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Zoo Biology 25:369–381 (2006) Research Article Transit Time and Digestibility of Two Experimental Diets in the Maned Wolf (Chrysocyon brachyurus) and Domestic Dog (Canis lupus) Sara E. Childs-Sanford and C. Roselina Angel Department of Animal and Avian Sciences, University of Maryland, College Park, Maryland Recent research involving nutritional management of clinical disease secondary to cystinuria in captive maned wolves (Chrysocyon brachyurus) in the United States resulted in the production of a commercially manufactured maintenance diet and subsequently, a further modified experimental diet. These two diets differed only in their protein sources and sodium concentrations. The purpose of this study was to further investigate these diets by determining their digestibility and transit time in maned wolves, and also to compare these results to the digestibility and transit time of the diets in domestic dogs. The experiment consisted of two diets (maned wolf commercial maintenance diet and experimental diet) and two species (maned wolf and domestic dog [beagle]) arranged as a 2 2 factorial design. For the transit time study, titanium dioxide (TiO 2 , 5 g/kg diet) was administered as a pulse dose and total collection of feces was carried out for 50 hr. There was no effect of diet or species on initial Ti recovery time (IRT), the amount of Ti recovered at IRT, or the time to reach 50% of Ti excretion in the feces. Maned wolves had lower total percent recovery (Po0.01) of Ti than dogs and shorter time to last recovery of Ti in the feces (Po0.05), however, marker excretion in the maned wolves may not have been complete. For the digestibility study, in which chromic oxide was used as a marker, fecal samples were collected on 2 consecutive days immediately after 12 days of being fed the diets and then analyzed for dry matter, energy, protein, and minerals. Crude protein, calcium, phosphorus, and zinc apparent digestibilities were unaffected by species or diet (P40.05). Apparent Published online 21 April 2006 in Wiley InterScience (www.interscience.wiley.com). DOI 10.1002/zoo.20095 Received 15 September 2005; Accepted 26 January 2006 Correspondence to: Dr. Roselina Angel, Department of Animal and Avian Sciences, University of Maryland, College Park, MD 20742. E-mail: [email protected] Dr. Childs’ present address is 137 Brook Way, Ithaca, NY 14850. r r 2006 Wiley-Liss, Inc.

Transit time and digestibility of two experimental diets in the maned wolf (Chrysocyon brachyurus) and domestic dog (Canis lupus)

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Page 1: Transit time and digestibility of two experimental diets in the maned wolf (Chrysocyon brachyurus) and domestic dog (Canis lupus)

Zoo Biology 25:369–381 (2006)

Research Article

Transit Time and Digestibility of TwoExperimental Diets in the Maned Wolf(Chrysocyon brachyurus) and DomesticDog (Canis lupus)Sara E. Childs-Sanford and C. Roselina Angel�

Department of Animal and Avian Sciences, University of Maryland, College Park,Maryland

Recent research involving nutritional management of clinical disease secondary tocystinuria in captive maned wolves (Chrysocyon brachyurus) in the United Statesresulted in the production of a commercially manufactured maintenance diet andsubsequently, a further modified experimental diet. These two diets differed onlyin their protein sources and sodium concentrations. The purpose of this study wasto further investigate these diets by determining their digestibility and transit timein maned wolves, and also to compare these results to the digestibility and transittime of the diets in domestic dogs. The experiment consisted of two diets (manedwolf commercial maintenance diet and experimental diet) and two species (manedwolf and domestic dog [beagle]) arranged as a 2� 2 factorial design. For thetransit time study, titanium dioxide (TiO2, 5 g/kg diet) was administered as a pulsedose and total collection of feces was carried out for 50 hr. There was no effectof diet or species on initial Ti recovery time (IRT), the amount of Ti recoveredat IRT, or the time to reach 50% of Ti excretion in the feces. Maned wolves hadlower total percent recovery (Po0.01) of Ti than dogs and shorter time to lastrecovery of Ti in the feces (Po0.05), however, marker excretion in the manedwolves may not have been complete. For the digestibility study, in which chromicoxide was used as a marker, fecal samples were collected on 2 consecutive daysimmediately after 12 days of being fed the diets and then analyzed for dry matter,energy, protein, and minerals. Crude protein, calcium, phosphorus, and zincapparent digestibilities were unaffected by species or diet (P40.05). Apparent

Published online 21 April 2006 in Wiley InterScience (www.interscience.wiley.com).

