Digestive physiology of primates
Marcus Clauss Clinic for Zoo Animals, Exotic Pets and Wildlife, Vetsuisse Faculty, University of Zurich, Switzerland Institute of Anthropology 2011
based on a true story
Why are primates fascinating for digestive physiologists?
•!A broad variety of anatomical and physiological digestive adaptations within one taxonomic group
•!Experimental work is particularly challenging Major ‘limitation’: ethical responsibility
1000.0000 Caecum fermenter Colon fermenter 100.0000 Nonruminant foregut Ruminant foregut Papio anubis 10.0000
1.0000
0.1000
GIT contents (kg) 0.0100
0.0010
0.0001 0.01 0.10 1.00 10.00 100.00 1000.00 10000.00 BM (kg) from Clauss et al. (2007) Major ‘limitation’: ethical responsibility
1000.0000 Caecum fermenter Colon fermenter 100.0000 Nonruminant foregut Ruminant foregut Papio anubis 10.0000
1.0000
0.1000
GIT contents (kg) 0.0100
0.0010
0.0001 0.01 0.10 1.00 10.00 100.00 1000.00 10000.00 BM (kg) from Clauss et al. (2007) Major limitation: diets used in digestion studies Major limitation: diets used in digestion studies
90
80
70
60
50
40
aD DM (%) 30
20
10
0 0 20 40 60 80 Dietary NDF (%DM)
Data collection on langurs from Nijboer & Clauss (2006) Major limitation: diets used in digestion studies
90
80
70
60
50
40
aD DM (%) 30
20
10
0 0 20 40 60 80 Dietary NDF (%DM)
Data collection on langurs from Nijboer & Clauss (2006) Major limitation: diets used in digestion studies
90
80
70 ? 60
50
40
aD DM (%) 30
20
10
0 0 20 40 60 80 Dietary NDF (%DM)
Data collection on langurs from Nijboer & Clauss (2006) Comparing fibre fractions: Foods in “increasing quality”-order from
Gaulin (1979) Comparing fibre fractions: Foods in “increasing quality”-order from
Gaulin (1979) Comparing fibre fractions: Foods in “increasing quality”-order from
Gaulin (1979)
Against many evidence, “fruits” are considered higher quality! Comparing fibre fractions: Foods in “increasing quality”-order from
Gaulin (1979)
Evident discrepancies in the data given! Outline
•!Digestive anatomy
•!Digestive physiology I
•!The Jarman-Bell principle
•!Digestive physiology II
•!Feed your monkey
Digestive anatomy
Hindgut Fermentation - Caecum
from Stevens & Hume (1995) Hindgut Fermentation - Colon
from Stevens & Hume (1995) Hindgut Fermentation - Colon
from Stevens & Hume (1995) Primate caecum/colon fermenters
from Stevens & Hume (1995) Caecum volume
1000
) 100 3
10 olume (cm olume
Prosimians
Caecum v 1 New World Monkeys Cercopithecine monkeys Colobine monkeys Apes 0.1 10 100 Body length (cm)
Data from Chivers & Hladik (1980) Foregut Fermentation
from Stevens & Hume (1995) Foregut Fermentation
Photos A. Schwarm/ M. Clauss Foregut Fermentation - Ruminant
aus Stevens & Hume (1995) Photo Llama: A. Riek Stomach volume
10000 Prosimians New World Monkeys Cercopithecine monkeys )
3 Colobine monkeys 1000 Apes
100 Stomach volume (cm Stomach volume
10 10 100 Body length (cm)
Data from Chivers & Hladik (1980) Stomach volume
100000
Prosimians )
! 10000 New World Monkeys Cercopithecine monkeys Colobine monkeys Apes 1000 Domestic pig Domestic horse Domestic ruminant
Stomach volume (cm Stomach volume 100 Sloth
10 10 100 1000 Body length (cm)
Data from Chivers & Hladik (1980) Colobines: fermentation capacity
100 Ruminants Langurs Sloth
10
1 Fermentation contents (kg) Fermentation
0.1 1 10 100 1000 Body mass (kg)
Data collection from Parra (1978) Colobines: fermentation capacity
Data collection from Schwarm et al. (2010)
Digestive constraint I:
The ‘foregut fermentation trap‘
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) Foregut vs. Hindgut Fermentation
