Foregut and hindgut fermenters:

How ruminants chew their way

out of the foregut fermentation
trap
Marcus Clauss
Clinic for Zoo Animals, Exotic Pets and Wildlife, Vetsuisse Faculty, University of
Zurich, Switzerland
Wildlife Digestive Physiology Course Vienna 2009
based on a true story
Digestive adaptations
Digestive adaptations
Digestive adaptations
Digestive adaptations
 What comparative digestive physiology can
offer to domestic ruminant research

• Understanding where ruminants ‘came

from’ in evolutionary terms

from www.orthomam.univ-montp2.fr
 What comparative digestive physiology can
offer to domestic ruminant research

• Understanding where domestic ruminants

‘came from’ among the ruminants

from Agnarsson et al. (2008)

 What comparative digestive physiology can
offer to domestic ruminant research

• Understanding where domestic ruminants

‘came from’ among the ruminants ...

... and where they might

be taken to in the future

from Agnarsson et al. (2008)

Hindgut Fermentation - Caecum

from Stevens & Hume (1995)

Hindgut Fermentation - Colon

from Stevens & Hume (1995)

Hindgut Fermentation - Colon

from Stevens & Hume (1995)

Foregut Fermentation

from Stevens & Hume (1995)

 Foregut Fermentation

Photos A. Schwarm/
M. Clauss
Foregut Fermentation - Ruminant

aus Stevens & Hume (1995)

Photo Llama: A. Riek
Foregut fermentation = Ruminant digestion?
Foregut fermentation = Ruminant digestion?
Foregut vs. Hindgut Fermentation

from Stevens & Hume (1995)

Foregut vs. Hindgut Fermentation

Fermentation
after
enzymatic
digestion and
absorption:

from Stevens & Hume (1995)

Foregut vs. Hindgut Fermentation

Fermentation
after
enzymatic
digestion and
absorption:
‘Loss’ of
bacterial
protein,
bacterial
products (B-
Vitamins?)

from Stevens & Hume (1995)

Foregut vs. Hindgut Fermentation

Fermentation
after
enzymatic
digestion and
absorption:
‘Loss’ of
bacterial
protein,
bacterial
products (B-
Vitamins?)
(coprophagy)

from Stevens & Hume (1995)

Foregut vs. Hindgut Fermentation

Fermentation
after
enzymatic
digestion and
absorption:
‘Loss’ of
bacterial
protein,
bacterial
products (B-
Vitamins?)
(coprophagy)
Use of easily
digestible
substrates

from Stevens & Hume (1995)

 Foregut vs. Hindgut Fermentation

Fermentation Fermentation
prior to after
enzymatic enzymatic
digestion and digestion and
absorption: absorption:
‘Loss’ of
bacterial
protein,
bacterial
products (B-
Vitamins?)
(coprophagy)
Use of easily
digestible
substrates

from Stevens & Hume (1995)

 Foregut vs. Hindgut Fermentation

Fermentation Fermentation
prior to after
enzymatic enzymatic
digestion and digestion and
absorption: absorption:
Use of ‘Loss’ of
bacterial bacterial
protein, protein,
bacterial bacterial
products (B- products (B-
Vitamins) Vitamins?)
(coprophagy)
Use of easily
digestible
substrates

from Stevens & Hume (1995)

 Foregut vs. Hindgut Fermentation

Fermentation Fermentation
prior to after
enzymatic enzymatic
digestion and digestion and
absorption: absorption:
Use of ‘Loss’ of
bacterial bacterial
protein, protein,
bacterial bacterial
products (B- products (B-
Vitamins) Vitamins?)
Bacterial (coprophagy)
detoxification?
Use of easily
digestible
substrates

from Stevens & Hume (1995)

 Foregut vs. Hindgut Fermentation

Fermentation Fermentation
prior to after
enzymatic enzymatic
digestion and digestion and
absorption: absorption:
Use of ‘Loss’ of
bacterial bacterial
protein, protein,
bacterial bacterial
products (B- products (B-
Vitamins) Vitamins?)
Bacterial (coprophagy)
detoxification?
Use of easily
‘Loss’ of easily digestible
digestible substrates
substrates and
bacterial
modification from Stevens & Hume (1995)
Saturation of body fat

from Clauss et al. (2008)

 Foregut vs. Hindgut Fermentation

Bacterially
modified fatty
acids
(e.g. CLA)

from Stevens & Hume (1995)

 Foregut vs. Hindgut Fermentation

Bacterially What about

modified fatty coprophagic
acids small hindgut
fermenters?
(e.g. CLA)

from Stevens & Hume (1995)

 Foregut vs. Hindgut Fermentation

What about
coprophagic
small hindgut
fermenters?

