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Feeding herbivorous reptiles and primates
I. Digestive anatomy/physiology & natural diet
Marcus Clauss
Clinic for Zoo Animals, Exotic Pets and Wildlife, Vetsuisse Faculty, University of Zurich, Switzerland
EAZA Acadmey Arnhem 2015
Structure
•! Basic feeding ecology •! Basic digestive anatomy
! Reptiles vs. mammals ! Mammal herbivores
•! Primate digestive anatomy by phylogeny (=> balcony break)
•! Primate feeding problems ! Obesity ! Dysbacteriosis ! R/R ! Faeces consistency
•! Reptile feeding problems ! Growth
! Gout
from Hiiemae (2000)
Sufficient amounts of available packages
from Hiiemae (2000)
Sufficient amounts of available packages
from Hiiemae (2000)
Sufficient amounts of available packages
from Hiiemae (2000)
Sufficient amounts of available packages
from Hiiemae (2000)
Sufficient amounts of available packages
from Hiiemae (2000)
Sufficient amounts of available packages
from Hiiemae (2000)
Sufficient amounts of available packages
intermittent feeding
from Hiiemae (2000)
Sufficient amounts of available packages
continuous feeding
intermittent feeding
0.01
0.1
1
10
100
1000
0.1 1 10 100 1000
Prey
mas
s (k
g)
Carnivore mass (kg)
Carnivora Varanid
from Carbone et al. (1999)
Prey size in carnivores
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0.1
1
10
100
1000
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Prey
mas
s (k
g)
Carnivore mass (kg)
Carnivora Varanid
from Carbone et al. (1999), Losos and Greene (1988)
Prey size in carnivores
0.01
0.1
1
10
100
1000
0.1 1 10 100 1000
Prey
mas
s (k
g)
Carnivore mass (kg)
Carnivora Varanid
from Carbone et al. (1999), Losos and Greene (1988), Sailer et al. (1985)
Prey size in carnivores/omnivores
0.01
0.1
1
10
100
1000
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Prey
mas
s (k
g)
Carnivore mass (kg)
Carnivora Varanid
from Carbone et al. (1999), Losos and Greene (1988), Sailer et al. (1985), Schluter (1984)
Prey size in carnivores/omnivores
Natural diets
Natural diets
Natural diets
Phylogeny is no reliable clue
Basic gut anatomy
Carnivore
Basic gut anatomy
Stevens & Hume (1995)
Carnivore
Basic gut anatomy
Stevens & Hume (1995)
Carnivore Herbivore
Basic gut anatomy
Stevens & Hume (1995)
Carnivore Herbivore
Basic gut anatomy
Stevens & Hume (1995), Fritz pers. comm.
Carnivore Herbivore
Basic gut anatomy
Stevens & Hume (1995)
Hindgut Fermentation - Caecum
Stevens & Hume (1995)
from Stevens & Hume (1995)
Hindgut Fermentation - Colon
from Stevens & Hume (1995)
Foregut Fermentation
0.1
1
10
100
1000
10 100
Cae
cum
volu
me
(cm
!)
Body length (cm)
Prosimians
New World Monkeys
Cercopithecine monkeys
Colobine monkeys
Apes
Arctocebus Avahi Lepilemur
Euoticus Galago
Cebus Alouatta Lagothrix
Data from Chivers & Hladik (1980)
Caecum volume in primates
Data from Chivers & Hladik (1980)
Stomach volume in primates
10
100
1000
10000
10 100
Sto
mac
h v
olu
me
(cm
3)
Body length (cm)
Prosimians
New World Monkeys
Cercopithecine monkeys
Colobine monkeys
Apes
Foregut vs. Hindgut Fermentation
from Stevens & Hume (1995)
Foregut vs. Hindgut Fermentation
Fermentation after enzymatic digestion and absorption:
from Stevens & Hume (1995)
Fermentation after enzymatic digestion and absorption:
‘Loss’ of bacterial protein, bacterial products (B-Vitamins?)?
from Stevens & Hume (1995)
Foregut vs. Hindgut Fermentation
Foregut vs. Hindgut Fermentation
Fermentation after enzymatic digestion and absorption:
‘Loss’ of bacterial protein, bacterial products (B-Vitamins?)?