DOI 10.1002/zoo.20095

Received 15 September 2005; Accepted 26 January 2006

�Correspondence to: Dr. Roselina Angel, Department of Animal and Avian Sciences, University

of Maryland, College Park, MD 20742. E-mail: [email protected]

Dr. Childs’ present address is 137 Brook Way, Ithaca, NY 14850.

rr 2006 Wiley-Liss, Inc.

Page 2: Transit time and digestibility of two experimental diets in the maned wolf (Chrysocyon brachyurus) and domestic dog (Canis lupus)

digestibility of dry matter (Po0.05) and energy (Po0.01) were higher in theexperimental diet and in the dogs. Both dogs and maned wolves fed themaintenance diet exhibited a greater apparent retention of copper, iron, andmagnesium (Po0.01). Dogs had a higher apparent retention of magnesium andsodium than the maned wolves. Zoo Biol 25:369–381, 2006. �c 2006Wiley-Liss, Inc.

Keywords: titanium dioxide; chromic oxide; apparent digestibility; apparent retention

INTRODUCTION

For much of its history in captivity, the maned wolf (Chrysocyon brachyurus)has been generally unthrifty, with common problems including poor body condition,chronically soft stools, rapid ingesta passage, gingivitis, and cystinuria [Bush, 1980;Bovee et al., 1981]. Cystinuria, a metabolic defect involving the renal tubular andsmall intestinal epithelial cells, results in excessive urinary cystine with clinicalmanifestations secondary to cystine urolithiasis [Rutchik and Resnick, 1997;Goodyer et al., 2000]. Maned wolves have been plagued by cystinuria-relatedcomplications that have resulted in considerable morbidity and mortality [Boveeet al., 1981; Mussart and Coppo, 1999]. Basic therapeutic principles in themanagement of cystinuria focus on the two main goals of decreasing the amountof cystine excreted in the urine and increasing the solubility of any cystine that isexcreted in the urine. In humans and domestic dogs, these objectives are typicallyapproached through administration of thiol-containing drugs, pharmacologicagents used to raise urine pH, and dietary modification [Ng and Streem, 1999;Barbey et al., 2000].

The captive maned wolf has historically been fed like a carnivore, with earlydiets being composed entirely of raw meat. Subsequent manufactured dietsincluded primarily felid diets, with a switch in recent years to diets formulated forcanids [Allen et al., 1996]. Although the general diet composition of the manedwolf in the wild has been estimated [Motta-Junior et al., 1996], no nutrition studieshave been carried out on wild maned wolves or their diets. Captive diets continueto be developed based on domestic canid formulations. Dietary modification hasbeen investigated as a method of reducing and preventing clinical disease fromcystinuria in captive maned wolves [Boniface, 1998], resulting in the developmentof a maned wolf diet that was made commercially available in 1998 and fed toalmost all maned wolves in the United States for approximately 4 years. The diet,as compared to a typical canine maintenance formula, was characterized bymoderately low protein, low sulfur-containing amino acids (cysteine, methionine),and high fiber, and resulted in decreased urinary excretion of cysteine in the manedwolves studied. More recent research resulted in further modifications to this diet,specifically targeting the extremely low urine pH typical of captive maned wolves[Childs et al., 2001]. A diet was developed in which the protein level remainedunchanged but the proportion of plant-based protein was increased. In addition,the sodium (Na) in this diet was decreased based on human researchdemonstrating that low Na diets effectively reduce urinary cysteine excretion[Norman and Manette, 1990; Peces et al., 1991]. This diet was shown to raise urinepH in maned wolves [Childs et al., 2001]. The current study, part of a largerproject continuing this most recent research, was designed in an effort to assess the

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nutrient availabilities of this new diet as well as the previous commercial diet tomaned wolves, to be able to make long-term feeding and future researchrecommendations.

