, chicks in bigger broods spend more
energy in activity competing for food. Parents of big broods have to collect more
food and tend to spend less time in nest sanitation. They bring in a higher pro-
portion of leatherjackets and earthworms with higher water content, causing thin
rejecta, which are difficult to remove.
In conclusion, growth efficiency of a wild Starling in its natural environment is
similar to a farm animal like the Domestic Fowl.
5
Foraging Limits in Free Ranging Birds
The number of offspring a bird can produce is mainly a function of food availabil-
ity and foraging capacity. In the Starling it was the availability of spiders, leath-
erjackets, earthworms and beetles, and how much a bird can collect to feed the

2
in body fluids is in isotopic equilibrium with body water
due to exchange in the bicarbonate pools. The hydrogen isotope is lost as water
only. Thus, the washout for the oxygen isotope is faster than for the hydrogen iso-
tope, and the difference represents the CO
2
production. The isotopes of choice are
the stable, heavy, isotopes of oxygen and hydrogen, oxygen-18 (
18
O) and deute-
rium (
2
H), since these avoid the need to use radioactivity and can be safely used
in any organism (Fig. 1.4). Both isotopes naturally occur in drinking water and
thus in body water. Oxygen-18 (
18
O) has eight protons and ten neutrons instead
of the eight protons and eight neutrons found in normal oxygen (
16
O). Deuterium
(
2
H) has one proton and one neutron instead of one neutron for normal hydro-
gen (
1
H). ‘Normal’ water consists largely of the lighter isotopes
1
H and
16
O, the

2
18
O
2
H
18
O
H
2
18
O CO
18
O
2
HHO
K
2
r H
2
O
K
18
r CO
2
+r H
2
O
K
18
– K

the elimination rate of
18
O (K
18
) is a measure for rH
2
O plus carbon dioxide production (rCO
2
),
and rCO
2
= K
18
−K
2
7
Martins (Delichon urbica). Hirundines can stay on the wing day round, where they
feed on flying insects. The most extreme example is the Swift (Apus apus), it only
comes down to breed. Then, they occupy a hole in a steep cliff, or nowadays often
in high buildings. To get again on wing, they need a free fall of some meters, as
the legs are not strong enough to take off from the ground. A grounded swift dies
from starvation.
Here, the main example of free ranging birds reaching foraging limits is the
House Martin. Energy expenditure in free ranging adult House Martins was meas-
ured while they were feeding nestlings. Observations covered three subsequent
years in a colony of some 20 nests at a farm where food supply was monitored
continuously with a suction trap for insects at the same height as foraging House
Martins of 10–15 m.
Measuring energy expenditure with doubly labelled water required capturing
birds at two time points, initially to apply the labelled water and measure the sub-

tenance, food processing and physical activity. For animals like nestlings, there
is an additional component for growth. The activity component is the most vari-
able. Comparison between species requires a figure without dimension, or units.
As such, total expenditure in kJ/day can be divided by resting energy expenditure
in kJ/day. Resting energy expenditure of a specific animal is determined by body
size  and  composition,  age,  gender  and  body  temperature.  Dividing  total  energy 
expenditure by resting energy expenditure adjusts for specific subject characteris-
tics. It results in a dimension less figure allowing for comparison of activity levels
between species, also species differing in size. A larger animal has higher resting 
energy expenditure than a smaller animal. Total energy expenditure is higher as
well, and divided by resting energy expenditure might result in a comparable activ-
ity level to a smaller animal. Thus, the activity level of modern man was observed
to be in line with the activity level of a mammal living in the wild (Chap. 8).
The first year of the study, energy expenditure in adult House Martins that were
feeding their nestlings was 2.9 times resting energy expenditure. The two subse-
quent years, it was clearly higher with an average value of 3.9 times resting energy
expenditure. The first year, the breeding success in the colony was below average.
It was a wet summer with temperatures below average and few insects. Food avail-
ability as measured with the suction trap increased gradually during the breeding
season from May to September but was systematically nearly 50 % lower in the
first year compared to the two following years. Thus, the performance of a bird is a
function of food availability. The upper limit of energy expenditure, reached during
the maximum feeding rate, is around four times resting energy expenditure. The
activity factor of four seems to be a ceiling value (Bryant and Westerterp 1980).
Subsequent observations in nestling feeding Swallows and Sand Martins
resulted in values of 3.9 and 4.3 times resting energy expenditure, respectively
(Westerterp and Bryant 1984). It confirms the energetic ceiling is reached at an
activity factor of four. Subsequent observations in nestling feeding Starlings
resulted in activity factors ranging from 3.2 to 4.3 (Westerterp and Drent 1985).
The value of the activity factor in Starlings varied with the daily flight time.

