Introduction to herbivore digestive physiology
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1 Introduction to herbivore digestive physiology Marcus Clauss Clinic for Zoo Animals, Exotic Pets and Wildlife, Vetsuisse Faculty, University of Zurich, Switzerland Wildlife Digestive Physiology Vienna 2013
2 A green world
3 Primary consumers
4 Primary consumers from Akin & Amos (1975)
5 Primary consumers from Amos & Akin (1978)
6 Primary consumers from Akin & Benner (1988)
7 Primary consumers
8 Primary consumers
9 Primary consumers
10 Primary consumers
11 Primary consumers
12 Primary consumers
13 Primary consumers
14 Primary consumers
15 Primary consumers
16 Primary consumers
17 Primary consumers
18 Primary consumers
19 Herbivory
20 Herbivory
21 Herbivory Vertebrates cannot digest plant fibre by their own enzymes (aut-enzymatically); they have to rely on symbiotic gut microflora (allo-enzymatic digestion). Bacterial digestion = Fermentation The host has to supply this microflora with a habitat (so-called fermentation chambers ).
22 Carnivory is no physiological challenge... but a biomechanical and logistical one! Digesting prey is easy - catching prey is the hard part!
23 Herbivory is no logistical challenge... but a digestive one! Catching plants is easy - digesting plants is the hard part!
24 Food chains
25 Food chains
26 Food chains - and shortcuts
27 Food chains - and shortcuts no shortcut
28 Productive yet minute packages of plant food in marine systems
29 Productive yet minute packages of plant food in marine systems
30 Rare large marine herbivores
31 Rare large marine herbivores
32 Food chains - and shortcuts no shortcut
33 Ubiquitous dense large packages of plant food in terrestrial systems
34 Food chains - and shortcuts no shortcut
35 Food chains - and shortcuts no shortcut
36 Herbivory - Principles (fibre digestion)
37 Competition for light...
38 Competition for light...
39 Competition for light results in a struggle against gravity in terrestrial systems:
40 Competition for light results in a struggle against gravity in terrestrial systems: the evolution of fibre
41 Fibre analysis from Hall (2003)
42 Photosynthesis
43 Photosynthesis O 2
44 First fundamental question Do you want to use plant fibre or only the plant cell contents?
45 First fundamental question Do you want to use plant fibre or only the plant cell contents?
46 First fundamental question Do you want to use plant fibre or only the plant cell contents?
47 Fibre digestion Organic polymers (cellulose, hemicellulose) from Karasov & Martinez del Rio (2007)
48 Fibre digestion Organic polymers (cellulose, hemicellulose) Hydrolysis (soluble sugars) from Karasov & Martinez del Rio (2007)
49 Fibre digestion Organic polymers (cellulose, hemicellulose) Hydrolysis (soluble sugars) Primary fermentation (lactate, succinate) from Karasov & Martinez del Rio (2007)
50 Fibre digestion Organic polymers (cellulose, hemicellulose) Hydrolysis (soluble sugars) Primary fermentation (lactate, succinate) Secondary fermentation from Karasov & Martinez del Rio (2007)
51 Fibre digestion Organic polymers (cellulose, hemicellulose) Hydrolysis (soluble sugars) Primary fermentation (lactate, succinate) Secondary fermentation acetate, propionate, butyrate H 2 CO 2 from Karasov & Martinez del Rio (2007)
52 Fibre digestion Organic polymers (cellulose, hemicellulose) Hydrolysis (soluble sugars) Primary fermentation (lactate, succinate) Secondary fermentation acetate, propionate, butyrate H 2 CO 2 Removal ( sinks )? from Karasov & Martinez del Rio (2007)
53 Fibre digestion Organic polymers (cellulose, hemicellulose) Hydrolysis (soluble sugars) Primary fermentation (lactate, succinate) Secondary fermentation acetate, propionate, butyrate H 2 CO 2 Methanogenesis (CH 4, H 2 O ) from Karasov & Martinez del Rio (2007)
54 Fibre digestion Organic polymers (cellulose, hemicellulose) Hydrolysis (soluble sugars) Primary fermentation (lactate, succinate) Secondary fermentation acetate, propionate, butyrate H 2 CO 2 Acetogenesis (C 2 H 3 O 2, H 2 O ) Methanogenesis (CH 4, H 2 O ) from Karasov & Martinez del Rio (2007)
