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RUMINANT
PHYSIOLOGY:
Digestion, Metabolism,
Growth and
Reproduction
Edited by
P.B. Cronjé
CABI Publishing
RUMINANT PHYSIOLOGY
Digestion, Metabolism, Growth and
Reproduction
Dedication
This volume is dedicated to the memory of the late Dr F.M.C. Gilchrist.
RUMINANT PHYSIOLOGY
Digestion, Metabolism, Growth
and Reproduction
Edited by
P.B. Cronjé
Department of Animal and Wildlife Sciences
University of Pretoria
Pretoria
South Africa
Associate Editors
E.A. Boomker
P.H. Henning
W. Schultheiss
J.G. van der Walt
CABI Publishing
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A catalogue record for this book is available from the British Library, London, UK
Library of Congress Cataloging-in-Publication Data
Ruminant physiology : digestion, metabolism, growth, and reproduction / edited by
P. Cronje ; assoc. editors, E.A. Boomker … [et al.].
p. cm.
Includes bibliographical references and index.
ISBN 0-85199-463-6 (alk. paper)
1. Ruminants--Physiology--Congresses. I. Cronjé, P. (Pierre) II. Boomker, E. A.
QL737.U5 R868 2000
571.1¢963- - dc21
ISBN 0 85199 463 6
Typeset in 10/12pt Garamond by Columns Design Ltd, Reading
Printed and bound in the UK by Biddles Ltd, Guildford and King’s Lynn
00–023661
Contents
Contributors
Foreword
Part I Regulation of Feed Intake
1 Integration of Learning and Metabolic Signals into a Theory of
Dietary Choice and Food Intake
J.M. Forbes and F.D. Provenza
2 Mathematical Models of Food Intake and Metabolism in Ruminants
A.W. Illius, N.S. Jessop and M. Gill
3 Control of Salivation and Motility of the Reticulorumen by the Brain
in Sheep
W.L. Grovum and J.S. Gonzalez
Part II Rumen Microbiology and Fermentation
ix
xiii
1
3
21
41
59
4 Molecular Ecology and Diversity in Gut Microbial Ecosystems
R.I. Mackie, R.I. Aminov, B.A. White and C.S. McSweeney
61
5 Microbial Adherence to the Plant Cell Wall and Enzymatic Hydrolysis
C.W. Forsberg, E. Forano and A. Chesson
79
6 The Microbial Ecology and Physiology of Ruminal Nitrogen Metabolism
M. Morrison
99
Part III Nutrient Absorption and Splanchnic Metabolism
7 Tissue, Cellular and Molecular Aspects of Peptide Absorption and
Utilization
K.E. Webb, Jr
115
117
v
vi
Contents
8 Influence of Gastrointestinal Metabolism on Substrate Supply to the Liver
C.J. Seal and D.S. Parker
131
9 The Liver: Integrator of Nitrogen Metabolism
G.E. Lobley, G.D. Milano and J.G. van der Walt
149
Part IV Tissue Maintenance and Utilization of Endogenous
Body Reserves
169
10 Adipose Tissue: Beyond an Energy Reserve
R.G. Vernon and K.L. Houseknecht
171
11 Regulation of Growth and Metabolism During Postnatal Development
B.H. Breier, M.H. Oliver and B.W. Gallaher
187
12 Direct Effects of Photoperiod on Lipid Metabolism, Leptin Synthesis
and Milk Secretion in Adult Sheep
Y. Chilliard and F. Bocquier
205
Part V Tissue Growth
225
13 Muscle Growth and Genetic Regulation
J.J. Bass, M. Sharma, J. Oldham and R. Kambadur
227
14 Control and Manipulation of Hyperplasia and Hypertrophy in
Muscle Tissue
P.J. Buttery, J.M. Brameld and J.M. Dawson
237
15 Regulation of Protein Synthesis for Wool Growth
N.R. Adams, S. Liu and D.G. Masters
255
Part VI Reproduction, Pregnancy and Lactation
273
16 Regulation of Macronutrient Partitioning between Maternal and
Conceptus Tissues in the Pregnant Ruminant
A.W. Bell and R.A. Ehrhardt
275
17 The Thermal Physiology of the Ruminant Fetus
H. Laburn, A. Faurie and D. Mitchell
295
18 Regulation of Nutrient Partitioning During Lactation: Homeostasis
and Homeorhesis Revisited
D.E. Bauman
311
19 The Insulin-like Growth Factor (IGF) System in the Mammary Gland:
Role for IGFBP-3 Binding Protein
C.R. Baumrucker
329