(coprophagy)
from Stevens & Hume (1995)
Photos: B. Burger
Coprophagy/Caecotrophy
Photos: B. Burger
Coprophagy/Caecotrophy
Photos: B. Burger
Coprophagy/Caecotrophy
Photos: B. Burger
Coprophagy/Caecotrophy
Photos: B. Burger, M. Clauss
Coprophagy/Caecotrophy
Coprophagy/Caecotrophy
Photo: A. Tschudin
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
Foregut vs. Hindgut Fermentation
Fermentation prior to enzymatic digestion and absorption:
Fermentation after enzymatic digestion and absorption:
‘Loss’ of bacterial protein, bacterial products (B-Vitamins?)?
(coprophagy)
Use of easily digestible substrates
from Stevens & Hume (1995)
Fermentation prior to enzymatic digestion and absorption:
Use of bacterial protein, bacterial products (B-Vitamins)
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 prior to enzymatic digestion and absorption:
Use of bacterial protein, bacterial products (B-Vitamins)
Bacterial detoxification?
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 prior to enzymatic digestion and absorption:
Use of bacterial protein, bacterial products (B-Vitamins)
Bacterial detoxification?
‘Loss’ of easily digestible substrates and bacterial modification
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
Foregut vs. Hindgut Fermentation
from Stevens und Hume (1995)
Fermentation prior to enzymatic digestion and absorption:
Use of bacterial protein, bacterial products (B-Vitamins)
Bacterial detoxification?
‘Loss’ of easily digestible substrates
Fermentation after enzymatic digestion and absorption:
‘Loss’ of bacterial protein, bacterial products (B-Vitamins?)
(coprophagy)
Use of easily digestible substrates
Fermentation prior to prior to priorenzymatic digestion and absorption:
Use of bacterial protein, bacterial products (B-Vitamins)
Bacterial detoxification?
‘Loss’ of easily of easily digestible substrates
Fermentation after after afterenzymatic digestion and absorption:
‘Loss’ of bacterial protein, bacterial products (B-Vitamins?)
(coprophagy)
Use of easily digestible substrates
particularly suited for
fibre fermen-tation
Digestive tract: galagos
Euoticus elegantulus
Chivers & Hladik (1980), Stevens & Hume (1995)
Otolemur crassicaudatus
Digestive tract: lemurs
Varecia variegata Lemur catta
Hapalemur griseus Propithecus verreauxi
Chivers & Hladik (1980), Campbell et al. (2000), Navarrete pers. comm.
Lepilemur leucopus Eulemur macaco
Digestive tract form and function: lemurs
Varecia variegata
Lemur catta Hapalemur griseus
Propithecus tattersalli Propithecus verreauxi
> digesta retention
fibre digestibility
FOLIVORE FRUGIVORE Campbell et al. (2000, 2004ab)
Digestive tract: Callitrichids
Stevens & Hume (1995), Navarrete pers. comm.
Callithrix jacchus Saimiri sciurus Leontopithecus chrysomelas
Saguinis oedipus
Saguinus fuscicollis Callithrix emiliae
GUMMIVORE ‘OMNIVORE’ Power et al. (1990), Ferrari & Martins
(1992)
Marmosets Tamarins
more efficienct gum digestion
Caecum form and function: gummivory
Digestive tract: Cebidae, Aotidae, Atelidae
Navarrete pers. comm., Stevens &
Hume (1995)
Alouatta sara Ateles paniscus Cebus apella Aotus trivirgatus
Digestive tract: Papionini
Navarrete pers. comm., Stevens & Hume (1995), Mau et al. (2011)
Papio anubis
Mandrillus sphinx
Macaca mulatta Macaca arctoides
Papio colon
Theropithecus colon
Theropithecus gelada
Digestive tract: Colobinae
Navarrete/Jens pers. comm., Schwarm pers. comm., Caton (1997), Stevens & Hume (1995)
Trachypithecus stomach Colobus guereza Colobus avyssinicus
Colobus Trachypithecus Presbytis
Nasalis Rhinopithecus
Pygatrix Procolobus
Nasalis larvatus
Digestive tract: Hominoidea
Stevens & Hume (1995), Navarrete pers. comm., Clauss pers. obs.
