tannins in the nutrition of wild herbivoresffffffff-f77d... · salivary tannin-binding proteins...

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Tannins in the nutrition of wildherbivores

Tannins are feeding deterrents.

They occur in browse (leaves).

They deter feeding by reducingdigestive efficiency and bytoxicity.

xxxxxxxxxx

from Foley et al. (1999)

from Foley et al. (1999)

from Foley et al. (1999)

Ecological Studies

Duiker do not seem to avoid tannins Müller et al. (1998)

Duiker do not avoid tannins Faurie and Perrin (1993)

Roe deer do not avoid tannins Tixier et al. (1997)

Mule deer and b lack -tailed deer do not avoid tannins McArthur et al. (1993) Greater kudu avoid tannins Cooper and Owen -Smith (1985), Cooper et al. (1988)

Giraffe avoid tannins Furstenburg and van Hoven (1994)

Impala avoid tannins Cooper and Owen -Smith (1985) , Cooper et al. (1988)

Goat avoid tannins Cooper and Owen -Smith (1985)

Cattle avoid tannins Wilkins et al. (1953), Donnelly (1954) African buffalo avoid tannins Field (1976)

Mouse lemur avoid tannins Ganzhorn (1988)

Greater dwarf lemur do not avoid tannins Ganzhorn (1988)

Brown lemur do not avoid tannins Ganzhorn (1988)

Eastern woolly lemur do not avoid tannins Ganzhorn et al. (1985) Indri do not avoid tannins Ganzhorn (1988)

Howler monkey avoid tannins Glander (1981)

Marmosets avoid tannins Simmen (1994)

Vervet monkey avoid tannins Wrangham and Waterman (1981)

Rhesus monkey avoid tannins Marks et al. (1987) Baboons avoid phenolics Barton and Whiten (1994)

Guereza avoid tannins Oates et al. (1977)

Black colobus monkey avoid tannins McKey et al. (1981)

Orangutan avoid tannins Leighton (1993) Gorilla do not avoid tannins Calvert 1985

Chimpanzees avoid tannins Wrangham and Waterman (1983)

Ecological Studies

Duiker do not seem to avoid tannins Müller et al. (1998)

Duiker do not avoid tannins Faurie and Perrin (1993)

Roe deer do not avoid tannins Tixier et al. (1997)

Mule deer and b lack -tailed deer do not avoid tannins McArthur et al. (1993) Greater kudu avoid tannins Cooper and Owen -Smith (1985), Cooper et al. (1988)

Giraffe avoid tannins Furstenburg and van Hoven (1994)

Impala avoid tannins Cooper and Owen -Smith (1985) , Cooper et al. (1988)

Goat avoid tannins Cooper and Owen -Smith (1985)

Cattle avoid tannins Wilkins et al. (1953), Donnelly (1954) African buffalo avoid tannins Field (1976)

Mouse lemur avoid tannins Ganzhorn (1988)

Greater dwarf lemur do not avoid tannins Ganzhorn (1988)

Brown lemur do not avoid tannins Ganzhorn (1988)

Eastern woolly lemur do not avoid tannins Ganzhorn et al. (1985) Indri do not avoid tannins Ganzhorn (1988)

Howler monkey avoid tannins Glander (1981)

Marmosets avoid tannins Simmen (1994)

Vervet monkey avoid tannins Wrangham and Waterman (1981)

Rhesus monkey avoid tannins Marks et al. (1987) Baboons avoid phenolics Barton and Whiten (1994)

Guereza avoid tannins Oates et al. (1977)

Black colobus monkey avoid tannins McKey et al. (1981)

Orangutan avoid tannins Leighton (1993) Gorilla do not avoid tannins Calvert 1985

Chimpanzees avoid tannins Wrangham and Waterman (1983)

All these animals will try to minimize tanninintake. However, most cannot avoid them

completely!

Tannins are part of the natural diet of manyanimals.

Salivary tannin-binding proteins

Species Source

Swamp wallab ies ( W bicolor ) McArthur et al. (1995)

Pademelon ( Thylogale thetis ) McArthur et al. (1995)

Humans ( Homo sapiens ) McArthur et al. (1995), Charlton et al. (1996), Bacon and Rhoades (1998)

Mouse ( Mus musculus ) Mehansho et al. (1985), Asquith et al. ( 1985)

Rat ( Rattus norvegicus ) Mehansho et al. (1983), Jansman et al. (1994)

Root vole ( Microtus oeconomus ) Juntheikki et al. (1996)

Beaver ( Castor canadensis ) Hagerman and Robbins (1993)

Pika ( Ochotona princeps ) Dearing (1997)

