Nothing Special   »   [go: up one dir, main page]

Beheerder, Journal Manager, Gussek Et Al

Download as pdf or txt
Download as pdf or txt
You are on page 1of 9

Research article

Feeding practices for captive giraffes (Giraffa camelopardalis) in Europe:


JZAR Research article

a survey in EEP zoos


I. Gussek1, S. Hirsch2, M. Hartmann2, K.-H. Südekum1 and J. Hummel3*

1
Institute of Animal Science, University of Bonn, Endenicher Allee 15, 53115 Bonn, Germany
2
Institute for Food and Resource Economics, University of Bonn, Nußallee 21, 53115 Bonn, Germany
3
Department of Animal Sciences, University of Göttingen, Kellnerweg 6, 37077 Göttingen, Germany
*
Correspondence: Jürgen Hummel, Department of Animal Sciences, University of Göttingen, Kellnerweg 6, 37077 Göttingen, Germany; jhummel@gwdg.de
Girafas: browsers/ramoneadores
Alimentos com compostos peletizados

Keywords: Abstract
browse, concentrate, dietary proportion, As with other browsing ruminants, the nutrition of giraffes (Giraffa camelopardalis) can be challenging.
dry matter intake, forage, produce Feeding browse in very large amounts is not feasible. Therefore, substitutes need to be provided
that have to meet requirements and the species’ digestive capacity to the greatest possible extent.
Article history: To achieve a comprehensive overview of current giraffe feeding practice in Europe, a survey was
Received: 20 July 2016 conducted among 153 member zoos of the European Endangered Species Programme. Information
Accepted: 20 January 2017 from 81 returned questionnaires showed a considerable variety of feeds being provided in varying
Published online: 31 January 2017 proportions. The use of lucerne hay (89% of zoos) and fresh browse as trees or branches (96% of zoos)
OPEN ACCESS

was more common than stated in previous studies. The use of a pelleted compound feed was almost
standard practice, but many diets additionally contained cereal grains, as concentrate feeds high in
rapidly fermentable starch. Eighty-five percent of the zoos reported feeding fresh fruits and vegetables,
even though this is not recommended due to high sugar contents with a potentially negative influence
on ruminal fermentation. The estimated non-forage proportion (sum of concentrate feeds and fresh
fruits and vegetables) in the overall dietary dry matter (DM) was 37% in summer and 43% in winter
(median), which is in accordance with recommendations. However, a considerable range of non-forage
proportions was found, with 43% of the zoos providing amounts that were likely to be exceeding 50% of
the potential daily DM intake. Data on dietary proportions revealed a geographical variation, with zoos
from Western Europe showing the lowest and zoos from Eastern Europe showing the highest proportion
of concentrate feeds in rations. An index of feeding appropriateness, oriented towards conformity with
feeding recommendations, may be useful to evaluate and improve feeding management precisely and
individually, as room for improvement was revealed for half of the participating zoos.

Introduction 2007). On the one hand, being a ruminant implies a forage fibre
requirement to maintain efficient rumen function (Van Soest
The European Endangered Species Programme (EEP) for the 1994). On the other hand, forages or fibrous feeds should match
giraffe (Giraffa camelopardalis) unites 153 giraffe facilities and the digestive physiological adaptations of browsers against the
increasing numbers of animals have been registered during the background of chemical and structural particularities of browse
last decade (Jebram 2012). Nevertheless, giraffe husbandry compared to temperate grasses (Bailey 1964; Bailey and Ulyatt
poses challenges and the European Association of Zoos and 1970; Robbins and Moen 1975; Demment and Van Soest 1985;
Aquaria (EAZA) has published husbandry and management Spalinger et al. 1986). Year-round feeding of browse in large
guidelines (EAZA Giraffe EEPs 2006). The feeding of giraffes amounts is logistically demanding in temperate zones with a
is a matter of particular interest in these recommendations, period of dormant vegetation. Appropriate substitutes need
since multiple husbandry problems in giraffes are reported to be combined in proper ratios to meet nutrient and energy
to be nutrition related (e.g. Bashaw et al. 2001; Clauss et al. requirements and to prevent pathological consequences (Potter
2006; Hummel et al. 2006a). Giraffes are classified as browsing and Clauss 2005; Clauss et al. 2006) or behavioural disturbances
ruminants (Van Soest 1988; Hofmann 1989), which are generally (Hummel et al. 2006a). The main focus in feeding instructions is
considered to be more challenging to feed in captivity compared on providing rations with sufficient amounts of palatable high
to grazing ruminants (Clauss et al. 2003; Clauss and Dierenfeld quality forage (at least 50% of diet dry matter [DM]; Schmidt