Leiber et al. (2008) from Stevens & Hume (1995)

 Foregut vs. Hindgut Fermentation

Endogenous
nitrogen
products
(urea) can be
N
recycled by
introducing
them into the
fermentation
chamber - use
by microbes -
re-digestion of
N as bacterial
amino acids

from Stevens & Hume (1995)

 Foregut vs. Hindgut Fermentation

Endogenous Urea could be

nitrogen available for
products bacteria in
(urea) can be
N hindgut
recycled by fermenters,
introducing but it would
them into the not be
fermentation recycled
chamber - use
by microbes -
N
re-digestion of
N as bacterial
amino acids

from Stevens & Hume (1995)

 Foregut vs. Hindgut Fermentation

Endogenous In theory, this

nitrogen could be
products possible in
(urea) can be
N coprophagic
recycled by hindgut
introducing fermenters,
them into the too
fermentation
chamber - use
by microbes - N
re-digestion of
N as bacterial
amino acids

from Stevens & Hume (1995)

 Foregut vs. Hindgut Fermentation

Phosphorus is
supplied P
directly to
microbes via
saliva

from Stevens & Hume (1995)

 Foregut vs. Hindgut Fermentation

Phosphorus is In order to
supplied P guarantee
directly to phosphorus
microbes via availability in
saliva the hindgut,
Ca calcium is
actively
absorbed
from ingesta
and excreted
via urine

from Stevens & Hume (1995)

hypothesis by Clauss & Hummel (2008)
 Foregut vs. Hindgut Fermentation

Lysozyme
secretion in
the glandular
stomach (and
ribonuclease in
the
duodenum) as
an example of
convergent
evolution of
enzymes
(for the
digestion of
bacteria)

from Stevens & Hume (1995), Karasov &

Martinez del Rio (2007)
 Foregut vs. Hindgut Fermentation

Lysozyme Intermittent
secretion in colonic
the glandular lysozyme
stomach (and secretion in
ribonuclease in synchrony
the with
duodenum) as caecotroph
an example of formation
convergent
evolution of
enzymes
(for the
digestion of
bacteria)

from Stevens & Hume (1995), Karasov &

Martinez del Rio (2007), Camara & Prieur (1984)
 Foregut vs. Hindgut Fermentation

Lower
bacterial
nitrogen losses
in the faeces?

from Stevens & Hume (1995)

 Foregut vs. Hindgut Fermentation

Lower Higher
bacterial bacterial
nitrogen losses nitrogen
in the faeces? losses in the
faeces?

from Stevens & Hume (1995)

 Foregut vs. Hindgut Fermentation

Lower Lower
bacterial bacterial
nitrogen losses nitrogen
in the faeces? losses in hard
faeces in
coprophagic
hindgut
fermenters
due to
bacterial
accumulation
in
caecotrophs?

from Stevens & Hume (1995)

Metabolic faecal nitrogen in zoo herbivores

from Schwarm et al. (2009)

Metabolic faecal nitrogen in zoo herbivores

from Schwarm et al. (2009)

Foregut vs. Hindgut Fermentation

Ontogenetic
diet shifts are
no problem
because all
ingested
material is
always
digested
enzymatically
first

from Stevens & Hume (1995)

 Foregut vs. Hindgut Fermentation

Ontogenetic Ontogenetic
diet shifting: diet shifts are
animal food no problem
must be because all
directed past ingested
the foregut to material is
prevent mal- always
fermentation! digested
enzymatically
first

from Stevens & Hume (1995)

 Foregut vs. Hindgut Fermentation

Ontogenetic Ontogenetic
diet shifting: diet shifts are
animal food no problem
must be because all
directed past ingested
the foregut to material is
prevent mal- always
fermentation! digested
enzymatically
first

from Stevens & Hume (1995)

 Foregut vs. Hindgut Fermentation

Ontogenetic
diet shifting:
animal food
must be
directed past
the foregut to
prevent mal-
fermentation!