55 Fibre digestion Organic polymers (cellulose, hemicellulose) Hydrolysis (soluble sugars) Primary fermentation (lactate, succinate) Secondary fermentation acetate, propionate, butyrate H 2 CO 2 Acetogenesis (C 2 H 3 O 2, H 2 ) Acetogenesis (C 2 H 3 O 2, H 2 O ) Methanogenesis (CH 4, H 2 O ) from Karasov & Martinez del Rio (2007)
56 Fibre digestion Organic polymers (cellulose, hemicellulose) Hydrolysis (soluble sugars) Primary fermentation (lactate, succinate) Secondary fermentation acetate, propionate, butyrate H 2 CO 2 Acetogenesis (C 2 H 3 O 2, H 2 ) Acetogenesis (C 2 H 3 O 2, H 2 O ) Methanogenesis (CH 4, H 2 O ) Methanogenesis (CH 4, HCO 3 ) from Karasov & Martinez del Rio (2007)
57 Fibre digestion Organic polymers (cellulose, hemicellulose) Hydrolysis (soluble sugars) Primary fermentation (lactate, succinate) Secondary fermentation acetate, propionate, butyrate H 2 CO 2 Acetogenesis (C 2 H 3 O 2, H 2 ) Acetogenesis (C 2 H 3 O 2, H 2 O ) Methanogenesis (CH 4, H 2 O ) Methanogenesis (CH 4, HCO 3 ) from Karasov & Martinez del Rio (2007)
58 Fibre digestion Organic polymers (cellulose, hemicellulose) Hydrolysis (soluble sugars) acetate, propionate, butyrate Acetogenesis (C 2 H 3 O 2, H 2 ) Primary fermentation (lactate, succinate) Secondary fermentation Acetogenesis (C 2 H 3 O 2, H 2 O ) H 2 CO 2 Microbial biomass Methanogenesis (CH 4, H 2 O ) Methanogenesis (CH 4, HCO 3 ) from Karasov & Martinez del Rio (2007)
59 acetate, propionate, butyrate Acetogenesis (C 2 H 3 O 2, H 2 ) Fibre digestion Organic polymers (cellulose, hemicellulose) Hydrolysis (soluble sugars) Primary fermentation (lactate, succinate) Secondary fermentation e, propionate, butyrate H 2 CO 2 Microbial biomass Acetogenesis (C 2 H 3 O 2, H 2 O ) Methanogenesis (CH 4, H 2 O ) Methanogenesis (CH 4, HCO 3 ) from Karasov & Martinez del Rio (2007)
60 Fibre digestion Organic polymers (cellulose, hemicellulose) Hydrolysis (soluble sugars) Herbivore Primary fermentation (lactate, succinate) acetate, propionate, butyrate Acetogenesis (C 2 H 3 O 2, H 2 ) Secondary fermentation Acetogenesis (C 2 H 3 O 2, H 2 O ) H 2 CO 2 Microbial biomass Methanogenesis (CH 4, H 2 O ) Methanogenesis (CH 4, HCO 3 ) from Karasov & Martinez del Rio (2007)
61 Fibre digestion Organic polymers (cellulose, hemicellulose) Hydrolysis (soluble sugars) Herbivore Primary fermentation (lactate, succinate) Secondary fermentation acetate, propionate, butyrate Acetogenesis (C 2 H 3 O 2, H 2 ) Acetogenesis (C 2 H 3 O 2, H 2 O ) H 2 CO 2 Methanogenesis (CH 4, H 2 O ) Microbial biomass Sewer Detritus Methanogenesis (CH 4, HCO 3 ) from Karasov & Martinez del Rio (2007)
62 Fibre digestion Organic polymers (cellulose, hemicellulose) Hydrolysis (soluble sugars) Herbivore Primary fermentation (lactate, succinate) acetate, propionate, butyrate Acetogenesis (C 2 H 3 O 2, H 2 ) Secondary fermentation Acetogenesis (C 2 H 3 O 2, H 2 O ) Nonruminant H 2 CO 2 Microbial biomass Methanogenesis (CH 4, H 2 O ) Methanogenesis (CH 4, HCO 3 ) from Karasov & Martinez del Rio (2007)
63 Fibre digestion Organic polymers (cellulose, hemicellulose) Hydrolysis (soluble sugars) Herbivore Primary fermentation (lactate, succinate) acetate, propionate, butyrate Acetogenesis (C 2 H 3 O 2, H 2 ) Secondary fermentation Acetogenesis (C 2 H 3 O 2, H 2 O ) H 2 CO 2 Microbial biomass Methanogenesis (CH 4, H 2 O ) Ruminant Methanogenesis (CH 4, HCO 3 ) from Karasov & Martinez del Rio (2007)
64 Methane allometry in herbivores Methane (l/d) Ruminants Camelid Equids Elephant Wallaby Hyrax Rabbit Guinea pig Body mass (kg) from Franz et al. (2011)
65 Methane allometry in herbivores Methane (l/d) Ruminants Camelid Equids Elephant Wallaby Hyrax Rabbit Guinea pig Body mass (kg) from Franz et al. (2011)
66 Methane allometry in herbivores Methane (l/d) Ruminants Camelid Equids Elephant Wallaby Hyrax Rabbit Guinea pig Body mass (kg) from Franz et al. (2011)
67 Herbivory - Principles (body size)
68 Two fundamental questions 1. In-house or outsourcing of fibre digestion? In-house fibre digestion necessitates anatomical and physiological adaptations that might be costly in some circumstances. 2. What sequence of fibre digestion and autoenzymatic digestion?