62 Journal of Zoo and Aquarium Research 5(1) 2017


Alfafa (leguminosa perene).
Família Fabaceae e Feeding practices for giraffes in Europe
subfamília Faboideae

and Barbiers 2005; Hummel and Clauss 2006). In several aspects, Table 1. Database for estimation of dry matter intake (DMI) (g/kg BW0.75/d)
lucerne shows chemical and structural characteristics similar and dietary forage-to-concentrate ratio; based on DMI calculated for 97
to browse (Hummel et al. 2006b, c), enables a comparably high giraffes in twelve German zoos.
forage intake in ruminants in general (Thornton and Minson 1973; g DMI/kg BW0.75/d
Waghorn et al. 1989) and has been shown to be better accepted
Age Status Male Female Juvenile
by giraffes than grasses (Foose 1982). In addition, browse should
be supplied for nutrient supplementation and behavioural >2.5 years Maintenance 62 59 -
enrichment (Valdes and Schlegel 2012). As an additional fibre Lactation month 1–6 p.p. – 121 –
source, dehydrated lucerne pellets are recommended (Hummel
and Clauss 2006). Energy-rich diet ingredients should be based on Lactation month 7–9 p.p. – 94 –
suitable compound feeds or components rich in easily digestible Lactation month 9–12 p.p. – 81 –
cell wall constituents, such as unmolassed sugar beet pulp. The 2.5–1.75 years Growth – – 75
use of cereal grains and commercial fruits and vegetables should
be restricted to a minimum (Hummel and Clauss 2006). Due to high 1.75–1.25 years Growth – – 83
contents of starch and sugar (Schmidt et al., 2005), any over-use of 1.00–1.25 years Growth – – 71
such feeds increases the risk of nutrition-related disorders (Potter
9–12 months Growth – – 64
and Clauss 2005; Clauss et al. 2006; Hummel et al. 2006a).
Along with current reports on feeding practice in other browsing 7–9 months Growth – – 46
ruminants (Taylor et al. 2013; Wright et al. 2011), the last overview 4–6 months Growth – – 26
of giraffe nutrition was reported by Hummel et al. (2006d) for
<4 months n.c. – – n.c.
European zoos and by Sullivan et al. (2010) for North American
institutions. Some potential for further improvements in feeding kg BW 0.75
= metabolic body size; p.p. = post partum; n.c. = not considered.
giraffes became apparent. The use of lucerne hay was confirmed
to be common by Hummel et al. (2006d), but the use of non-
forage feeds in amounts corresponding to an average proportion
of 51% of DM intake was also found. Sullivan et al. (2010) found
considerable variation in the offered forage-to-concentrate ratio
(FC ratio; a range of 18 to 77% concentrate feed in the diet as fed)
and only 65% of the facilities reported feeding browse. Almost the data collected on BW development in giraffes by Reason and
one decade later, the present nutritional survey was conducted Laird (2004). Theoretical DM intake (DMI) related to metabolic
to (1) gain comprehensive knowledge of current feeding practice body size (kg BW0.75) was estimated using our own data on DMI
in European facilities and (2) evaluate developments and trends in in giraffes (Table 1), prepared from DMI documentation in 12
giraffe nutrition. Additionally, (3) the location of zoos (west, north, German zoos based on metabolisable energy (ME) requirement
east or south of Europe) and structure of herds (number and age and the individual status (lactation, growth) of each animal. This
of giraffes) were considered to evaluate potential geographic or data base was within the range of values published on DMI in
group-specific effects on feeding practice among EEP member giraffes (Prins and Domhof 1984; Baer et al. 1985; Hatt et al. 1998;
zoos. Dinglreiter 2000; Clauss et al. 2001). If not declared otherwise,
amounts of concentrate feeds and produce offered were assumed