from Stevens & Hume (1995), Moss et al. (2003)

Bypass structures in foregut fermenters

from Langer (1988)

Photos A. Schwarm
Bypass structures in foregut fermenters

Because only a fluid food

can be easily diverted in a
bypass structure, foregut
fermentation might be
primarily limited to
mammals.

from Langer (1988)

Photos A. Schwarm
 Foregut vs. Hindgut Fermentation

Foregut fermentation occurs in just one avian and

no reptilian species.
from Stevens & Hume (1995)
Foregut fermentation = Ruminant digestion?
 Foregut vs. Hindgut Fermentation

Fermentation Fermentation
prior to after
enzymatic enzymatic
digestion and digestion and
absorption: absorption:
particularly
Use of suited for ‘Loss’ of
bacterial bacterial
fibre fermen-
protein, protein,
bacterial tation bacterial
products (B- products (B-
Vitamins) Vitamins?)
Bacterial (coprophagy)
detoxification?
Use of easily
‘Loss’ of easily digestible
digestible substrates
substrates

from Stevens und Hume (1995)

 Fibre content
Intake level
European Mammal Herbivores in Deep Time

from Langer (1991)

European Mammal Herbivores in Deep Time

from Langer (1991)

Foregut vs. Hindgut Fermentation

No selective
particle
retention!

“no intake limitation”

from Stevens und Hume (1995)

 Foregut vs. Hindgut Fermentation

Selective
retention
of large
particles!
No selective
particle
retention!

“distinct intake limitation” “no intake limitation”

from Stevens und Hume (1995);

Schwarm et al. (2008)
Foregut vs. Hindgut Fermentation

from Janis (1976)

 Ruminant vs. Nonruminant
Foregut Fermentation

Selective
retention
of large
particles!

?
“distinct intake limitation”

from Stevens und Hume (1995);

Schwarm et al. (2008)
 Ruminant vs. Nonruminant
Foregut Fermentation

Selective
No selective
retention
retention of
of large
large
particles!
particles!

“distinct intake limitation”

from Stevens und Hume (1995);

Schwarm et al. (2008)
 Ruminant vs. Nonruminant
Foregut Fermentation

Selective
No selective
retention
retention of
of large
large
particles!
particles!

“distinct intake limitation” “no intake limitation”

... but ...
from Stevens und Hume (1995);
Schwarm et al. (2008)
Comparative Food Intake

from Clauss et al. (2007)

Comparative Food Intake

from Clauss et al. (2007)

Comparative Food Intake

from Clauss et al. (2007)

Comparative Food Intake

Nonrum. ff have a significantly

lower intake than either
ruminants or hindgut
fermenters!

from Clauss et al. (2007)

Intake and Passage in Primates

from Clauss et al. (2008)

Intake and Passage in Primates

from Clauss et al. (2008)

Intake and Passage in Primates

Hindgut fermenters can have either -

high or low intake and (hence) short or
long ingesta retention

from Clauss et al. (2008)

Intake and Passage in Primates

Nonrum. ff appear limited to a low food intake and

(hence) long ingesta retention

from Clauss et al. (2008)

 Two Preconditions

1. It is energetically favourable to digest

‘autoenzymatically digestible’ components
autoenzymatically, not by fermentative
digestion.
2. Autoenzymatically digestible components are
fermented at a drastically higher rate than plant
fiber.

from Hummel et al. (2006ab)

 Digestive Strategies

Low intake
⇒ long passage

High intake
⇒ short passage
 Digestive Strategies

Low intake Autoenzymatic

digestion followed
⇒ long passage
by thorough
fermentative ✓
digestion

High intake
⇒ short passage
 Digestive Strategies

Low intake Autoenzymatic

digestion followed
⇒ long passage
by thorough
fermentative ✓
digestion

Autoenzymatic
digestion followed
by cursory ✓
High intake fermentative
⇒ short passage digestion
 Digestive Strategies

Low intake Autoenzymatic Fermentative digestion

digestion followed followed by
⇒ long passage
by thorough autoenzymatic
fermentative ✓ digestion of products
✓
digestion (and remains)

Autoenzymatic
digestion followed
by cursory ✓
High intake fermentative
⇒ short passage digestion
 Digestive Strategies