calorimetry. During food deprivation, using body reserves covers energy expendi-
ture, and animals lose weight. A 300-g rat lost 100-g body weight over 11 days
without food. Energy expenditure over the last two days of the 11-day depriva-
tion interval was only 0.8 W. Here, energy expenditure was calculated from the
difference in energy content of the body of sacrificed animals after nine and
11 days food deprivation. Thus, reducing intake reduces energy expenditure. In
the extreme situation of complete food deprivation, energy expenditure went down
more than 50 %, from 2.0 to 0.8 W, allowing rats to survive twice as long without
food.
There is a classical experiment on the effect of semi-starvation in normal-weight
men with similar results, the so-called Minnesota Experiment (Keys et al. 1950).
It was initiated to determine the effects of relief feeding, necessitated by the fam-
ine in occupied areas of Europe during World War II. The subjects were volunteers
recruited from camps of conscientious objectors. They stayed in the laboratory for
a 12-week baseline period, 24-weeks of semi-starvation, and the first 12-weeks of
rehabilitation. The weight maintenance diet of 14.6 MJ/d in the baseline period was
reduced to 6.6 MJ/d during semi-starvation. In the 24 weeks of semi-starvation,
body weight went down from an average of 69 to 53 kg. At the end of the 24-week
interval, subjects reached a new energy balance as body weight levelled off at
the lower value (Fig. 1.6). Energy expenditure equalled energy intake, i.e. energy
expenditure went down from 14.6 to 6.6 MJ/d, a reduction of 55 %.
Foraging Limits in Free Ranging Birds
10
1 Introduction, Energy Balance in Animals
Mechanisms causing the adaptation of energy expenditure to food deprivation
were studied by measuring oxygen consumption and carbon dioxide production in
rats (6). The rats were housed individually in metabolic cages (Fig. 1.7). The cages
were airtight except for an inlet and outlet for ventilation and measurement of the
gas exchange. Energy expenditure is calculated minute by minute from oxygen
consumption and carbon dioxide production. In combination with measurement of

covered  by  mobilizing  energy  from  body  stores.  Mobilizing  energy  from  body 
stores instead of food consumed also saves on energy costs associated with food
processing like waste production as faeces and urine. Energy expenditure for
food processing is a function of the quantity of food consumed. It is a fraction
of energy intake. Energy expenditure for food processing is 10 %, for a rat on a
Fig. 1.7 The metabolic cage
How Rats Economize, Energy Loss in Starvation
12
1 Introduction, Energy Balance in Animals
diet of standard laboratory food. Thus, when intake matches expenditure, energy
expenditure for food processing is 10 % of total energy expenditure. Energy
expenditure decreases by 10 % when a rat stops eating. This is the same for man,
as described in Chap. 5.
Activity energy expenditure was calculated as total energy expenditure minus
the sum of energy expenditure for food processing and resting energy expenditure.
In the baseline situation, before food deprivation, total energy expenditure was
2 W, resting energy expenditure 1.5 W, expenditure for food processing 10 % of 2
or 0.2 W, and activity energy expenditure the remaining 0.3 W. After 11 days food
deprivation, total energy expenditure was 0.8 W, resting energy expenditure 0.7 W,
expenditure for food processing 0 W, and activity energy expenditure the remain-
ing 0.1 W. Activities performed by the rats, as monitored with a radar system,
went down by about half. Animals moved less and more slowly. The more than
50 % decrease of activity energy expenditure, from 0.3 to 0.1 W or to one third of
the initial value, is also caused by body weight loss. Weight bearing activities take
less energy when body weight has gone down.
Summarizing,  energy  expenditure  of  a  300-g  laboratory  rat  was  2  W  under
ad libitum food conditions. Food deprivation of 11 days led to a decreased
body weight of 200 g and decreased total energy expenditure to 0.8 W. Resting
energy expenditure decreased from 1.5 to 0.7 W. Expenditure for food processing
decreased from 0.2 to 0.0 W, and activity energy expenditure decreased from 0.3