The digestibility of a diet, a measure of the biologic availability of its consti-tuent nutrients to the animal, is affected by numerous factors, including the chemicaland ingredient composition of the feed, feed ingredient quality, feed processingmethods, animal and environmental factors, and level of feeding. One animalfactor that has a significant effect on digestibility is gastrointestinal transit time.Transit time (TT) is typically defined as the time taken for a meal to pass from themouth to the anus [Mateos and Sell, 1981]. The TT influences the amount ofnutrients derived from diets by altering the duration of ingesta exposure to digestiveenzymes and absorptive surfaces, as well as through changes in the intestinalmicroflora and alterations in food intake ability [Mateos and Sell, 1981; Krogdahl,1986]. The captive maned wolf is generally thought to have a very rapid TT,especially after experiencing stress, manipulation, or dietary changes [Brady andDitton, 1979; Bush, 1980; Barboza et al., 1994], although no studies have been doneto assess this.

The maned wolf, a rare South American canid, has many very unique physical,behavioral, and likely physiologic characteristics [Langguth, 1975; Dietz, 1984].Little research has been carried out on the maned wolf, and thus the domestic dogis often used for comparison in areas where research is lacking, as evidenced byhistoric nutritional practices. Although the primary intent of the current researchproject was to assess the digestibility and TT of two diets in maned wolves, the studywas duplicated in domestic dogs (beagles) in an effort to highlight major similaritiesor differences between the two species. The goals of this study were to determine:1) the TT of the commercially available maned wolf maintenance diet as well as thenew experimental diet in maned wolves; 2) the availability of nutrients to the manedwolf in the new experimental diet as compared to the previous maintenance formula;and 3) if TT and nutrient digestibility of these diets in maned wolves differ from thatin domestic canids.

MATERIALS AND METHODS

Animals

The study was carried out on six adult maned wolves (three males, averageweight5 28.8 kg; three females, average weight5 22.8 kg) maintained at theNational Zoological Park’s Conservation and Research Center (Front Royal,VA), and on six beagles (four males, average weight5 14.5 kg; two females,average weight5 11.3 kg) maintained at an animal research facility (Kansas City,KS). The dogs were housed individually in indoor concrete pens. Maned wolveswere housed in enclosures with an outdoor region and a concrete indoor enclosurewith a den [Brady and Ditton, 1979]. All maned wolves were maintainedindividually and were confined to the indoor enclosures during the TT study. Forthe digestibility study, maned wolves were allowed access to outdoor pens, andfour of them were allowed to remain in mated pairs. All animal procedures wereapproved by the institutional Animal Care and Use Committee where the animalswere housed.

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Diets

Diets were manufactured by Purina Mills Inc. (St. Louis, MO) and extrudedinto a medium-sized kibble. The two diets were formulated to be isocaloric andisonitrogenous, differing only in their protein sources and Na level (Table 1). The

TABLE 1. Formulated ingredient and nutrient composition, as fed, in two experimental diets

Ingredient (%) Maintenance diet Experimental diet

Meat meal 9.58 0.00Low ash poultry meat meal 2.00 0.00Dried whey 0.50 0.50Brewer’s yeast 2.00 2.00Beef digesta 3.00 3.00Dehulled soybean meal 11.81 21.50Corn gluten meal 0.00 3.45Soy protein Concentrate 0.00 0.20Rice flour 25.00 25.00Corn flour 9.35 0.00Poultry fat 6.00 6.00Bleachable fancy tallow 6.88 8.47Soy oil 0.50 0.50Ground beet pulp 4.00 11.21Apple pomace 7.00 7.00Ground soy hulls 6.44 2.77Tomato pomace 2.50 2.50Sodium chloride 0.35 0.39Lysine 0.00 0.02Other 3.09b 5.49c

Formulated nutrient concentrations (analyzed concentrations)

Protein 18.50 (18.85) 18.50 (17.85)Fat 16.00 (17.2) 16.00 (16.9)Moisture (9.5) (8.0)Ash 7.27 7.22Crude fiber 6.5 (6.1) 6.5 (6.2)Neutral detergent fiber 13.77 (19.2) 15.69 (20.9)Acid detergent fiber 9.38 (13.95) 10.01 (16.6)Insoluble fiber (14.8) (16.9)Soluble fiber (3.25) (4.32)Metabolizable Energy, kcal/kg 3530 3530Methionine 0.26 (0.30) 0.27 (0.29)Cystine 0.21 (0.25) 0.22 (0.27)Taurine 0.30 (0.30) 0.30 (0.295)Lysine 0.95 (1.04) 0.98 (1.05)Sodium 0.50 (0.37) 0.20 (0.17)Potassium 0.60 (0.41) 0.80 (0.48)Calcium 1.39 (1.24) 1.30 (1.03)Phosphorus 0.80 (0.78) 0.80 (0.62)Magnesium 0.124 (0.124) 0.137 (0.110)Iron 0.41 (0.40) 0.33 (0.34)Manganese 0.057 (0.079) 0.058 (0.060)Zinc 0.18 (0.084) 0.177 (0.142)Copper 0.013 (0.010) 0.013 (0.010)Average kcal per gram of diet: (4,639) (4,825)