Low intake Autoenzymatic Fermentative digestion

digestion followed followed by
⇒ long passage
by thorough autoenzymatic
fermentative ✓ digestion of products
✓
digestion (and remains)

Autoenzymatic Cursory fermentative

digestion mainly of
digestion followed
autoenzymatically
by cursory ✓ digestible components
High intake fermentative followed by ineffective
⇒ short passage digestion autoenzymatic digestion
of undigested fiber?
 Digestive Strategies

Low intake Autoenzymatic Fermentative digestion

digestion followed followed by
⇒ long passage
by thorough autoenzymatic
fermentative ✓ digestion of products
✓
digestion (and remains)

Autoenzymatic Cursory fermentative

digestion mainly of
digestion followed
autoenzymatically
by cursory ✓ digestible components
High intake fermentative followed by ineffective
⇒ short passage digestion autoenzymatic digestion
of undigested fiber?
 Intake and Passage

ungulates mammal herbivores

from Foose (1982) Clauss et al. (2007)
 Intake and Passage

ungulates mammal herbivores

from Foose (1982) Clauss et al. (2007)
 Intake and Passage

Nonrum. ff appear limited to a low food intake and (hence) long

ingesta retention
while hindgut fermenters can cover the whole range

ungulates mammal herbivores

from Foose (1982) Clauss et al. (2007)
Food Intake and BMR

Data overlap from Savage et al. (2004) and Clauss et al. (2007)
Food Intake and BMR

Data overlap from Savage et al. (2004) and Clauss et al. (2007)
Food Intake and BMR

Hindgut fermenters can

cover the whole range of
DMI and BMR.

Data overlap from Savage et al. (2004) and Clauss et al. (2007)
 Food Intake and BMR

Due to their long-passage-

strategy, nonrum. ff are
limited to a low DMI and
(hence) low BMR strategy

Data overlap from Savage et al. (2004) and Clauss et al. (2007)
From Digestive to Metabolic Strategies

Low intake
⇒ long passage ✓ ✓
⇒ low BMR

High intake ✓
⇒ short passage
⇒ high BMR
European Mammal Herbivores in Deep Time

from Langer (1991)

 How can you increase fermentative digestive
efficiency?

• Digestion of plant fibre by bacteria is the

more efficient ...
– the more time is available for it
= the longer the mean gastrointestinal
retention time.

– the finer the plant fibre particles are

= the finer the ingesta is chewed.
 How can you increase energy intake?

• higher food intake

• higher digestive efficiency

 How can you increase energy intake?

• higher food intake

• longer retention

• finer chewing
 How can you increase energy intake?

• higher food intake

• longer retention

• finer chewing
 How can you increase energy intake?

• higher food intake

higher gut

volume

• longer retention

• finer chewing
 How can you increase energy intake?

• higher food intake

higher gut

volume

• longer retention

• finer chewing
 How can you increase energy intake?

• higher food intake

higher gut

volume

• longer retention

• finer chewing
Higher breathing frequency in bovini - larger rumen - less space for lung - Mortolaa and
Lanthier(2005)
 How can you increase energy intake?

• higher food intake

higher gut

volume

• longer retention

• finer chewing
Mortolaa and Lanthier (2005)
wetter faeces in bovini - larger rumen - less space for colon - Clauss et al. (2003)
 How can you increase energy intake?

• higher food intake

 sorting !
• longer retention

• finer chewing
If you do not sort ...
If you do not sort ...
If you do not sort ...
If you do not sort ...
If you do not sort ...
If you do not sort ...
If you do not sort ...
If you do not sort ...
The power of sorting
The power of sorting
The power of sorting
The power of sorting
The power of sorting
The power of sorting
Ruminant vs. Nonruminant
Foregut Fermentation

Schwarm et al. (2008)

Ruminant vs. Nonruminant
Foregut Fermentation

Schwarm et al. (2008,2009)

Ruminant vs. Nonruminant
Foregut Fermentation

Schwarm et al. (2008,2009)

Ruminant vs. Nonruminant
Foregut Fermentation

Schwarm et al. (2008,2009)

Ruminant vs. Nonruminant
Foregut Fermentation

Schwarm et al. (2008,2009)

 How can you increase energy intake?

• higher food intake

 sorting !
• longer retention

• finer chewing
 How can you increase energy intake?