Methods to be completely consumed (as done by, for example, Hummel
et al. 2006d), resulting in the estimated non-forage proportion,
Questionnaire which was used to calculate the potential FC ratio.
The survey was conducted using a questionnaire (see Appendix) The classification of dehydrated lucerne pellets and the pelleted
that was sent to zoos (n  =  153) that were members of the “browse-based” product as non-forage feeds was done with
giraffe EEP. The questionnaire was divided into four sections: (1) reference to their different physical structure and irrespective of
general information on number, date of birth, sex and subspecies potential similarities in nutrient composition with lucerne hay or
of animals in a facility, (2) information on forage feeding, (3) dried browse.
information on feeding of non-forage feeds (concentrate feeds:
compound feeds, dehydrated lucerne pellets, straight feeding Index of feeding appropriateness
stuffs (single component feeds like cereal grain products or A scoring system was developed to assign an index of feeding
sugar beet pulp); produce (fresh fruits and vegetables)) and (4) appropriateness (IFA) to every facility by using the equation:
additional information on general feeding practice. Questions in
sections two and three needed to be answered separately for IFA = (2 · a) + (2 · b) + c + ∑d + ∑([% of respective concentrate
summer and winter. Zoos could give information on amounts feed in the concentrate portion in DM/100]· e) + ∑f (Table 2).
of feed either referring to one individual or to the whole group
of giraffes. Amounts were generally given as fed. For evaluating Scores included in the index calculation encoded respective
regional effects, participating zoos were sorted geographically into non-forage proportions (a; minimum [min.] -4, maximum [max.]
(1) Western Europe, (2) Northern Europe, (3) Eastern Europe, and 4 points), produce proportions (b; min. -4, max. 4 points), feeding
(4) southern Europe including the Middle East. frequencies of non-forage feeds per day (c, min. -1, max. 1
point), types of main forage in the diet (d; min. -1, max. 3 points),
Dry matter intake and forage-to-concentrate ratio composition of the concentrate portion (e; min.-2, max. 2 points)
Offered amounts of feed were standardised from volumes to and feeding of additional forage (f; min. 0, max.2 points). Due to
weights if necessary (Madgwick and Satoo 1975; BVL 2002; the high relevance of FC ratio in ruminant nutrition, variables a
Hatt and Clauss 2006; Spiekers et al. 2009; Mosig 2012) and and b were multiplied by two in the index equation. Section d
converted into DM, using standard data collections on animal refers to the proportion of a respective concentrate feed in the
feeds (Universität Hohenheim – Dokumentationsstelle 1997; DLG whole portion of concentrates in DM. Each bullet point in sections
2010; Agroscope 2013). Body weights (BW) were estimated using d, e, and f is counted individually. An increasing IFA represented

Journal of Zoo and Aquarium Research 5(1) 2017 63


Gussek et al.

Table 2. Index variables and scoring system for calculating the index of feeding appropriateness (IFA)1.
Variable -2 points -1 point 1 point 2 points
Percentage of
non-forage feeds (a) and produce (b) >70% 50–70% 30–50% <30%
in diet DM >5% 2–5% 0.1–2% 0%
Feeding of non-forage feeds per day (c) 1 time ≥2 times
Types of main forage in the diet (d) Grass hay Lucerne hay and/or Browse2 year-round
browse2 seasonal
Composition of the concentrate portion (% of % of cereal grains/100 % of compound feed and/or
concentrate feed in the concentrate portion in dried lucerne meal products
DM) (e) and/or beet pulp/100