69 Two fundamental questions 1. In-house or outsourcing of fibre digestion? In-house fibre digestion necessitates anatomical and physiological adaptations that might be costly in some circumstances. 2. What sequence of fibre digestion and autoenzymatic digestion?
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76 external rumen
77
78
79 Body size Most biologists consider body mass the most important characteristic of an organism. It is also (mostly) easy to measure. All morphological and physiological traits scale somehow with body mass. "Scaling is interesting because, aside from natural selection, it is one of the few laws we really have in biology." John Gittleman
80 Two fundamental questions 1. In-house or outsourcing of fibre digestion? In-house fibre digestion necessitates anatomical and physiological adaptations that might be costly in some circumstances. Outsourcing is only feasible at small body sizes where you have high encounter rates with nutritionally relevant amounts of microorganisms. (although there are billions of microorganisms in this room, their mass is not enough to meet the daily energy requirements of a single member of the audience)
81 acetate, propionate, butyrate Acetogenesis (C 2 H 3 O 2, H 2 ) Fibre digestion Organic polymers (cellulose, hemicellulose) Hydrolysis (soluble sugars) Primary fermentation (lactate, succinate) Secondary fermentation e, propionate, butyrate H 2 CO 2 Microbial biomass Acetogenesis (C 2 H 3 O 2, H 2 O ) Methanogenesis (CH 4, H 2 O ) Methanogenesis (CH 4, HCO 3 ) from Karasov & Martinez del Rio (2007)
82 Fibre digestion Organic polymers (cellulose, hemicellulose) Hydrolysis (soluble sugars) Herbivore Primary fermentation (lactate, succinate) acetate, propionate, butyrate Acetogenesis (C 2 H 3 O 2, H 2 ) Secondary fermentation Acetogenesis (C 2 H 3 O 2, H 2 O ) H 2 CO 2 Microbial biomass Methanogenesis (CH 4, H 2 O ) Methanogenesis (CH 4, HCO 3 ) from Karasov & Martinez del Rio (2007)
83 Surface/volume geometry 6:1... affects all surface-related processes 24:8=3:1 heat loss energy requirements food intake from Clauss & Hummel (2005)
84 Surface/volume geometry 6:1... affects all surface-related processes 24:8=3:1 from Karasov & Martinez del Rio (2007)
85 Surface/volume geometry 6:1... affects all surface-related processes 24:8=3:1 oxic anoxic gut contents from Karasov & Martinez del Rio (2007)
86 Surface/volume geometry 6:1... affects all surface-related processes 24:8=3:1 short long diffusion ways from Karasov & Martinez del Rio (2007)
87 Gut moisture content DMClin (kg) WMC (kg) y = 0.028x Body mass (kg) from Müller et al. (2013)
88 Gut moisture content y = 0.108x 1.06 DMClin (kg) WMC (kg) y = 0.028x Body mass (kg) from Müller et al. (2013)
89 Gut moisture content y = 0.108x 1.06 DMClin (kg) WMC (kg) y = 0.028x Body mass (kg) from Müller et al. (2013)
90 Gut moisture content y = 0.108x 1.06 DMClin (kg) WMC (kg) y = 0.028x Body mass (kg) from Müller et al. (2013)
91 Surface/volume geometry 6:1... affects all surface-related processes 24:8=3:1 short long diffusion ways from Karasov & Martinez del Rio (2007)
92 Herbivory - Principles (digestive tracts)
93 Two fundamental questions 2. What sequence of fibre digestion and autoenzymatic digestion? - fibre digestion prior to auto-enzymatic digestion allows the use of bacterial biomass - bacterial digestion after auto-enzymatic digestion allows more efficient use of those substrates that can be digested auto-enzymatically Foregut Stomach Small intestine Hindgut
94 Two fundamental questions 2. What sequence of fibre digestion and autoenzymatic digestion? - fibre digestion prior to auto-enzymatic digestion allows the use of bacterial biomass - bacterial digestion after auto-enzymatic digestion allows more efficient use of those substrates that can be digested auto-enzymatically Foregut Stomach Auto-enzymatic digestion (microbial digestion) Hindgut