developed for the assessment of the activity pattern under daily living conditions.
With the methodology, new insights were acquired in energy balance and physical
activity in man. In the last chapter, evidence from research in animals and man is
combined under the title ‘Modern man in line with wild mammals’.
How Rats Economize, Energy Loss in Starvation
15
Abstract Energy balance in animals and man is a balance between
energy intake and energy expenditure for body functions and physical activ-
ity. Energy expenditure determines energy requirement. Energy requirement is
met by energy intake. When energy intake does not match energy requirement,
there is a misbalance, caused by intake that is either too high or too low. When
intake exceeds expenditure, there is a positive energy balance and excess energy
is stored in body reserves. When energy intake does not meet expenditure, energy
is mobilized from body reserves. Both result in a change of body weight and body
composition. This chapter firstly describes the assessment of energy expenditure
in man, based on the methodology as described for animals in the foregoing chap-
ter. Subsequent sections describe assessment of physical activity, food intake and
body composition, resulting in the assessment of energy and macronutrient bal-
ance. The methodology forms the basis for the insights as described in the follow-
ing chapters on regulation of energy balance as a function of behaviour, growth,
disease, and ageing. Energy balance can be derived from the measurement of
energy expenditure, food intake, and body composition. The indicated method
for the measurement of energy expenditure is indirect calorimetry via a venti-
lated hood, respiration chamber and with the doubly labelled water method. Food
intake is usually assessed with self-report like a dietary recall or a dietary record.
Self reported food intake has important limitations and the validity is insufficient
for research purposes. Body composition can be calculated from body weight
and body volume or total body water. At a negative or positive energy balance,
the deficit or excess energy is largely mobilised or stored as body fat. The best
long term indicator for energy balance over weeks and months is body weight and

6
) is oxidised with 6 molecules oxygen (O
2
) to 6 
molecules of carbon dioxide (CO
2
) and 6 molecules of water (H
2
O):
In grams, 180 g glucose (one molecule) oxidize with 192 g oxygen to produce 
264 g carbon dioxide, 108 g water, and energy. Oxidizing one molecule of glucose 
provides 3 MJ energy and thus,  the  energy expenditure of  12  MJ/d  is  covered by 
the oxidation of four molecules glucose. The body weight change due to the dif-
ference between the weight of oxygen consumed and carbon dioxide produced is
(4 × 192) − (4 × 264) = −288 g/day. Water loss through breathing and evapora-
tion via the skin is on average one-third to two-thirds of the average daily water
turnover of 3 l/d, or 1,000–2,000 g/day depending on clothing, ambient temperature 
and humidity. The calculation shows, insensible perspiration is more a measure for
water loss through evaporation than for energy expenditure.
The next development in the assessment of energy expenditure was a calo-
rimeter. A calorimeter is a device for measuring the heat given off by something,
like burning food or faeces in a bomb calorimeter. The first calorimeters for the
measurement of energy expenditure measured the heat given off from an animal.
Lavoisier (Paris, 1780) placed a guinea pig in a wire cage surrounded by chunks 
of ice. As the ice melted from the animal’s body heat, the water collected below
in a container, which could be weighed. The amount of melted water allowed the
calculation of the heat production, 334 J/g. The calorimeter was adiabatic in that 
the outer space, around the ice cavity surrounding the cage, was packed with snow
to maintain a constant temperature around the inner shell, which was filled with
ice. The days when these measurements could be made was limited by the mild

Current Methods
In  indirect  calorimetry  the  energy  production  is  calculated  from  chemical  pro-
cesses. Knowing, for example, that the oxidation of 1 mol glucose requires 6 mol 
oxygen  and produces  6  mol  carbon  dioxide,  6  mol  water  and  3  MJ  energy,  the 
energy production can then be calculated from the oxygen consumption and car-
bon dioxide production. The ratio of oxygen and carbon dioxide varies with the
nutrient oxidised (Table 2.1). Brouwer (1957) drew up a simple formula for calcu-
lating the energy production (kJ), based on the quantities of carbohydrate (C, g), 
protein (P, g) and fat (F, g) oxidized, from oxygen consumption (l), carbon dioxide 
production (l) and urine-nitrogen loss. The principle of the calculation consists of 
three equations with the three measured variables:
Protein  oxidation  (g)  is  calculated  as  6.25  x  urine-nitrogen  (g),  and  subse-
quently oxygen consumption and carbon dioxide production can be corrected for
protein oxidation to enable the calculation of carbohydrate and fat oxidation:
The general formula for the calculation of energy production (E) derived from 
these gures is:
Oxygen consumption
= 0. 829 C + 0. 967 P + 2. 019 F
Carbon dioxide production
= 0. 829 C + 0. 885 P + 1. 427 F
Energy production = 17. 5 C + 18. 1 P + 39. 6 F
C =−2. 97 oxygen consumption + 4. 17 carbon dioxide production − 0. 39 P
F
=
1. 72 oxygen consumption
−
1. 72 carbon dioxide production
−
0. 32 P
E