Pongo pygmaeus
Pan troglodytes
Hylobatus concolor
Gorilla gorilla
Hylobatus syndactylus
traditional primtae feeding (mistakes)
•! 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
Monkey zoo diet 1878
Major limitation: diets used in digestion studies
Feeding high-sugar/starch diets
Stevens & Hume (1995)
Feeding high-sugar/starch diets
Stevens & Hume (1995)
Easily digestible nutrients absorbed in small intestine => obesity
Feeding high-sugar/starch diets
Stevens & Hume (1995)
cf. Schwitzer & Kaumanns (2001)
Feeding high-sugar/starch diets
!! Gorillas (Cousins 1972, Leigh 1992) !! Orangutans: wild ! 38.7 kg, " 86.3 kg
zoo ! up to 81 kg, " up to 189 kg; (Schmidt 2004)
!! Chimpanzees: 10.5% !! obese (Videan et al. 2007)
!! Macaques: 7-23% obese (Walike et al. 1977, Schwartz et al. 1993, Chen at al. 2002)
!! Marmosets (Savage et al. 1993, Encarnación & Heymann 1998, Araújo et al. 2000)
!!Lemurs (Schaaf & Stuart 1983, Schwitzer & Kaumanns 2001, Taylor et al. 2012)
Obesity in primates
Obesity in primates
Easily digestible nutrients absorbed in small intestine => obesity Only at very excessive amounts: ‘caecum acidosis’, diarrhoea, laminitis
Feeding high-sugar/starch diets
Stevens & Hume (1995)
Easily digestible nutrients absorbed in small intestine => obesity Only at very excessive amounts: ‘caecum acidosis’, diarrhoea, laminitis
Feeding high-sugar/starch diets
Stevens & Hume (1995)
Easily digestible nutrients absorbed in small intestine => obesity Only at very excessive amounts: ‘caecum acidosis’, diarrhoea, laminitis
Feeding high-sugar/starch diets
Stevens & Hume (1995)
Gorilla R/R
Chimpanzee R/R
Orangutan R/R
Easily digestible nutrients absorbed in small intestine => obesity Only at very excessive amounts: ‘caecum acidosis’, diarrhoea, laminitis
Feeding high-sugar/starch diets
Stevens & Hume (1995)
Easily digestible nutrients enter the fermentation chamber !!‘malfermentation’
Easily digestible nutrients absorbed in small intestine => obesity Only at very excessive amounts: ‘caecum acidosis’, diarrhoea, laminitis
Feeding high-sugar/starch diets
Stevens & Hume (1995)
Easily digestible nutrients enter the fermentation chamber !!‘malfermentation’ Low food intake Laminitis Liver abscess Reduced lifespan? Diarrhoea Oral stereotypies
Easily digestible nutrients absorbed in small intestine => obesity Only at very excessive amounts: ‘caecum acidosis’, diarrhoea, laminitis
Feeding high-sugar/starch diets
Stevens & Hume (1995)
Fibre and faeces consistency in langurs
Nijboer et al. (2006)
Easily digestible nutrients enter the fermentation chamber => ‘malfermentation’
Easily digestible nutrients absorbed in small intestine => obesity
Obese lemurs Thin, unthrifty langurs
cf. Edwards (1995), Schwitzer & Kaumanns (2001)
Feeding high-sugar/starch diets
Feeding high-sugar/starch diets
traditional reptile feeding (mistakes)
Recommendations from successive editions of the same (German) textbook
Historical tortoise diets
Year Recommendation 1980-1993 80% fruits, 19% meat, 1% minerals
Fruits: apple, pear, orange, banana, tomato, greens (grass, clover, salad) Meat: muscle, heart – finely cut – also canned dog/cat food If fruits not available: oat flakes, rice, dry dog food, cooked potato
1999 Leafy green vegetables, vegetables, fruits (apple, banana, pear, grapes, kiwi), sometimes canned dog/cat food, grain products
2004-2009 Greens (herbs, low proportion of salad/vegetables), low amounts of fruits (lead to malfermentation and diarrhoea), canned dog/cat food should not be main component (cause gout), milk and grain products only in small amounts, hay always ad libitum, cuttlefish bone/egg shells
Recommendations from successive editions of the same (German) textbook
Historical tortoise diets
Year Recommendation 1980-1993 80% fruits, 19% meat, 1% minerals
Fruits: apple, pear, orange, banana, tomato, greens (grass, clover, salad) Meat: muscle, heart – finely cut – also canned dog/cat food If fruits not available: oat flakes, rice, dry dog food, cooked potato