20 Integrating the Effects of Genotype and Nutrition on Utilization of
Body Reserves During Lactation of Dairy Cattle
J.P. McNamara
353
Contents
vii
Part VII Ruminant Physiology and Genetics
371
21 Genetic Manipulation of Ruminant Biochemistry and Physiology for
Improved Productivity: Current Status and Future Potential
K.A. Ward
373
22 Genetics of Rumen Microorganisms: Gene Transfer, Genetic Analysis
and Strain Manipulation
H.J. Flint and K.P. Scott
389
23 Nutrient–Gene Interactions: Future Potential and Applications
P.B. Cronjé
409
Part VIII Host Resistance to Parasites and Pathogens
423
24 Host Resistance to Gastrointestinal Parasites of Sheep
S.J. McClure, D.L. Emery and J.W. Steel
425
25 Host Resistance to Fleece Rot and Blowfly Strike
I.G. Colditz and R.L. Tellam
437
26 Host Resistance to Mastitis
K. Persson Waller
449
Index
463
Contributors
N.R. Adams, CSIRO Division of Animal Production and CRC for Premium Quality
Wool, Wembley, 6014 Western Australia
R.I. Aminov, Department of Animal Sciences and Division of Nutritional Sciences,
University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA
J.J. Bass, AgResearch, Ruakura Agricultural Research Centre, Private Bag 3123, Hamilton,
New Zealand
D.E. Bauman, Department of Animal Science, Cornell University, Ithaca, NY 14853,
USA
C.R. Baumrucker, Department of Dairy and Animal Science, Penn State University, 302
Henning Building, University Park, PA 16802, USA
A.W. Bell, Department of Animal Science, Cornell University, Ithaca, NY 14853, USA
F. Bocquier, Adipose Tissue and Milk Lipids Team, Herbivore Research Unit, INRATheix, 63122 St Genès Champanelle, France
J.M. Brameld, Division of Nutritional Biochemistry, School of Biological Sciences,
University of Nottingham, Sutton Bonington Campus, Loughborough, Leicestershire
LEI2 5RD, UK
B.H. Breier, Research Centre for Developmental Medicine and Biology, Faculty of
Medicine and Health Science, University of Auckland, Private Bag 92019, Auckland,
New Zealand
P.J. Buttery, Division of Nutritional Biochemistry, School of Biological Sciences, University
of Nottingham, Sutton Bonington Campus, Loughborough, Leicestershire LE12 5RD,
UK
A. Chesson, Rowett Research Institute, Greenburn Road, Bucksburn, Aberdeen AB21 9SB,
UK
Y. Chilliard, Adipose Tissue and Milk Lipids Team, Herbivore Research Unit, INRATheix, 63122 St Genès Champanelle, France
I.G. Colditz, CSIRO Animal Production, Pastoral Research Laboratory, Armidale, NSW
2350, Australia
ix
x
Contributors
P.B. Cronjé, Department of Animal and Wildlife Sciences, University of Pretoria, Pretoria
0002, South Africa
J.M. Dawson, Division of Nutritional Biochemistry, School of Biological Sciences,
University of Nottingham, Sutton Bonington Campus, Loughborough, Leicestershire
LE12 5RD, UK
R.A. Ehrhardt, Department of Animal Science, Cornell University, Ithaca, NY 14853,
USA
D.L. Emery, CSIRO Animal Production, McMaster Laboratory, Prospect, NSW 2148,
Australia
A. Faurie, Department of Physiology and Brain Function Research Unit, University of the
Witwatersrand, 7 York Road, Parktown, Johannesburg 2193, South Africa
H.J. Flint, Rowett Research Institute, Greenburn Road, Bucksburn, Aberdeen AB21 9SB,
UK
E. Forano, Laboratoire de Microbiologie, INRA CR de Clermont-Ferrand – Theix, 63122
St Genès Champanelle, France
J.M. Forbes, Centre for Animal Sciences, Leeds Institute of Biotechnology and Agriculture,
University of Leeds, Leeds LS2 9JT, UK
C.W. Forsberg, Department of Microbiology, University of Guelph, Guelph, Ontario
N1G 2W1, Canada
B.W. Gallaher, Research Centre for Developmental Medicine and Biology, Faculty of
Medicine and Health Science, University of Auckland, Private Bag 92019, Auckland,
New Zealand