Fermentation Fermentation prior to after enzymatic enzymatic digestion and digestion and absorption: particularly absorption: Use of suited for ‘Loss’ of bacterial fibre fermen- bacterial 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) Intake and Passage in Primates
60
50
40
30 MRT (h) MRT 20
10
0 0 20 40 60 80 100 120 140
DMI (g/kg0.75/d) simple-stomached with forestomach Eulemur/Varecia
from Clauss et al. (2008) Intake and Passage in Primates
60
50
40
30 MRT (h) MRT 20
10
0 0 20 40 60 80 100 120 140
DMI (g/kg0.75/d) simple-stomached with forestomach Eulemur/Varecia
from Clauss et al. (2008) Intake and Passage in Primates
Hindgut fermenters can have either - 60 high or low intake and (hence) short or long ingesta retention 50
40
30 MRT (h) MRT 20
10
0 0 20 40 60 80 100 120 140
DMI (g/kg0.75/d) simple-stomached with forestomach Eulemur/Varecia
from Clauss et al. (2008) Intake and Passage in Primates
Nonrum. ff appear limited to a low food intake and 60 (hence) long ingesta retention 50
40
30 MRT (h) MRT 20
10
0 0 20 40 60 80 100 120 140
DMI (g/kg0.75/d) simple-stomached with forestomach Eulemur/Varecia
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. 80
70
60
50
40
30
20
10 Gas production (ml/h/200mgTS) 0 0 6 12 18 24 Time (h) 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 High intake ! digestible components 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 High intake ! digestible components fermentative followed by ineffective !! short passage digestion autoenzymatic digestion of undigested fiber? From Digestive to Metabolic Strategies
Low intake !! long passage ! ! !! low BMR
High intake ! !! short passage !! high BMR
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 “Mammals are the definite chewers”
aus The Animal Diversity Web - http://animaldiversity.org Ingesta particle size (chewing efficiency)
100
10
MPS (mm) 1
0.1 0.001 0.01 0.1 1 10 100 1000 10000 BM (kg) Simple-stomached Nonruminant ff
from Fritz (2007) Ingesta particle size (chewing efficiency)
100
10
MPS (mm) 1
0.1 0.001 0.01 0.1 1 10 100 1000 10000 BM (kg) Simple-stomached Nonruminant ff
from Fritz (2007) “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)
100
10
MPS (mm) 1
0.1 0.001 0.01 0.1 1 10 100 1000 10000 BM (kg) Simple-stomached Nonruminant ff
from Fritz (2007) Ingesta particle size (chewing efficiency)
100
10
MPS (mm) 1
0.1 0.001 0.01 0.1 1 10 100 1000 10000 BM (kg) Simple-stomached Nonruminant ff Ruminants
from Fritz (2007) Ingesta particle size (chewing efficiency)
100
10
MPS (mm) 1
0.1 0.001 0.01 0.1 1 10 100 1000 10000 BM (kg) Simple-stomached Nonruminant ff
from Fritz (2007) Matsuda et al. (2011) Matsuda et al. (2011) 35
30
25
20
15 Time spent feeding (% of day)
10 R/R no R/R
Matsuda et al. (2011)
The Jarman-Bell principle
The Jarman-Bell principle The Jarman-Bell principle
How do you quantify food abundance (for different-sized animals!)? The Jarman-Bell principle
How do you quantify food quality? Body size and prey abundance
from Sailer et al. (1985) Body size and prey abundance
from Sailer et al. (1985) Body size and prey abundance
from Sailer et al. (1985) Body size and prey abundance
from Carbone et al. (1999) Body size and prey abundance
from Schluter (1984) Body size and diet quality Body size and diet quality
from Sailer et al. (1985) Body size and primate digestion
•!Body size effects on digestive physiology might explain the advantage of a holwer monkey over a marmoset in terms of fibre fermentation, but it cannot be used to construe a digestive advantage of a gorilla over a howler! Jarman-Bell
•! Rather than stating “Large body size confers the advantage of being able to use more abundant food of lower quality”, try: •! “At any body size, the food of the abundance necessary for the body size in question can be digested appropriately.”