1999 Leafy green vegetables, vegetables, fruits (apple, banana, pear, grapes, kiwi), sometimes canned dog/cat food, grain products
2004-2009 Greens (herbs, low proportion of salad/vegetables), low amounts of fruits (lead to malfermentation and diarrhoea), canned dog/cat food should not be main component (cause gout), milk and grain products only in small amounts, hay always ad libitum, cuttlefish bone/egg shells
Recommendations from successive editions of the same (German) textbook
Historical tortoise diets
Year Recommendation 1980-1993 80% fruits, 19% meat, 1% minerals
Fruits: apple, pear, orange, banana, tomato, greens (grass, clover, salad) Meat: muscle, heart – finely cut – also canned dog/cat food If fruits not available: oat flakes, rice, dry dog food, cooked potato
1999 Leafy green vegetables, vegetables, fruits (apple, banana, pear, grapes, kiwi), sometimes canned dog/cat food, grain products
2004-2009 Greens (herbs, low proportion of salad/vegetables), low amounts of fruits (lead to malfermentation and diarrhoea), canned dog/cat food should not be main component (cause gout), milk and grain products only in small amounts, hay always ad libitum, cuttlefish bone/egg shells
Recommendations from successive editions of the same (German) textbook
Historical tortoise diets
Year Recommendation 1980-1993 80% fruits, 19% meat, 1% minerals
Fruits: apple, pear, orange, banana, tomato, greens (grass, clover, salad) Meat: muscle, heart – finely cut – also canned dog/cat food If fruits not available: oat flakes, rice, dry dog food, cooked potato
1999 Leafy green vegetables, vegetables, fruits (apple, banana, pear, grapes, kiwi), sometimes canned dog/cat food, grain products
2004-2009 Greens (herbs, low proportion of salad/vegetables), low amounts of fruits (lead to malfermentation and diarrhoea), canned dog/cat food should not be main component (cause gout), milk and grain products only in small amounts, hay always ad libitum, cuttlefish bone/egg shells
Recommendations from successive editions of the same (German) textbook
low amounts of fruits (lead to malfermentation and diarrhoea), canned dog/cat food should not be main component (cause
milk and grain products only in small amounts
Historical tortoise diets
Feeding high-energy diets (sugar/starch/meat or just a lot)
Stevens & Hume (1995)
Feeding high-energy diets (sugar/starch/meat or just a lot)
Stevens & Hume (1995)
fast growth
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Age (d)
captive (Lapid et al. 2005)
free-range (Lapid et al. 2005)
Geochelone pardalis Geochelone nigra
Testudo graeca
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" intensive
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Body
mas
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)
Age (d)
intensive (own data)
extensive (Wilson 1968)
Tortoise growth
Ritz et al. (2010ab, 2012)
Geochelone pardalis Geochelone nigra
Testudo graeca
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Body
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intensive (own data)
extensive (Wilson 1968)
" extensive or free-range
" intensive
Tortoise growth
Ritz et al. (2010ab, 2012)
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Geochelone pardalis Gopherus agassizi
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extensive (Miller 1932 & 1955)
extensive (Patterson & Brattstrom 1972)
free-range (Germano 1992)
free-range (Germano 1994)
Geochelone sulcata
" extensive or free-range
" intensive
Tortoise growth
Ritz et al. (2010ab, 2012)
Geochelone pardalis Gopherus agassizi
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extensive (Miller 1932 & 1955)
extensive (Patterson & Brattstrom 1972)
free-range (Germano 1992)
free-range (Germano 1994)
Geochelone sulcata
" extensive or free-range
" intensive
Tortoise growth
Ritz et al. (2010ab, 2012)
Feeding meat
Stevens & Hume (1995)
Feeding meat
Stevens & Hume (1995)
gout (uric acid deposition)
Gout in reptiles
Hatt pers. comm.
Gout in reptiles
Hatt pers. comm.
Gout in reptiles
Hatt pers. comm.
Gout in reptiles
Hatt pers. comm.
thank you for your attention
