Phylogenetic constraints on digesta separation: Variation in fluid throughput in the digestive tract in mammalian herbivores

TLDR: The results indicate that MRT(solute)GIT and the degree of digesta washing are related to digestion type, whereas variation in MRT('fluid passage')GIT is influenced mainly by effects of body mass and food intake, and fluid throughput and digestiona washing emerge as important correlates of digestive anatomy.

Abstract: The relevance of the mean retention time (MRT) of particles through the gastrointestinal tract (GIT) is well understood and MRTparticleGIT is an important parameter in digestion models. Solute markers have been used to estimate MRTsoluteGIT (or ‘fluid passage’) in animals, but the relevance of this measure is less evident and is usually sought in its relation to MRTparticleGIT. The ratio between the two measures indicates the degree of ‘digesta washing’, with little washing occurring at ratios of 1, aborad washing at ratios N1 (where the solute marker travels faster than the particle marker), and orad (retrograde) washing at ratios b1 (where the solute marker travels slower than the particle marker). We analysed digesta washing in a dataset of 98 mammalian species including man of different digestion types (caecum, colon and nonruminant foregut fermenters, and ruminants), controlling for phylogeny; a subset of 72 species allowed testing for the influence of food intake level. The results indicate that MRTsoluteGIT and the degree of digesta washing are related to digestion type, whereas variation in MRTparticleGIT is influenced mainly by effects of body mass and food intake. Thus, fluid throughput and digesta washing emerge as important correlates of digestive anatomy. Most importantly, primates appear constrained to little digesta washing compared to non-primate mammalian herbivores, regardless of their digestion type. These results may help explain the absence of primates from certain herbivore niches and represent a drastic example of a physiologic limitation in a phylogenetic group. Moreexperimental research is required to illuminate relative benefits and costs of digesta washing.

Figures

Table 4. Results of General Linear Models, either calculated conventionally (conv) or using Phylogenetic Generalized Linear Least-Squares (PGLS; 836 used to correct for non-independence of data originating from species related to each other by evolutionary ancestry), relating passage parameters 837 (mean retention time MRT of particles or solutes [in h], or their ratio SF) to log-transformed body mass (BM [kg]), the relative dry matter intake 838 (rDMI [g kg-0.75 d-1]), or MRTparticles in 37 (a, c) or 16 (b) primate species belonging to one of the three major primate digestion types (caecum 839 fermenter, colon fermenter, nonruminant foregut fermenter), respectively. 840 841

Table 3. Results of General Linear Models, either calculated conventionally (conv) or using Phylogenetic Generalized Linear Least-Squares (PGLS; 826 used to correct for non-independence of data originating from species related to each other by evolutionary ancestry), relating passage parameters 827 (mean retention time MRT of particles or solutes [in h], or their ratio SF) to log-transformed body mass (BM [kg]), the relative dry matter intake 828 (rDMI [g kg-0.75 d-1]), or MRTparticles in 61 (a, c) or 56 (b) non-primate mammal species belonging to one of the four major digestion types (caecum 829 fermenter, colon fermenter, nonruminant foregut fermenter, ruminant), respectively. Differences between the conventional and the PGLS GLM are 830 indicated by grey shading. 831 832

Table 2. Results of General Linear Models relating passage parameters (mean retention time MRT of particles or solutes [in h], or their ratio SF) to 816 log-transformed body mass (BM [kg]), the relative dry matter intake (rDMI [g kg-0.75 d-1]), or MRTparticles in 98 (a, c) or 72 (b) mammal species, 817 respectively, using “being a primate” and the digestion type (caecum fermenter, colon fermenter, nonruminant foregut fermenter, ruminant) as 818 cofactors as well as the interaction of the two cofactors. A significant interaction indicates different effects between the digestion types in primates 819

Table 1. Datasets used in this study. Species are ordered as in the phylogenetic tree (Fig. 1). GIT denotes digestion type (1 caecum fermenter, 2 810 colon fermenter, 3 nonruminant foregut fermenter, 4 ruminant); markers include chromium-mordeanted fibre (1), cerium-mordanted fibre (2), 811 phenanthroline-ruthenium chloride (3), cobalt-EDTA (4), chromium-EDTA (5) or polyethylene glycol (6); BM body mass, MRT mean retention 812 time, SF selectivity factor, DMI dry matter intake 813 814