•! Or, in other words: Rather than stating “Larger animals digest more efficiently”, try: •! “Larger animals often have to ingest food of lower quality (but that’s no problem).”
Digestive constraint II:
Generally low ‘digesta washing’ in primates?
Relevance of ingesta passage
90
80
70
60
50
40 aD NDF (%) 30 ADF15 20 ADF30 IF/SF 10
0 0 10 20 30 40 50 60 70 80 MRT GIT (h) from Clauss et al. (2008) Body size and transit time
from Lambert (1998) Body size and transit time
from Lambert (1998) Body size and transit time
from Lambert (1998) Retention time is not a fixture
120
100 Hippo Elephant 80
60 MRT (h)
40
20
0 0 50 100 150 200
DMI (g/kg0.75/d)
Clauss et al. (2007) Retention time is not a fixture
from Sawada et al. (2010) Digesta passage patterns
from Müller et al. (2011) Digesta passage patterns
from Müller et al. (2011) Digesta passage patterns
from Müller et al. (2011) Digesta passage patterns
from Müller et al. (2011) Digesta passage patterns
from Müller et al. (2011) Digesta passage patterns
from Müller et al. (2011) Digesta passage patterns
from Müller et al. (2011) Digesta passage patterns
from Müller et al. (2011) Digesta passage patterns
1.! Primates appear to be limited in their digestive physiology insofar as they do not achieve a separation of fluid and particle movement in the gut (‘digesta washing’). 2.! Digesta washing is considered an important adaptation to herbivory in groups such as ruminants or caecum fermenters. 3.! Digesta washing is particularly considered an adaptation to grass-dominated diets. 4.! Does the absence of digesta washing represent an evolutionary constraint in primates?
feeding your monkey
Feeding high-sugar/starch diets Feeding high-sugar/starch diets Feeding high-sugar/starch diets
Easily digestible nutrients absorbed in small intestine => obesity Feeding high-sugar/starch diets
cf. Schwitzer & Kaumanns (2001) Obesity in primates Feeding high-sugar/starch diets
Easily digestible nutrients absorbed in small intestine => obesity
Only at very excessive amounts: ‘caecum acidosis’, diarrhoea, laminitis
Feeding high-sugar/starch diets
Easily digestible nutrients absorbed in small intestine => obesity
Only at very excessive amounts: ‘caecum acidosis’, diarrhoea, laminitis Feeding high-sugar/starch diets
Easily digestible nutrients enter the fermentation Easily digestible chamber nutrients absorbed !!‘malfermentation’ in small intestine => obesity
Only at very excessive amounts: ‘caecum acidosis’, diarrhoea, laminitis Feeding high-sugar/starch diets
Easily digestible nutrients enter the fermentation Easily digestible chamber nutrients absorbed !!‘malfermentation’ in small intestine => obesity Low food intake Laminitis Only at very Liver abscess excessive amounts: Reduced lifespan? ‘caecum acidosis’, Diarrhoea diarrhoea, laminitis Oral stereotypies Feeding high-sugar/starch diets
Easily digestible nutrients enter the fermentation Easily digestible chamber nutrients absorbed => in small intestine ‘malfermentation’ => obesity
Thin, unthrifty langurs Obese lemurs
cf. Schwitzer & Kaumanns (2001) Feeding high-sugar/starch diets Monkey zoo diet 1878
•! Milk, sugar and soft bread •! Cooked rice, potatoes, carrots •! Fruits, nuts, almonds •! Tea, coffee, beer, wine •! Fried meat should be investigated! •! 1 cigar
Martin PF (1878) Die Praxis der Naturgeschichte. Weimar
thank you for your attention