95 Two fundamental questions 2. What sequence of fibre digestion and autoenzymatic digestion? - fibre digestion prior to auto-enzymatic digestion allows the use of bacterial biomass - bacterial digestion after auto-enzymatic digestion allows more efficient use of those substrates that can be digested auto-enzymatically Foregut Pre-autoenzymatic digestion Auto-enzymatic digestion (microbial digestion) Hindgut
96 Two fundamental questions 2. What sequence of fibre digestion and autoenzymatic digestion? - fibre digestion prior to auto-enzymatic digestion allows the use of bacterial biomass - bacterial digestion after auto-enzymatic digestion allows more efficient use of those substrates that can be digested auto-enzymatically Foregut Pre-autoenzymatic digestion Auto-enzymatic digestion (microbial digestion) Microbial digestion
97 Two fundamental questions 2. What sequence of fibre digestion and autoenzymatic digestion? - fibre digestion prior to auto-enzymatic digestion allows the use of bacterial biomass - bacterial digestion after auto-enzymatic digestion allows more efficient use of those substrates that can be digested auto-enzymatically Microbial digestion Pre-autoenzymatic digestion Auto-enzymatic digestion (microbial digestion) Microbial digestion
98 Two fundamental questions 2. What sequence of fibre digestion and autoenzymatic digestion? - fibre digestion prior to auto-enzymatic digestion allows the use of bacterial biomass - bacterial digestion after auto-enzymatic digestion allows more efficient use of those substrates that can be digested auto-enzymatically Microbial digestion Pre-autoenzymatic digestion Auto-enzymatic digestion (microbial digestion) Microbial digestion
99 Two fundamental questions 2. What sequence of fibre digestion and autoenzymatic digestion? - fibre digestion prior to auto-enzymatic digestion allows the use of bacterial biomass - bacterial digestion after auto-enzymatic digestion allows more efficient use of those substrates that can be digested auto-enzymatically Microbial digestion Pre-autoenzymatic digestion Auto-enzymatic digestion (microbial digestion) Microbial digestion
100 Two fundamental questions 2. What sequence of fibre digestion and autoenzymatic digestion? - fibre digestion prior to auto-enzymatic digestion allows the use of bacterial biomass - bacterial digestion after auto-enzymatic digestion allows more efficient use of those substrates that can be digested auto-enzymatically Microbial digestion Pre-autoenzymatic digestion Auto-enzymatic digestion (microbial digestion) Microbial digestion
101 Two fundamental questions 2. What sequence of fibre digestion and autoenzymatic digestion? - fibre digestion prior to auto-enzymatic digestion allows the use of bacterial biomass - bacterial digestion after auto-enzymatic digestion allows more efficient use of those substrates that can be digested auto-enzymatically high intake Microbial digestion Pre-autoenzymatic digestion Auto-enzymatic digestion (microbial digestion) Microbial digestion
102 Two fundamental questions 2. What sequence of fibre digestion and autoenzymatic digestion? - fibre digestion prior to auto-enzymatic digestion allows the use of bacterial biomass - bacterial digestion after auto-enzymatic digestion allows more efficient use of those substrates that can be digested auto-enzymatically low intake Microbial digestion Pre-autoenzymatic digestion Auto-enzymatic digestion (microbial digestion) Microbial digestion
103 Hindgut fermentation - the conventional approach
104
105 scheme from Karasov & Martinez del Rio (2007)
106 Scarabaeus spp. (fresh dung) Pachysoma spp. (plant litter)
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108 Herbivorous fish Kendall Clements
109 Hindgut Fermentation - Reptiles from Stevens & Hume (1995)
110 Hindgut Fermentation - Reptiles from Stevens & Hume (1995) Photo: J. Fritz
111 Herbivores - Birds from Stevens und Hume (1995)
112 Herbivores - Birds from Stevens und Hume (1995) Photo: J. Fritz
113 Herbivores - Birds Photos: J. Fritz
114 Hindgut Fermentation - Caecum from Stevens & Hume (1995)
115 Herbivores - Colon fermenters from Stevens und Hume (1995)
116 Herbivores - Colon fermenters from Stevens und Hume (1995) Photo: M. Clauss
117 Hindgut Fermentation - Colon from Stevens & Hume (1995)