• higher food intake

• longer retention

• finer chewing
“Mammals are the definite chewers”

aus The Animal Diversity Web - http://animaldiversity.org

“Mammals are the definite chewers”

aus Jernvall et al. (1996)

“Mammals are the definite chewers”

aus Jernvall et al. (1996)

“Mammals are the definite chewers”

aus Jernvall et al. (1996)

Ingesta particle size (chewing efficiency)

from Fritz (2007)

Ingesta particle size (chewing efficiency)

from Fritz (2007)

Ingesta particle size (chewing efficiency)

from Fritz (2007)

“Mammals are the definite chewers”

aus Jernvall et al. (1996)

Ingesta particle size (chewing efficiency)

from Fritz (2007)

Ingesta particle size (chewing efficiency)

from Fritz (2007)

Why can‘t everyone just chew more?
Chewing in ruminants and nonruminants

Photo A. Schwarm
Chewing in ruminants and nonruminants

Photo A. Schwarm
Chewing in ruminants and nonruminants

Photo A. Schwarm
Chewing in ruminants and nonruminants

Photo A. Schwarm
Chewing in ruminants and nonruminants

Photo A. Schwarm
Chewing in ruminants and nonruminants

Photo A. Schwarm
 How can you increase energy intake?

• higher food intake

 sorting !
• longer retention

• finer chewing
 Sorting !
The rumen sorting mechanism

from Grau (1955)

The rumen sorting mechanism

from Grau (1955)

The rumen sorting mechanism

from Grau (1955)

& Ehrlein (1979)
(from Ehrlein 1979)
(from Ehrlein 1979)
(from Ehrlein 1979)
(from Ehrlein 1979)
(from Ehrlein 1979)
(from Ehrlein 1979)
(from Ehrlein 1979)
(from Ehrlein 1979)
Sorting by density

fermentation = gas production

gas bubbles = updrift

fermented particles
no gas bubbles = high density
Sorting by density

Fermentation = Gasproduktion
Gasbläschen = Auftrieb

ab-fermentierte Partikel
keine Gasbläschen = hohe Dichte
from Ehrlein (1979)
Sorting by density

Flotation and Sedimentation

only works in a fluid medium
Ruminants have moist forestomach contents

Photos A. Schwarm &

M. Lechner-Doll
Ruminants must eliminate the moisture from their GIT
content
Ruminants must eliminate the moisture from their GIT
content
from Hofmann (1973)
Ruminants must eliminate the moisture from their GIT
content
from Hofmann (1973)
& Nickel et al. (1967)
Ruminants must eliminate the moisture from their GIT
content
from Hofmann (1973)
& Nickel et al. (1967)
Ruminants achieve very fine particles

from Fritz (2007)

Ruminants achieve very fine particles

from Fritz (2007)

Comparative food intake

from Clauss et al. (2007)

Comparative food intake

from Clauss et al. (2007)

Ruminants eat more than nonruminants

from Clauss et al. (2007)

 Intake and Passage

ungulates mammal herbivores

from Foose (1982) Clauss et al. (2007)
 Intake and Passage

ungulates mammal herbivores

from Foose (1982) Clauss et al. (2007)
 Intake and Passage

ungulates mammal herbivores

from Foose (1982) Clauss et al. (2007)
 Intake and Passage

Ruminants expand the intake range of foregut fermenters

(while retaining long retention times)

ungulates mammal herbivores

from Foose (1982) Clauss et al. (2007)
Food Intake and BMR

Data overlap from Savage et al. (2004) and Clauss et al. (2007)
Food Intake and BMR

Data overlap from Savage et al. (2004) and Clauss et al. (2007)
Food Intake and BMR
Ruminants achieve high BMRs for
foregut fermenters

Data overlap from Savage et al. (2004) and Clauss et al. (2007)
Comparative Herbivore BMR

data from Savage et al. (2004)

Comparative Herbivore BMR

data from Savage et al. (2004)

Comparative Herbivore BMR

data from Savage et al. (2004)

Foregut vs. Hindgut Fermentation

Selective
excretion of
small particles
Selective Indiscriminate (and intensified
excretion of retention of particle size
reduction)
large particles
particles

“no intake “severe intake “lessened intake

limitation” limitation” limitation”

from Stevens und Hume (1995)

Digestive and Metabolic Strategies

Low intake
⇒ long passage ✓ ✓
⇒ low BMR

High intake ✓
⇒ differentiated
passage
⇒ high BMR
Digestive and Metabolic Strategies