M. Gill, NR International, Central Avenue, Chatham Maritime, Kent ME4 4TB, UK
J.S. Gonzalez, Department of Animal Production, University of Leon, 24071 Leon, Spain
W.L. Grovum, Department of Biomedical Sciences, Ontario Veterinary College, University
of Guelph, Guelph, Ontario, N1G 2W1, Canada
K.L. Houseknecht, Animal Health Drug Discovery, Pfizer Inc., Groton, CT 063408002, USA
A.W. Illius, Division of Biological Sciences, University of Edinburgh, West Mains Road,
Edinburgh EH9 3JT, UK
N.S. Jessop, Division of Biological Sciences, University of Edinburgh, West Mains Road,
Edinburgh EH9 3JT, UK
R. Kambadur, AgResearch, Ruakura Agricultural Research Centre, Private Bag 3123,
Hamilton, New Zealand
H. Laburn, Department of Physiology and Brain Function Research Unit, University of
the Witwatersrand, 7 York Road, Parktown, Johannesburg 2193, South Africa
S. Liu, CSIRO Division of Animal Production and CRC for Premium Quality Wool,
Wembley, 6014 Western Australia
G.E. Lobley, Rowett Research Institute, Greenburn Road, Bucksburn, Aberdeen AB21
9SB, UK
R.I. Mackie, Department of Animal Sciences and Division of Nutritional Sciences,
University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA
D.G. Masters, CSIRO Division of Animal Production and CRC for Premium Quality
Wool, Wembley, 6014 Western Australia
S.J. McClure, CSIRO Animal Production, McMaster Laboratory, Prospect, NSW 2148,
Australia
J.P. McNamara, Department of Animal Sciences, 233 Clark Hall, Washington State
University, PO Box 646351, Pullman, WA 99164-6351, USA
Contributors
xi
C.S. McSweeney, CSIRO Tropical Agriculture, Long Pocket Laboratory, Indooroopilly,
Queensland 4068, Australia
G.D. Milano, Departamento de Fisiopatologia, Facultad de Ciencias Veterinarias UNCPBA, Campus Iniversitario, Paraje Arroyo Seco (7000) Tandil, Argentina
D. Mitchell, Department of Physiology and Brain Function Research Unit, University of
the Witwatersrand, 7 York Road, Parktown, Johannesburg 2193, South Africa
M. Morrison, Department of Animal Science, School of Biological Sciences and Center for
Biotechnology, University of Nebraska, Lincoln, NE 68583-0908, USA
J. Oldham, AgResearch, Ruakura Agricultural Research Centre, Private Bag 3123,
Hamilton, New Zealand
M.H. Oliver, Research Centre for Developmental Medicine and Biology, Faculty of
Medicine and Health Science, University of Auckland, Private Bag 92019, Auckland,
New Zealand
D.S. Parker, Department of Biological and Nutritional Sciences, Faculty of Agriculture
and Biological Science, University of Newcastle upon Tyne, Newcastle upon Tyne
NE1 7RU, UK: present address; Novius Europe s.a./n.v., Rue Gulledellestraat 94,
B-1200 Brussels, Belgium
K. Persson Waller, Swedish University of Agricultural Sciences, Faculty of Veterinary
Medicine, Department of Obstetrics and Gynaecology, P0 Box 7039 Uppsala, S-750
07 Sweden
F.D. Provenza, Department of Rangeland Resources, Utah State University, Logan, Utah
84322–5230, USA
K.P. Scott, Rowett Research Institute, Greenburn Road, Bucksburn, Aberdeen AB21 9SB,
UK
C.J. Seal, Department of Biological and Nutritional Sciences, Faculty of Agriculture and
Biological Science, University of Newcastle upon Tyne, Newcastle upon Tyne NE1
7RU, UK
M. Sharma, AgResearch, Ruakura Agricultural Research Centre, Private Bag 3123,
Hamilton, New Zealand
J.W. Steel, CSIRO Animal Production, McMaster Laboratory, Prospect, NSW 2148,
Australia
R.L. Tellam, CSIRO Tropical Agriculture, Longpocket Laboratory, Indooroopilly,
Queensland 4068, Australia
R.G. Vernon, Hannah Research Institute, Ayr KA6 5HL, UK
J.G. van der Walt, Department of Veterinary Physiology, Faculty of Veterinary Science,
Private Bag X04, Onderstepoort 0110, South Africa