118 Hindgut Fermentation - Colon from Stevens & Hume (1995)
119 Hindgut Fermentation - Colon from Stevens & Hume (1995) White rhino photo: D. Müller
120 Foregut Fermentation from Stevens & Hume (1995)
121 Photos A. Schwarm/ M. Clauss Foregut Fermentation
122 Photo M. Clauss Foregut Fermentation
123 Photo M. Clauss Foregut Fermentation
124 Herbivores - Foregut fermenters from Schwarm et al. (in prep.)) Photo: A. Schwarm
125 Foregut Fermentation - Ruminant aus Stevens & Hume (1995) Photo Llama: A. Riek
126 Foregut/Hindgut Fermenters With the majority of rodent species un-studied, we have not grasped the variability, and adaptive significance, of foregut and hindgut fermentation yet. Demon mole rat (Tachyoryctes daemon) papillated forestomach from Vrontsov (2003)
127 Foregut/Hindgut Fermenters With the majority of rodent species un-studied, we have not grasped the variability, and adaptive significance, of foregut and hindgut fermentation yet. Laotian rock rat (Laonastes aenigmamus) kangoroo-like forestomach from Scopin et al. (2011)
128 Foregut/Hindgut Fermenters With the majority of rodent species un-studied, we have not grasped the variability, and adaptive significance, of foregut and hindgut fermentation yet. Maned (crested) rat (Lophiomys imhausi) complex forestomach from Vrontsov (1967)
129 Foregut/Hindgut Fermenters With the majority of rodent species un-studied, we have not grasped the variability, and adaptive significance, of foregut and hindgut fermentation yet. White-tailed antsangy (Brachytarsomys albicauda) complex forestomach from Vrontsov (1967)
130 Foregut/Hindgut Fermenters With the majority of rodent species un-studied, we have not grasped the variability, and adaptive significance, of foregut and hindgut fermentation yet. Malagas giant rat (Hypogeomys antimena) complex forestomach from Vrontsov (1967)
131 Herbivores - Hyrax from Stevens und Hume (1995)
132 Herbivores - Hyrax from Stevens und Hume (1995)
133 Analysing for energy in plant material in vitro fermentation (gas production) May give a more biological estimation (compared to bomb calorimetry) of digestibility of energy - but higher variability Based on the use of enzymes (in vitro digestion) or gut microbes (in vitro fermentation), or a combination of both In vitro fermentation can be used to simulate foregut fermentation or other sections of the GIT with fermentative capacity
134 n o i t c u d o r p s a g Cumulative gas production e v i t a l u m u C ] M D g m / l m [ (ml/200 mg DM) Forage fermentation patterns Duration of fermentation [h] Grass (Sy,x=6.2) Herbs (Sy,x=5.2) Legumes (Sy,x=5.0) Browse + PEG (Sy,x=6.5) Browse (Sy,x=7.5) Twigs (Sy,x=3.7) from Hummel et al. (2006)
135 n o i t c u d o r p s a g Cumulative gas production e v i t a l u m u C ] M D g m / l m [ (ml/200 mg DM) Forage fermentation patterns Duration of fermentation [h] Grass (Sy,x=6.2) Herbs (Sy,x=5.2) Legumes (Sy,x=5.0) Browse + PEG (Sy,x=6.5) Browse (Sy,x=7.5) Twigs (Sy,x=3.7) from Hummel et al. (2006)
136 n o i t c u d o r p s a g Cumulative gas production e v i t a l u m u C ] M D g m / l m [ (ml/200 mg DM) Forage fermentation patterns Duration of fermentation [h] Grass (Sy,x=6.2) Herbs (Sy,x=5.2) Legumes (Sy,x=5.0) Browse + PEG (Sy,x=6.5) Browse (Sy,x=7.5) Twigs (Sy,x=3.7) from Hummel et al. (2006)
137 n o i t c u d o r p s a g Cumulative gas production e v i t a l u m u C ] M D g m / l m [ (ml/200 mg DM) Forage fermentation patterns Duration of fermentation [h] Grass (Sy,x=6.2) Herbs (Sy,x=5.2) Legumes (Sy,x=5.0) Browse + PEG (Sy,x=6.5) Browse (Sy,x=7.5) Twigs (Sy,x=3.7) from Hummel et al. (2006)
138 Fibre composition of forages 100% 80% NDF 60% 40% HC C ADL 20% 0% Grass Browse Twigs Herbs Legumes from Hummel et al. (2006)
139 Lignin is a major constraint on digestibility max. gas prod. (ml/200mg DM) y = -0.19x R 2 = ADL (g/kg DM) from Hummel et al. (2006)
140 Forage fermentation patterns 5 ml/200mg/h Grass Legumes Herbs Browse leaves Twigs Time (h) from Hummel et al. (2006)
141 thank you for your attention
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