Full text

University of Zurich
Zurich Open Repository and Archive
Winterthurerstr. 190
CH-8057 Zurich
http://www.zora.uzh.ch
Year: 2011
Phylogenetic constraints on digesta separation: Variation in fluid
throughput in the digestive tract in mammalian herbivores
Müller, D W H; Caton, J; Codron, D; Schwarm, A; Lentle, R; Streich, W J; Hummel,
J; Clauss, M
http://www.ncbi.nlm.nih.gov/pubmed/21689778.
Postprint available at:
http://www.zora.uzh.ch
Posted at the Zurich Open Repository and Archive, University of Zurich.
http://www.zora.uzh.ch
Originally published at:
Müller, D W H; Caton, J; Codron, D; Schwarm, A; Lentle, R; Streich, W J; Hummel, J; Clauss, M (2011).
Phylogenetic constraints on digesta separation: Variation in fluid throughput in the digestive tract in mammalian
herbivores. Comparative Biochemistry and Physiology - Part A: Molecular and Integrative Physiology,
160(2):207-220.
http://www.ncbi.nlm.nih.gov/pubmed/21689778.
Postprint available at:
http://www.zora.uzh.ch
Posted at the Zurich Open Repository and Archive, University of Zurich.
http://www.zora.uzh.ch
Originally published at:
Müller, D W H; Caton, J; Codron, D; Schwarm, A; Lentle, R; Streich, W J; Hummel, J; Clauss, M (2011).
Phylogenetic constraints on digesta separation: Variation in fluid throughput in the digestive tract in mammalian
herbivores. Comparative Biochemistry and Physiology - Part A: Molecular and Integrative Physiology,
160(2):207-220.

Phylogenetic constraints on digesta separation: Variation in fluid
throughput in the digestive tract in mammalian herbivores
Abstract
The relevance of the mean retention time (MRT) of particles through the gastrointestinal tract (GIT) is
well understood and MRTparticleGIT is an important parameter in digestion models. Solute markers
have been used to estimate MRTsoluteGIT (or ‘fluid passage') in animals, but the relevance of this
measure is less evident and is usually sought in its relation to MRTparticleGIT. The ratio between the
two measures indicates the degree of ‘digesta washing', with little washing occurring at ratios of 1,
aborad washing at ratios N1 (where the solute marker travels faster than the particle marker), and orad
(retrograde) washing at ratios b1 (where the solute marker travels slower than the particle marker). We
analysed digesta washing in a dataset of 98 mammalian species including man of different digestion
types (caecum, colon and nonruminant foregut fermenters, and ruminants), controlling for phylogeny; a
subset of 72 species allowed testing for the influence of food intake level. The results indicate that
MRTsoluteGIT and the degree of digesta washing are related to digestion type, whereas variation in
MRTparticleGIT is influenced mainly by effects of body mass and food intake. Thus, fluid throughput
and digesta washing emerge as important correlates of digestive anatomy. Most importantly, primates
appear constrained to little digesta washing compared to non-primate mammalian herbivores, regardless
of their digestion type. These results may help explain the absence of primates from certain herbivore
niches and represent a drastic example of a physiologic limitation in a phylogenetic group.
Moreexperimental research is required to illuminate relative benefits and costs of digesta washing.

Phylogenetic constraints on digesta separation: variation in fluid throughput in the 1
digestive tract in mammalian herbivores 2
3
Dennis W.H. Müller
1
, Judith Caton
2
, Daryl Codron
1
, Angela Schwarm
3
, Roger Lentle
4
, W. 4
Jürgen Streich
5
, Jürgen Hummel
6
, Marcus Clauss
1*
5
6
1
Clinic for Zoo Animals, Exotic Pets and Wildlife, Vetsuisse Faculty, University of Zurich, Winterthurerstr. 260, 7
8057 Zurich, Switzerland, dmueller@vetclinics.uzh.ch, dcodron@vetclinics.uzh.ch, 8
mclauss@vetclinics.uzh.ch 9
2
Department of Applied Mathematics, Research School of Physical Science and Engineering, The Australian 10
National University, Canberra, ACT 0200, Australia, judith.caton@anu.edu.au 11
3
Research Unit Nutritional Physiology ‘Oskar Kellner’, Leibniz Institute for Farm Animal Biology (FBN), 12
Wilhelm-Stahl-Allee 2, 18196 Dummerstorf, Germany, schwarm@fbn-dummerstorf.de 13
4
Institute of Food, Nutrition and Human Health, Massey University, R11 2.52, Manawatu, New Zealand, 14
R.G.Lentle@massey.ac.nz 15
5
Leibniz-Institute of Zoo and Wilflife Research (IZW) Berlin, Alfred-Kowalke-Str. 17, 10315 Berlin, Germany, 16
streich@izw-berlin.de 17
6
Institute of Animal Science, University of Bonn, Endenicher Allee 15, 53115 Bonn, Germany, jhum@itw.uni-18
bonn.de 19
20
*to whom correspondence should be addressed 21
22
Running head: Digesta washing 23
24