K.A. Ward, CSIRO Animal Production, LB1, Delivery Centre, Blacktown, NSW 2148
Australia
B.A. White, Department of Animal Sciences and Division of Nutritional Sciences,
University of Illinois at Urbana-Champaign, 1207 W. Gregory Drive, Urbana, IL
61801, USA
K.E. Webb, Jr, Department of Animal and Poultry Sciences, Virginia Polytechnic Institute
and State University, Blacksburg, VA 24061-0306, USA
Foreword
The IX International Symposium on Ruminant Physiology was held in Pretoria, South
Africa, during October 1999, and followed the traditions set by the previous meetings
held in Nottingham (1960), Ames (1965), Cambridge (1969), Sydney (1974),
Clermont-Ferrand (1979), Banff (1984), Sendai (1989) and Willingen (1994). The
event was attended by 250 delegates from 28 countries. The plenary papers are published in this volume, and the 242 poster communications were published in the South
African Journal of Animal Science.
The central issue that emerged from this symposium was that new technologies,
notably molecular biology and modelling, have become important research tools for
the physiologist. It was, however, apparent that more research is needed to relate
advances in these technologies and in our understanding of fundamental physiological
mechanisms to the solution of practical problems. The papers reiterated that animals,
as free-living organisms, have an inherent ability to select for different nutrients and to
control nutrient partitioning between different tissues, but that this can be modified
and manipulated by human intervention. The important question of whether tissues
are in competition for nutrients or whether the partitioning of nutrients is an integral
part of coordinating the optimal use of nutrients will, no doubt, elicit much new
research. There has been a clear shift from the traditional nutritional input–fermentation approach to rumen microbiology towards a molecular ecology approach, and a
new horizon has appeared with regard to our quest to understand host–parasite relationships.
Thanks are expressed to the members of the organizing committee, sub-committees and the many willing helpers. The sponsors deserve a special mention: their contributions made it possible to give financial support to deserving delegates, to publish the
poster abstracts and to produce this volume.
An international guiding committee was constituted to consider the future of the
ISRP and the offers to host the X ISRP. The members of the committee are: Dr John
Bass, Prof. Alan Bell, Prof. Giuseppi Bertoni, Prof. Peter Buttery, Prof. Norman Casey
(convenor), Dr Yves Chilliard, Prof. Pierre Cronjé, Prof. Jong Ha, Dr Jan Hofmeyr
xiv
Foreword
(WAAP Vice-president), Dr Heinz Meissner, Prof. Y Obara and Prof. Wolfgang von
Engelhardt. The committee formulated a number of guiding principles for future ISRP
meetings. These are: that the meeting should retain the character of previous symposia;
that the focus should remain on the physiology of livestock, reviewing advances over
the previous 5 years and setting directions for the next period; that comparative physiology and the impact of advances in physiology on products and sensitive consumer
issues are important; that the venue for meetings should be situated where there is a
core of established ruminant physiologists who could organize the symposium and, in
particular, attend to the scientific programme and publish the proceedings; that the
symposium should be easily accessible to young scientists and scientifically developing
communities. After considering several invitations and taking the principles agreed
upon into consideration, the hosting of the X ISRP was awarded to Denmark.