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first diet (maintenance) had approximately 40% of its protein derived from animalsources whereas the second diet (experimental) had only 5% of its protein derivedfrom animal sources. The second difference was in the Na:potassium ratio with theexperimental diet formulated to have a lower ratio than the maintenance diet.

Experimental Design

General

The study was carried out with the dogs and maned wolves at the same time of theyear but in different geographic locations, as specified previously. The same diet batchesand protocols were used for both species. The study was designed as a 2� 2 factorialarrangement of two diets (maintenance and experimental) and two species (dog andmaned wolf). The diets were tested using a split plot design, with diets being equallyrepresented within each period and no animal being tested on the same diet twice.

Each of the diets was randomly assigned to a group of animals within a time-period: one diet in the first period and the other diet in the second period. In eachtime period of 16 days, the first 2 days were used for the TT study and the remaining14 days constituted the digestibility study. Before initiation of the study all animalswere transitioned gradually to the diet on which they were to be tested in the firsttime-period. The two time-periods were separated by 9 days during which theanimals were transitioned to the diet on which they were to be tested duringthe second time-period. Throughout the study the animals were fed the same amountof food daily, and consumed all that was offered (maned wolves: male5 700 g,female5 500 g, pairs5 1,200 g; dogs: males5 280 g, females5 240 g).

Transit time

Titanium dioxide (TiO2), at a dosage of 5 g/kg of diet, was administeredorally in gelatin capsules as a bolus to each animal. The capsules were manually

Percent of protein in the diet coming from:

Animal sources: 43.8 5.3Plant sources: 56.2 94.7

aA palatability enhancing liquid ingredient with less than 10% dry matter.bContains (percent as fed): dicalcium phosphate 1.053, calcium carbonate 0.282, pyridoxine(1%) 0.144, choline chloride (70%) 0.141, menadione (2,900 ppm) 0.103, vitamin D3

(7,500 IU/g) 0.053, biotin (0.1%) 0.050, vitamin E (500 IU/g) 0.045, vitamin A (27240 IU/g)0.037, ferrous sulfate (31%) 0.030, calcium iodate (60%) 0.025, zinc oxide (72%) 0.022,l-lysine 0.022, ethoxyquin 0.018, selenium (0.06%) 0.015, calcium pantothenate (17.6 g/kg)0.013, folic acid (2%) 0.013, thiamin (10%) 0.012.cContains (% as fed): dicalcium phosphate 2.713, calcium carbonate 0.172, pyridoxine (1%)0.142, choline chloride (70%) 0.145, menadione (2,900 ppm) 0.103, vitamin D3 (7,500 IU/g)0.053, biotin (0.1%) 0.05, vitamin E (500 IU/g) 0.045, vitamin A (27240 IU/g) 0.037, ferroussulfate (31%) 0.030, calcium iodate (60%) 0.025, zinc oxide (72%) 0.022, ethoxyquin 0.018,selenium (0.06%) 0.015, calcium pantothenate (17.6 g/kg) 0.013, folic acid (2%) 0.013, thiamin(10%) 0.012.

TABLE 1. Continued

Maintenance diet Experimental diet

373Maned Wolf Ingesta Transit and Digestion

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administered to the domestic dogs whereas those for the maned wolves wereadministered by hiding the capsules in a small (r25 g) mouse. For 48 hr afteradministration of the bolus, all feces were collected and frozen (�201C) untilanalysis. Diurnal defecation times were recorded and feces collected at the timeof defecation. Video cameras in enclosures were used to record and estimatenocturnal defecation times. Nocturnal feces were collected the following morningand identified based on videotaped location in the enclosure. Feces were collected for50 hr after the animals were bolused.