Rabbit ( Oryctolagus c uniculus ) Mole et al. (1990)

Mountain hare McArthur et al. (1995)

Hare ( Lepus timidus ) Mole et al. (1990)

Black bear ( Ursus americanus ) Hagerman and Robbins (1993)

Camel ( Camelus dromedarius ) Schmidt -Witty et al. (1994)

Roe deer ( Capreolus capreolus ) Fickel et al. (1998)

White -tailed deer ( Odocoileus virginianus ) Robbins et al. (1987b), Mole et al. (1990)

Mule deer ( Odocoileus hemionus ) Austin et al. (1989), Robbins et al. (1987b), Hager man and Robbins (1993)

Moose ( Alces alces ) Hagerman and Robbins (1993), Juntheikki (1996)

Salivary tannin-binding proteins in rhinos

0

10

20

30

40

50

60

0 5 10 15 20 25 30 35 40

TBC(50 !g/ml , hydrolyzable tannins; % of maximum)

TBC

(1

50 !

g/m

l con

dens

ed ta

nnin

s;

% o

f max

imum

)

White Rhino

Black Rhino

from Clauss et al. (subm.)

Salivary tannin-binding proteins in black rhinos

0

20

40

60

80

100

120

0 5 10 15 20 25 30 35 40

TBC(50 !g/ml , hydrolyzable tannins; % of maximum)

TBC

(1

50 !

g/m

l con

dens

ed ta

nnin

s;

% o

f max

imum

)

regular diettannic acid diet

from Clauss et al. (subm.)

Tannins can function asantioxidants.

Phenolic substance can be absorbed from the gutand support other antioxidants within the body.

Even if not absorbed, phenolic substances canprotect other antioxidnts from being oxidized inthe gut and thereby increase their availability.

WWAP

0

200

400

600

800

1000

1200

1400

regular tannic acid quebracho

TAA

(yM

)

EmmaQuinto

Black rhino feeding trials

from Clauss et al. (in prep.)

In several captive animal species, low antioxidantstatus has been reported.

Roe deer have been suspected to be dependenton vitamin C intake in captivity. Enteritic disordersin roe deer have been cured by high dosages ofvitamin C alone.

Tannins prevent bloat.

Do foregut-fermentingarboreal folivoresdepend on tannins toprevent bloat and controlintestinal bacteria andparasites?

Tannins have anthelminticproperties.

Tannins have antibacterialproperties against a wide rangeof bacteria, including potentialgastrointestinal pathogens.

Are browsing ruminantsdependent on phenolicplant substances fortheir antioxidant supplyand/or intestinal parasiteand bacteria control?

If so, by what mechanisms did grazing ruminantsbecome independent of phenolic plant substances?

Tannins reduce the availability ofdietary iron.

Did some hindgut-fermentingbrowsers develop especiallyeffective iron absorptionmechanisms to compensatefor the chelating effects ofdietary tannins?

Is there a tannin “requirement”for certain species?

Roe deer preference trials

from Clauss et al. (2003)

Roe deer preference trials

from Clauss et al. (2003)

Group I

0

0.5

1

1.5

2

2.5

3

3.5

4

4.5

5

0 5 10 15 20

Day

tota

l int

ake

(kg)

ta

nnic

aci

d (%

)

total intake (kg)tannic acid (%)

Roe deer preference trials

from Clauss et al. (2003)

Group I

0

0.5

1

1.5

2

2.5

3

3.5

4

4.5

5

0 5 10 15 20

Day

tota

l int

ake

(kg)

ta

nnic

aci

d (%

)

total intake (kg)tannic acid (%)

Group II

0

0.5

1

1.5

2

2.5

3

3.5

0 5 10 15 20

Day

tota

l int

ake

(kg)

ta

nnic

aci

d (%

)

total intake (kg)tannic acid (%)

Roe deer preference trials

from Clauss et al. (2003)

Group I

0

0.5

1

1.5

2

2.5

3

3.5

4

4.5

5

0 5 10 15 20

Day

tota

l int

ake

(kg)

ta

nnic

aci

d (%

)

total intake (kg)tannic acid (%)

Group II

0

0.5

1

1.5

2

2.5

3

3.5

0 5 10 15 20

Day

tota

l int

ake

(kg)

ta

nnic

aci

d (%

)

total intake (kg)tannic acid (%)

Group III

0

1

2

3

4

5

6

7

0 5 10 15 20

Day

tota

l int

ake

(kg)

qu

ebra

cho

(%)

total intake (kg)quebracho (%)

Roe deer preference trials

from Clauss et al. (2003)