Norman H. Casey
(Chairman: Organizing Committee of the IX ISRP)
I
Regulation of Feed Intake
1
Integration of Learning and
Metabolic Signals into a Theory of
Dietary Choice and Food Intake
J.M. FORBES1 AND F.D. PROVENZA2
1Centre
for Animal Sciences, Leeds Institute of Biotechnology and Agriculture,
University of Leeds, Leeds, UK; 2Department of Rangeland Resources,
Utah State University, Logan, Utah, USA
Introduction
The challenge of understanding how diet selection and food intake are controlled is
one that occupies an important place in the fields of nutrition, physiology and psychology. In the case of ruminant animals there are two special reasons for our interest in the
subject: the complexities of the digestive system and consequent metabolic peculiarities; and the agricultural and ecological importance of the sub-order. Despite several
decades of intensive study there is still no consensus on how intake is controlled
(Fisher, 1996), nor is there agreement about the way in which animals determine which
food(s) to eat when a choice is available. The past few years have seen the publication of
sufficient new evidence to allow us to advance our hypotheses about the control of food
intake and diet selection.
Firstly we review advances in our understanding of the role of learning in determining preferences and aversions for foods by ruminants; we then summarize the ways
in which the central nervous system (CNS) is informed about digestive and metabolic
processes; discuss the day-to-day variation in intake as an enabling factor in the linking
of learning with the physiological consequences of eating; and finally propose how
learning and metabolic information are brought together to provide testable hypotheses
of the control of diet selection and voluntary food intake. We take it as axiomatic that
long- and short-term regulation of intake are interwoven and do not attempt to differentiate between the two.
Learned associations between the sensory properties of a food and the
metabolic consequences of eating that food
This section presents recent evidence to reinforce the concept that ruminant animals
learn to associate the post-ingestive consequences of eating a food with the sensory
properties of that food and that they use such conditioned preferences and aversions to
direct their selection between foods.
© CAB International 2000. Ruminant Physiology: Digestion, Metabolism,
Growth and Reproduction (ed. P.B. Cronjé)
3
4
J.M. Forbes and F.D. Provenza
Adaptation of choices of foods in order to avoid excessive intakes of toxins and to
ensure adequate intakes of essential nutrients
In establishing that ruminants can learn to choose between foods to avoid toxicity it is
logical to start with an overtly toxic substance, i.e. LiCl, which has been widely used in
conditioned aversion studies. Sheep find LiCl, injected or in the food, to be unpleasant
(Dutoit et al., 1991) as it induces a conditioned taste aversion, the strength of which is
proportional to the dose administered. Feeding neophobia also increases as a function
of the LiCl dose associated with the last novel food encountered. When sheep and
goats were offered food containing 2% LiCl, their daily intake after the third day fluctuated about a level that resulted in a LiCl dose of 39 mg kg1 for sheep and
27 mg kg1 for goats, i.e. similar to the doses causing mild aversion in rats and human
beings.
The word ‘toxin’ is usually reserved for a substance that causes obvious signs of discomfort or distress. However, all dietary components are capable of acting as toxins, if
present in great excess over requirements. Even a mild excess can generate aversion as
toxins do not have to be consciously sensed in order for their effects to be relayed to the
CNS and to have the potential to influence learned aversion. Equally, a deficiency of an
essential nutrient can form the unconditioned stimulus for the development of food
aversions. An example is provided by Hills et al. (1998) in which sheep either replete or
depleted in sulphur were offered foods with different contents of sulphur. Replete
sheep given high- and low-sulphur foods initially ate at random but within 2 days
reduced the proportion of the high-sulphur food to achieve a sulphur concentration in
the total diet very close to that thought to be optimal. Conversely, depleted sheep initially ate a high proportion of the high-sulphur food but later reduced the sulphur content chosen until it stabilized at the optimum level.