Abstract 25
The relevance of the mean retention time (MRT) of particles through the gastrointestinal tract 26
(GIT) is well understood and MRT
particle
GIT is an important parameter in digestion models. 27
Solute markers have been used to estimate MRT
solute
GIT (or ‘fluid passage’) in animals, but 28
the relevance of this measure is less evident and is usually sought in its relation to 29
MRT
particle
GIT. The ratio between the two measures indicates the degree of ‘digesta washing’, 30
with little washing occurring at ratios of 1, aborad washing at ratios >1 (where the solute 31
marker travels faster than the particle marker), and orad (retrograde) washing at ratios <1 32
(where the solute marker travels slower than the particle marker). We analysed digesta 33
washing in a dataset of 98 mammalian species including man of different digestion types 34
(caecum, colon and nonruminant foregut fermenters, and ruminants), controlling for 35
phylogeny; a subset of 72 species allowed testing for the influence of food intake level. The 36
results indicate that MRT
solute
GIT and the degree of digesta washing are related to digestion 37
type, whereas variation in MRT
particle
GIT is influenced mainly by effects of body mass and 38
food intake. Thus, fluid throughput and digesta washing emerge as important correlates of 39
digestive anatomy. Most importantly, primates appear constrained to little digesta washing 40
compared to non-primate mammalian herbivores, regardless of their digestion type. These 41
results may help explain the absence of primates from certain herbivore niches and represent a 42
drastic example of a physiologic limitation in a phylogenetic group. More experimental 43
research is required to illuminate relative benefits and costs of digesta washing. 44
45
Key words passage, digestion, fluid, particle, foregut fermenter, hindgut fermenter, ruminant, 46
nonruminant, caecum fermenter 47
48

List of abbreviations 49
BM body mass 50
DMI dry matter intake (also: absolute dry matter intake) 51
rDMI relative dry matter intake (expressed per unit metabolic body weight) 52
GIT gastrointestinal tract 53
GLM general linear model 54
MRT mean retention time 55
MRT
particle
GIT mean retention time of a particle marker in the gastrointestinal tract 56
MRT
solute
GIT mean retention time of a solute marker in the gastrointestinal tract 57
PGLS phylogenetic generalized least-squares 58
SF selectivity factor, the ratio of MRT
particle
/ MRT
solute
59
60
Introduction 61
Digestion is a time-dependent process (Stevens and Hume 1995; Karasov and Martínez del 62
Rio 2007); hence the time that ingested food takes to transit the digestive tract is an important 63
factor in digestive efficiency. At a given level of food intake, the more time is available for 64
digestion, the more complete digestion can be. Therefore, the digesta mean retention time 65
(MRT)
a
is a parameter that is considered crucial in digestive physiology, and that has been 66
measured in vast numbers of digestive studies (Stevens and Hume 1998; Clauss et al. 2007a). 67
Evaluation of MRT is particularly relevant in herbivorous species (Stevens and Hume 1998) 68
because the rate of allo-enzymatic digestion of plant fibre is generally slower than that of the 69
auto-enzymatic digestion of other substrates. MRT is usually assessed by administering 70
markers and measuring their appearance at a given point along the gastrointestinal tract (GIT) 71
e.g. the faeces, or the termination of a particular gut segment (Warner 1981b). Whether a 72
marker used is representative of the whole digesta, or of a relevant fraction of it, is an 73
important consideration in such studies. Commonly, at least two digesta phases are 74
considered separately – the particulate or solid phase, and the fluid or solute phase (Warner 75
1981b). 76
77
a
The terminology associated with measuring the time that digesta is retained in (or in other word: passes
through) the gastrointestinal tract varies. “Mean retention time (MRT [in hours or days])” is an integrated
measure that considers the complete excretion pattern of a digesta fraction; it is often also called “passage time”.
Unfortunately, the term “passage rate” has often been used for the same measure, although a ‘rate’ has the unit
[fraction per unit time] and hence cannot be equated with a data given in [unit time]. “Transit time” is the time of
first marker appearance in the faeces.

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Q1. What contributions have the authors mentioned in the paper "Phylogenetic constraints on digesta separation: variation in fluid throughput in the digestive tract in mammalian herbivores" ?

The relevance of the mean retention time ( MRT ) of particles through the gastrointestinal tract ( GIT ) is well understood and MRTparticleGIT is an important parameter in digestion models. Solute markers have been used to estimate MRTsoluteGIT ( or ‘ fluid passage ' ) in animals, but the relevance of this measure is less evident and is usually sought in its relation to MRTparticleGIT. The ratio between the two measures indicates the degree of ‘ digesta washing ', with little washing occurring at ratios of 1, aborad washing at ratios N1 ( where the solute marker travels faster than the particle marker ), and orad ( retrograde ) washing at ratios b1 ( where the solute marker travels slower than the particle marker ). The results indicate that MRTsoluteGIT and the degree of digesta washing are related to digestion type, whereas variation in MRTparticleGIT is influenced mainly by effects of body mass and food intake. The relevance of the mean retention time ( MRT ) of particles through the gastrointestinal tract 26 ( GIT ) is well understood and MRTparticleGIT is an important parameter in digestion models. 27 Solute markers have been used to estimate MRTsoluteGIT ( or ‘ fluid passage ’ ) in animals, but 28 the relevance of this measure is less evident and is usually sought in its relation to 29 MRTparticleGIT. The ratio between the two measures indicates the degree of ‘ digesta washing ’, 30 with little washing occurring at ratios of 1, aborad washing at ratios > 1 ( where the solute 31 marker travels faster than the particle marker ), and orad ( retrograde ) washing at ratios < 1 32 ( where the solute marker travels slower than the particle marker ). The 36 results indicate that MRTsoluteGIT and the degree of digesta washing are related to digestion 37 type, whereas variation in MRTparticleGIT is influenced mainly by effects of body mass and 38 food intake.