Apparent digestibility

At the end of the TT study, the animals remained on the same diet, however thediets used in the digestibility trial contained 2.5 g/kg of chromic oxide (Cr2O3).Animals were maintained on this diet for the next 14 days, and representative fecalsamples were collected from each animal on the last 2 days of each experimentalphase (paired wolves were separated for this collection period). Samples were frozen(�201C) until analysis.

Sample Analysis

All samples were freeze-dried and finely ground with a mortar and pestle.

Transit time

Samples were analyzed for titanium (Ti) by a colorimetric method [Peddieet al., 1982]. Briefly, 0.1 g of sample was ashed for 13 hr at 5801C, then cooled.Sulfuric acid (7.4M) (10ml) was added to the ashed samples then gently boiled for60min until the sample was completely dissolved. The cooled sample was transferredinto a beaker containing 25ml of distilled water and then filtered (Whatman #541)into a 100-ml volumetric flask. Hydrogen peroxide (30%) (20ml) was added to thevolumetric flask and the flask filled to volume with distilled water. The sample wasmixed well, transferred to a test tube, and absorbance read at 410 nm.

Apparent digestibility

Freeze-dried ground fecal samples were digested in a mixture of nitric andperchloric acid at 1001C for 4 hr, and then analyzed for chromium (Cr) [Saha andGilbreath, 1991]. They were also analyzed for moisture [Association of OfficialAnalytical Chemists, 1995a], nitrogen [Association of Official Analytical Chemists,1995b], gross energy [Association of Official Analytical Chemists, 1980], and calcium(Ca), phosphorus (P), copper (Cu), zinc (Zn), magnesium (Mg), iron (Fe), andsodium (Na) [Anderson, 1996].

Statistical Analysis

The time (hr) after administration of the TiO2 bolus when 50% of the markerhad been recovered in feces was estimated for each animal using the second-orderpolynomial regression analysis model: y5 ax21bx1c, where x is the time afterdosing (hr) and y is the % of total marker dosage recovered [Snedecor and Cochran,1989]. The time to 50% recovery, by animal, was used as an estimated parameter fordata analysis. Data for both TT and digestibility were analyzed using the JMPstatistical analysis program of SAS [2000] as a split plot (two periods) with diets andspecies (arranged as a complete 2� 2 factorial). The factors were diet (maintenance

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and experimental) and species (dog and maned wolf). Differences between meanswere considered significant when the probability (P) value was r0.05.

RESULTS

Transit time

There was no effect of diet or species on initial recovery time (IRT), theamount of Ti recovered at IRT, or the time to reach 50% of Ti excretion in the feces(Table 2). There was also no effect of diet on the total percent of Ti recovered fromthe feces during the trial, however, there was an effect of species. The maned wolveshad a lower recovery of Ti (average 86.69%) than the dogs (average 97.02%)(Table 2). There was also a species effect on the time to last recovery of Ti, with thetime being shorter in the maned wolves than in the dogs (Table 2).

Apparent digestibility

Mean apparent digestibilities of energy, dry matter (DM), protein, fat, andselected minerals are shown in Table 3. There were no diet by species interactions.Crude protein, Ca, P, and Zn apparent digestibilities were unaffected by species ordiet. The apparent digestible energy (ADE) and apparent DM digestibility (ADMD)were affected both by species and diet. The experimental diet had greater ADE andADMD than the maintenance diet (3,625 vs 3,486 kcal ADE/kg diet and 69.4% vs67.3% ADMD, respectively). Both ADE and ADMD were greater in dogs than inthe maned wolves (3,690 vs 3,420 kcal ADE/kg and 71% vs 65.7% ADMD,respectively). For Cu, Fe, and Mg apparent digestibilities, there was an effect of dietwith animals fed the maintenance diet exhibiting a greater digestibility than those onthe experimental diet. There was also an effect of species on apparent Mg and Nadigestibility, with higher digestibility in the dogs than in the maned wolves. Theeffect of species on apparent Cu digestibility was close to significant (P5 0.056).Dogs had a higher apparent digestibility of Cu and Fe than maned wolves when fedthe maintenance diet. Dogs on the experimental diet had a higher apparentdigestibility of Cu but not of Fe.