Other examples of non-random diet selection in order to control the intake of a
‘nutrient’ are: protein (Kyriazakis and Oldham, 1993), sodium (Denton, 1982), energy
(Burritt and Provenza, 1992) and oxalic acid (Kyriazakis et al., 1998).
Ruminants learn preferences for a food flavour associated with infusions that correct
deficiency; the same nutrient given to excess leads to avoidance of the associated
flavour
In order to demonstrate unequivocally that such appetites are dependent on learned
associations between the sensory properties of the foods and their nutritive value it is
necessary to divorce the flavour of the food from its yield of nutrients. This can be done
by offering animals a distinctive food and at the same time giving a nutrient by a route
that bypasses the mouth, usually intraruminal infusion. In one such experiment with
lambs (Villalba and Provenza, 1997a) one flavour was paired with rumen infusion of
starch (2.5–9.4% of daily digestible energy (DE) intake) and another flavour with
control. Subsequent preference was strongly for the starch-paired flavour, even 8
weeks after infusions had stopped. Starch is rapidly fermented to volatile fatty acids,
predominantly propionic, in the rumen. Propionate absorption is likely to be insufficient for glucose synthesis in straw-fed animals so the hypothesis was tested that the
supply of this limiting nutrient would induce a preference for the flavour of food eaten
Integration of Learning and Metabolic Signals
5
during supplementation (Villalba and Provenza, 1996). Even though the propionate
supplied was equivalent to no more than 1.4% of the daily metabolizable energy (ME)
intake, after 8 days of conditioning the sheep had developed a strong preference for
food flavoured with that flavour given during supplementation. It was shown that the
preference was induced by the propionate rather than the sodium or osmolality of the
infusions (Villalba and Provenza, 1996; Villalba and Provenza, 1997b).
We can conclude that a single nutrient can induce a preference or an aversion to
the flavour it was paired with during training, depending on the rate of administration
in relation to the animal’s requirements.
Continuum from deficiency, through sufficiency, to excess for each nutrient
Several recent experiments have addressed the question: Do ruminants prefer a flavour
associated with an intermediate, optimum content of a nutrient over flavours associated
with the same nutrient present in excess or deficiency?
Arsenos and Kyriazakis (1999) have demonstrated a continuum between conditioned preferences and aversions in sheep to flavoured foods associated with doses of
casein from 9 to 53 g given by gavage. The lower two doses led to conditioned flavour
preferences, presumably because they alleviated a N deficiency, while the higher two
doses led to conditioned flavour aversions, presumably being sensed as toxic overdoses.
The authors observe that the existence of a continuum of flavour preferences and aversions created by different amounts of the same nutrient source could be the basis of
how ruminants select a diet which meets their nutrient requirement at a particular
point in time.
Sheep preferred a flavour paired with intraruminal administration of acetate at several doses (4, 8 or 12% of daily DE intake) or propionate (4% of daily DE intake), but
became averse to a flavour paired with higher doses of propionate (12% of daily DE
intake). This again suggests a role for learning about different concentrations of
metabolites in the control of diet selection (Villalba and Provenza, 1997b).
There is thus evidence that a food that the animal believes alleviates a deficiency
becomes preferred over other foods, while one thought to be excessive in the same
nutrient becomes aversive. Under natural conditions such responses would lead to
‘nutritional wisdom’, i.e. eating a mixture of foods which most closely meets the animal’s nutrient requirements.
Ratio in which nutrients are supplied by different foods affects dietary choice
There are some situations in which the ratio of nutrients being absorbed from the digestive tract is such as to induce metabolic imbalance. When acetate and propionate were
infused together into the rumen of sheep, conditioned preferences were demonstrated
for the associated flavoured wheat straw but the preference was greater when the ratio of
acetate:propionate in the infusate was 55:45 than when it was 75:25 (Villalba and
Provenza, 1997b). It is likely that straw-fed lambs, with a high ratio of acetate:propionate produced by normal ruminal fermentation, would be deficient in glucose and this
would be better alleviated by the mixture with the higher proportion of propionate.