Low intake
⇒ long passage ✓ ✓ ✓
⇒ low BMR

High intake ✓
⇒ differentiated
passage
⇒ high BMR
Digestive and Metabolic Strategies

Low intake
⇒ long passage ✓ ✓ ✓
⇒ low BMR

High intake ✓ ✓
⇒ differentiated
passage
⇒ high BMR
European Mammal Herbivores in Deep Time

from Langer (1991)

European Mammal Herbivores in Deep Time

from Langer (1991)

Digestive and Metabolic Strategies

Low intake
⇒ long passage ✓ ✓ ✓
⇒ low BMR

High intake ✓ ✓
⇒ differentiated
passage
⇒ high BMR
 Conclusion: ruminants and fluids

• Ruminants increase energy uptake by means of

a sorting mechanism (that requires a fluid
medium)
Everything comes at a prize ...
Everything comes at a prize ...
Everything comes at a prize ...
Everything comes at a prize ...

www.kleinezeitung.at
 Why Rumination?

“Rumination seems to allow herbivores to ingest in

haste and masticate at leisure” (Karasov & Del Rio
2007)
⇒ Ruminants should ingest similar amounts of food as
other herbivores and just ‘chew later’ - or become
time-constrained in intake
 Why Rumination?

“Rumination seems to allow herbivores to ingest in

haste and masticate at leisure” (Karasov & Del Rio
2007)
⇒ Ruminants should ingest similar amounts of food as
other herbivores and just ‘chew later’ - or become
time-constrained in intake

Because rumination occurs in a state of ‘drowsiness’

similar to rest, it may represent an energy-saving
strategy (less time spent ‘wide awake’, Gordon
1968)
⇒ Ruminants should have lower energy requirements
than other herbivores
 Why Rumination?

“Rumination seems to allow herbivores to ingest in

haste and masticate at leisure” (Karasov & Del Rio
2007)
⇒ Ruminants should ingest similar amounts of food as
other herbivores and just ‘chew later’ - or become
time-constrained in intake

Because rumination occurs in a state of ‘drowsiness’

similar to rest, it may represent an energy-saving
strategy (less time spent ‘wide awake’, Gordon
1968)
⇒ Ruminants should have lower energy requirements
than other herbivores
 Why Rumination?

The rumen should not be considered a ‘delay organ’

but a ‘sorting organ’ that facilitates accelerated
passage of small particles.

(from Grau 1955)

 Why Rumination?

The rumen should not be considered a ‘delay organ’

but a ‘sorting organ’ that facilitates accelerated
passage of small particles.

Rumination is a mechanism to increase the

proportion of small particles.
 Why Rumination?

The rumen should not be considered a ‘delay organ’

but a ‘sorting organ’ that facilitates accelerated
passage of small particles.

Rumination is a mechanism to increase the

proportion of small particles.

=> The ruminant way of digestion is a strategy to

shorten passage as compared to other foregut
fermenters
Fine mechanics at highest level
 thank you
for your attention
 European Mammal Herbivores in Deep Time

from Langer (1994)

 European Mammal Herbivores in Deep Time

from Langer (1994)

 European Mammal Herbivores in Deep Time

from Langer (1994)

 European Mammal Herbivores in Deep Time

from Langer (1994)

 Artiodactyls (globally) in Deep Time

from Langer (1988)

 Foregut vs. Hindgut Fermentation

Fermentation Fermentation
prior to after
enzymatic enzymatic
digestion and digestion and
absorption: absorption:
Use of ‘Loss’ of
bacterial bacterial
protein, protein,
bacterial bacterial
products (B- products (B-
Vitamins) Vitamins?)
Bacterial Use of easily
detoxification? digestible
substrates
‘Loss’ of easily
digestible
substrates

from Stevens und Hume (1995)

 Foregut vs. Hindgut Fermentation

Fermentation Fermentation
prior to after
enzymatic enzymatic
digestion and digestion and
absorption: absorption:
Use of ‘Loss’ of
bacterial bacterial
protein, protein,
bacterial bacterial
products (B- products (B-
Vitamins) Vitamins?)
Bacterial Use of easily
detoxification? digestible
substrates
‘Loss’ of easily
digestible
substrates

from Stevens und Hume (1995)