DISCUSSION

In this study, the differences in protein composition between the maintenanceand experimental diets did not have any effect on TT. This finding is in agreementwith other studies in dogs where soy protein was included in the diet, especially ifit was in a hydrolyzed rather than an intact form [Zhao et al., 1997; Hill et al., 2000].Additionally, there was no difference between TT in the dogs and maned wolvesas measured by several parameters, including time to initial recovery of the markerin the feces, amount of marker obtained at initial recovery, and time to recovery of50% of the marker in the feces. These findings contradict previous beliefs thatcompared to other canids, maned wolves have an extremely rapid TT [Barboza et al.,1994]. Several reports, written at a time when the maned wolves were being fedprimarily a meat-based canid diet, describe a TT of 20min, or even less when animalswere stressed [Brady and Ditton, 1979; Bush, 1980].

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TABLE

2.Transittimeofthemaintenance

andexperim

entaldiets

inbeaglesandmaned

wolves

asaffectedbydietand/orspecies

Species

Diet

InitialTirecovery

time(IRT)(hours)a

AmountTi(m

g)

recovered

atIR

TTim

eto

recoveryof

50%

Ti(hours)b

Tim

eto

last

Ti

recovery(hours)c

Total%

Tirecoveryd

Doge

Maintenance

f2.88

1.11

14.2

47.5

97.0

Experim

entalg

3.90

6.82

11.7

47.2

97.0

Maned

Wolfe

Maintenance

4.25

3.34

13.5

43.3

87.2

Experim

ental

1.17

0.49

14.8

45.2

86.2

SEM

h0.60

3.57

1.09

1.24

1.25

P-value

0.39

0.58

0.26

0.09

o0.01

Main

Effects

(means)

Species

Dog

3.39

3.97

13.0

47.3

97.0

Maned

wolf

4.21

1.91

14.1

44.2

86.7

Diet

Maintenance

3.56

2.22

13.8

45.4

92.1

Experim

ental

4.03

3.66

13.3

46.2

91.6

Main

Effects

(P-values)

Species

0.20

0.58

0.30

0.02

o0.01

Diet

0.46

0.69

0.59

0.05

0.68

Speciesxdiet

0.38

0.26

0.10

0.38

0.69

aHours

followingtheinitialpulsedose

ofthemarker,titanium

(Ti),thatthemarker

wasfirstdetectedin

thefeces.

bNumber

ofhrfollowingtheinitialpulsedose

ofthemarker

atwhich50%

ofthetitanium

dose

hadbeenexcreted

inthefeces.

cHours

followingtheinitialpulsedose

oftitanium

thatthelast

tracesofthemarker

weredetectedin

thefeces.

dPercentageoftheinitialtitanium

pulsedose

(mg)thatwasrecovered

from

thefeces.

eBeagles(6

anim

als)andmaned

wolves

(6anim

als).Diets

tested

inasplitplotdesignwithtw

operiods.

f Maintenance

dietwasacommerciallyavailable

diet(M

azuriFeedss

,Inc.,St.Louis,MO,Maned

WolfMaintenance

Diet).

gTheexperim

entaldiet,ascomparedto

themaintenance

diet,hadagreaterproportionofitsprotein

from

plantsources

andalower

sodium

topotassium

ratio.

hStandard

errorofthemean.

376 Childs-Sanford and Angel

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Page 9: Transit time and digestibility of two experimental diets in the maned wolf (Chrysocyon brachyurus) and domestic dog (Canis lupus)

TABLE

3.Apparentdry

matter

andcrudeprotein

digestibilities,apparentdigestible

energy,andapparentmineralretentionasaffectedbydietand/or

species

Digestibility(%

)Retention

Speciesa

Dietb

Energy

(kcal/kg)

Dry

matter

Protein

Cac

Pc

Cuc

Znc

Mgc

Fec

Nac

Dog

Maintenance

3,641f

69.9

f75.6

26.7

49.4

14.6

e26.9

36.9

e16.8

e68.6

e

Experim

ental

3,740e

72.1

e76.1

23.8

49.5

9.50g

23.0

32.5

f9.50g

62.6

e

Maned

wolf

Maintenance

3,331h

64.7

h71.5

22.1

49.6

11.7

f24.7

31.9

f13.8

f53.1

f

Experim

ental

3,510g

66.7

g75.2

22.3

48.0

6.60h

24.6

26.2

g9.00g

42.1

g

SEM

d29.6

0.77

1.22

2.61

2.19

1.34

2.79

1.62

1.21

3.87

P-value

o0.01

o0.01

0.06

0.55

0.94

o0.01

0.79

o0.01

o0.01

o0.01

Main

effects(m

eans)