Group I

0

0.5

1

1.5

2

2.5

3

3.5

4

4.5

5

0 5 10 15 20

Day

tota

l int

ake

(kg)

ta

nnic

aci

d (%

)

total intake (kg)tannic acid (%)

Group II

0

0.5

1

1.5

2

2.5

3

3.5

0 5 10 15 20

Day

tota

l int

ake

(kg)

ta

nnic

aci

d (%

)

total intake (kg)tannic acid (%)

Group III

0

1

2

3

4

5

6

7

0 5 10 15 20

Day

tota

l int

ake

(kg)

qu

ebra

cho

(%)

total intake (kg)quebracho (%)

Group IV

0

1

2

3

4

5

6

7

0 2 4 6 8 10 12

Day

tota

l int

ake

(kg)

qu

ebra

cho

(%) total intake (kg)

quebracho (%)

Giraffe preference trials

Ellie

0

2

4

6

8

10

12

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25day

cons

umpt

ion

(kg)

lucerne hayregular pelletstannic acid pellets

from Clauss et al. (2002)

Giraffe preference trials

Ellie

0

2

4

6

8

10

12

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25day

cons

umpt

ion

(kg)

lucerne hayregular pelletstannic acid pellets

from Clauss et al. (2002)

Will

0

2

4

6

8

10

12

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26day

cons

umpt

ion

(kg)

lucerne hayregular pelletstannic acid pellets

Giraffe preference trials

Ellie

0

2

4

6

8

10

12

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25day

cons

umpt

ion

(kg)

lucerne hayregular pelletstannic acid pellets

from Clauss et al. (2002)

Will

0

2

4

6

8

10

12

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26day

cons

umpt

ion

(kg)

lucerne hayregular pelletstannic acid pellets

juveniles

0

2

4

6

8

10

12

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25day

cons

umpt

ion

(kg)

lucerne hayregular pelletstannic acid pellets

Giraffe preference trials

Ellie

0

2

4

6

8

10

12

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25day

cons

umpt

ion

(kg)

lucerne hayregular pelletstannic acid pellets

from Clauss et al. (2002)

Will

0

2

4

6

8

10

12

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26day

cons

umpt

ion

(kg)

lucerne hayregular pelletstannic acid pellets

juveniles

0

2

4

6

8

10

12

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25day

cons

umpt

ion

(kg)

lucerne hayregular pelletstannic acid pellets

Josie

0

2

4

6

8

10

12

1 3 5 7 9 11 13 15 17 19 21 23 25 27 29 31 33 35days

cons

umpt

ion

(kg)

lucerne hayregular pelletstannic acid pellets

Giraffe preference trials

Ellie

0

2

4

6

8

10

12

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25day

cons

umpt

ion

(kg)

lucerne hayregular pelletstannic acid pellets

from Clauss et al. (2002)

Will

0

2

4

6

8

10

12

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26day

cons

umpt

ion

(kg)

lucerne hayregular pelletstannic acid pellets

juveniles

0

2

4

6

8

10

12

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25day

cons

umpt

ion

(kg)

lucerne hayregular pelletstannic acid pellets

Josie

0

2

4

6

8

10

12

1 3 5 7 9 11 13 15 17 19 21 23 25 27 29 31 33 35days

cons

umpt

ion

(kg)

lucerne hayregular pelletstannic acid pellets

?

Roe deer feeding trials

from Clauss et al. (2003)

Roe deer feeding trials

from Clauss et al. (2003)

Roe deer feeding trials

pelleteddiet

from Clauss et al. (2003)

Roe deer feeding trials

regular 3% tannic acid

pelleteddiet

from Clauss et al. (2003)

Roe deer feeding trials

regular 3% tannic acid

pelleteddiet

0

500

1000

1500

2000

2500

3000

3500

4000

4500

Aug 99 Sep 99 Jan 00 May 00

Food

inta

ke p

er g

roup

(g)

Control groupTannin group

from Clauss et al. (2003)

Roe deer feeding trials

regular 3% tannic acid

pelleteddiet

0,0

5,0

10,0

15,0

20,0

25,0

30,0

Tannic acid period Quebracho period

Body

wei

ght g

ain

(%)

Control groupTannin group

*

control tanninfrom Clauss et al. (2003)

Low levels of dietary tannins canprevent protein/carbohydratedegradation in the forestomach,thus enhancing their nutritivevalue for ruminants.

In sheep, Kaitho et al. (1998) even reported weightgains due to the use of tannins.

Conclusions?

• Low levels of tannins might be beneficial for many captive wild animals (based on theoretical considerations)

• Many potentially tannin-related problems in captivity could possibly be solved by a morerestricted use of concentrate feeds, by anincrease in fibre content, by controlled minerallevels

• As always: more research needed …

end of session

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