Dog

3,690

71.0

75.8

24.5

49.5

12.0

25.8

34.7

13.2

65.6

Maned

Wolf

3,420

65.7

73.4

22.9

48.8

9.20

23.9

29.0

11.4

47.6

Maintenance

3,486

67.3

73.6

24.4

49.5

13.1

25.8

34.4

15.4

60.9

Experim

ental

3,625

69.4

75.7

23.0

48.8

8.00

23.8

29.3

9.30

52.3

Main

effects(P

-values)

Species

o0.01

o0.01

0.06

0.54

0.73

0.05

0.48

o0.01

0.08

o0.01

Diet

o0.01

0.01

0.10

0.58

0.74

o0.01

0.46

o0.01

o0.01

0.03

Species�diet

0.19

0.91

0.20

0.22

0.69

0.99

0.91

0.67

0.11

0.49

aBeagles(6

anim

als)andmaned

wolves

(6anim

als).Diets

tested

inasplitplotdesignwithtw

operiods.

bThemaintenance

dietwasacommerciallyavailable

diet(M

azuriFeedss

,Inc.,St.Louis,MO,Maned

WolfMaintenance

Diet).Theexperim

ental

diet,ascomparedto

themaintenance

diet,hadagreaterproportionofitsprotein

from

plantsources

andalower

sodium

topotassium

ratio.

cCalcium

(Ca),Phosphorus(P),Copper

(Cu),Zinc(Zn),Magnesium

(Mg),Iron(Fe),andSodium

(Na).

dStandard

errorofthemean.

e,f,g,hMeanswithdifferentsuperscriptlettersdiffer(Po0.05).

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There was an effect of species on the number of hr post-bolus that Ti was lastrecovered. The maned wolves had an earlier ‘‘last recovery’’ (44.21 hr) than the dogs(47.32 hr). Several of the dogs had feces collected for analysis as late as 50 hr after theTiO2 bolus, but many of the maned wolves did not defecate this close to the end ofthe study. Therefore, if the maned wolves had been given additional time to defecate,additional Ti may have been recovered, lengthening the time to last recovery of Tias well as increasing the total recovery.

The total fecal recovery of Ti in the dog was high (average 97.02%), andcorresponds well with Ti recovery in similar studies carried out in pigs (96%) andrats (98%) [Njaa, 1961; Kavanagh et al., 2001]. The total recovery of Ti for themaned wolves, however, was lower (average5 86.69%). Potential environmentalfactors that may have contributed to loss of Ti during collection include difficultyin carrying out a total fecal collection without leaving residue due to the softconsistency of maned wolf feces, as well as a small amount of loss at the time ofcapsule ingestion when on occasion the capsules were ruptured during chewing.

Alternatively, instead of Ti loss during collection, the collection perioditself may not have been long enough for the maned wolves, and Ti may stillhave been present in the gastrointestinal tract. The latter scenario seems most likely,due to the close agreement of the average percent recoveries in maned wolveson both the maintenance and experimental diets. If this is the case, it implies thatthe TT for wolves may actually be slightly longer than for the domestic dogs usedin this study.

The close agreement of the various parameters used to measure TT in the dogsand maned wolves suggest that TT in maned wolves is similar to that in other canidswhen diets comparable to those tested are fed. Few studies have been carried outmeasuring ororectal TT in domestic dogs on various diets, but some reportsdocument TT of 22 hr [Warner, 1981] and 19–34 hr [Rolfe et al., 2002]. The reportedTT for domestic dogs show some variation, due likely to breed differences, dietdifferences, use of various markers, and differences in methodologies and definitionsof TT. In general, however, the average times listed in reports for domestic dogs areshorter than those determined in the present study. This may have been due to highlevels of soluble fiber in the diets tested. In addition to being known for a rapid TT,maned wolves fed canine and feline meat-based diets commonly had loose or waterystool. Therefore, high levels of soluble fiber had been included in the commercialmaintenance diet in an effort to increase fecal bulk and improve stool quality[Boniface, 1998], and these levels were continued in the experimental diet. Dietaryfiber can have various effects on TT, depending both on the type of fiber and how thefiber was processed [Smith and Eastwood, 1980; Hillenmeier, 1995]. In many reports,insoluble fiber decreases TT, whereas soluble fiber tends to lengthen it [Burrowset al., 1982; Stevens et al., 1988].

The lack of effect of diet on protein digestibility in either the dogs or manedwolves is similar to findings in dog studies where animal-protein based diets werecompared to those containing vegetable or soy-based protein [Huber et al., 1994;Yamka et al., 2003]. Several authors have concluded that in dogs, the digestibilityof soy protein is slightly less than that of animal proteins [Kendall and Holme, 1982;Hill et al., 2001], however, the use of a highly processed soy product in theexperimental diet of this study (soy protein isolate) likely resulted in a high level ofprotein digestibility [Wiernusz et al., 1995; Clapper et al., 2001].

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The experimental diet resulted in higher apparent digestibilities of energy andDM in both species. This finding is in contrast to similar studies in dogs where dietscontaining soybean products were fed. Several researchers observed no effect ofincreased soybean content in diets on DM or energy digestibility in dogs [Huberet al., 1994; Bednar et al., 2000; Clapper et al., 2001], whereas others detecteddecreases [Hill et al., 2001; Yamka et al., 2003]. These studies typically used soybeanmeal or soy flour as the source of soy protein. Increased processing of soy productshas been demonstrated to increase diet digestibility [Wiernusz et al., 1995; Zhaoet al., 1997]. Therefore, the use of soy protein isolate as a main source of protein inthe diets may have resulted in higher digestibility, even compared to the meat andpoultry meat meal, leading to the increased digestibility of DM and energy in theexperimental diet.

The apparent digestibility of Mg, Fe, Cu, and Na was lower in both specieson the experimental diet as compared to the maintenance diet. This may be in partdue to the presence of several anti-nutritional factors in soy protein, includingoligosaccharides and phytate [Clapper et al., 2001; Yamka et al., 2003, 2005]. Inparticular, the presence of phytate in soy has been demonstrated to decrease theavailability of several minerals, especially in monogastric species [Kamao et al., 2000;Hurrell, 2003]. With a possible effect of phytate on mineral retention, however, it isunusual that there is no effect of diet on Zn digestibility [Lonnerdal et al., 1999;Norii and Suzuki, 2002]. The mechanism for the decrease in Na digestibility in dogsand maned wolves on the experimental diet is unknown, but is hypothesized by otherresearchers to be due to an effect of soy protein on reducing digestibility [March,1984; Hill et al., 2001]. This finding may also reflect the fact that the experimentaldiet is much lower in Na (0.17%) than the maintenance diet (0.37%) [Patience et al.,1987; McCabe et al., 1994].

CONCLUSIONS

1. No significant differences in several parameters commonly used to measure TTwere detected between maned wolves and dogs. Based on the findings in this studyof similar TT between dogs and maned wolves on these two diets, the TT was nota contributor to any of the species or diet effects observed on nutrientdigestibility.

2. Higher digestibility of the experimental diet implies that the soybean proteinisolate and other plant protein sources used had a very high digestibility, evenwhen compared to the meat-based protein present in larger proportions in themaintenance diet. On the other hand, the soybean protein sources in theexperimental diet may have also been the cause of decreased apparent digestion ofminerals in both dogs and maned wolves as compared to the maintenance diet,likely due to the presence of anti-nutritional factors.

3. Several of the measurements in this study were affected by species, including DM,energy, Cu, Mg, Fe, and Na digestibilities. In all cases, there was a similar trendtoward lower apparent digestibility in the maned wolves than in the dogs. Thesefindings should alert nutritionists to the possibility of significant speciesdifferences between maned wolves and other canids in nutrient digestibility,an important consideration because most maned wolves are fed formulas basedon domestic canid formulations.

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ACKNOWLEDGMENTS

The authors gratefully acknowledge the assistance of C. Gray for implementingthe canine part of the study; the animal care staff of the National ZoologicalPark’s Conservation and Research Center, especially K. Lang and M. Rodden; andJ. Sanford for lab assistance.

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