Feeding of additional forage (f) Fresh forage3and/or


Browse ensiled/
frozen/dried
1
IFA = (2 · a) + (2 · b) + c + ∑d + ∑([% of respective concentrate feed in the concentrate portion in DM/100] · e) + ∑f, each bullet point in section d, e and f
counts individually; ∑ = addition of scores for multiple bullet points; 2Whole trees and branches; 3Fresh lucerne, nettles, blackberry, thistles, rose leaves.

increasing feeding appropriateness (evaluation scale from -12 giraffes consisted of a mean of 6 (± 3 SD; range 1–18) individuals
to 16 points). To evaluate the results, the scale was quartered which were a mean of 8 (± 2.7 SD; range 3.8–14.3) years old.
(results ≤0 points, 1 to 6 points, 7 to 11 points and ≥12 points) and
the mean index value was taken as the critical value. Diet composition
Lucerne hay was fed in 89% of the facilities, with 96% of those using
Statistical evaluation it year-round and 4% during winter time. Grass hay was fed in 27% of
Due to extreme outliers, the proportions referring to the FC ratio the facilities (only seasonally in 18% of those) and grass-clover hay
were averaged by median, and first and third quartiles are given was used in 2% of the zoos. During summer, fresh lucerne and fresh
to show variances. Other values are presented as arithmetic grass was provided in 17% and 30% of the facilities, respectively.
mean with standard deviation (SD). Seasonal differences in One facility provided fresh lucerne and grass year-long. In 2% of
forage and non-forage proportions were tested with the Tukey the facilities molassed lucerne hay was fed; grass haylage, lucerne
test and considered significant at p≤0.05. To evaluate potential silage, chopped lucerne hay or grass silage was used in single
geographic or group-specific effects (number and age of giraffes zoos only. Ninety-six percent of the participating facilities stated
in a zoo), an analysis of variance was conducted with region, that they fed fresh browse, 86% of those during summer (as leafy
number of animals and mean age of animals per group as fixed twigs and trees) and winter (as twigs and trees without leaves).
effects and comparison of least squares means of the variables Frozen browse (9%), browse silage (7%) and dried browse (31%)
forage proportion and produce proportion using the Tukey test. were used in the zoos as forage sources during winter; the latter
Subsequently, a cluster analysis was conducted for the variables was also fed year-round in four and during summer in one facility.
forage proportion and produce proportion (hierarchical method Thirty-one different types of browse were supplied in the zoos.
of Ward, 3 cluster-algorithm) and the geographical distribution of Willow was most commonly used (81% of the facilities) followed
zoos and distribution of group-specific characteristics among the by birch (51%), beech (44%), oak (44%), ash (41%), hazelnut (39%), Urtiga
clusters was enumerated. Differences between the clusters were robinia (35%), maple (22%), various types of berries (18%), fruit
tested with a Student’s t-test and considered significant at p≤0.05. trees (15%) and hawthorn (13%). Additionally, nettles (6% of the
For all variables, the respective mean values per zoo were used in facilities), blackberry, thistles and rose leaves (single facilities only)
the data base. The statistical tests were done using the program were provided as fresh summer forage. Seven percent of the zoos
SAS 9.3 (SAS Institute Inc, Cary NC, USA). Milho provided whole maize plants or maize stover during the growing
season. Forages were fed in various combinations (Table 3), with
Results the combination of preserved lucerne supplemented with browse,
or preserved lucerne supplemented with fresh forage and browse
Zoo and group information being the most common combinations. Lucerne-free forage
A response rate of 53% was achieved, representing 81 separately portions were fed in 8% of the zoos, with either grass hay/haylage
managed groups of giraffes from 22 countries. The participating or grass-clover hay being the main forage source. Two facilities did
zoos were located in Austria (1), Belgium (2), Czech Republic (4), not provide any browse.
Denmark (5), France (10), Germany (16), Hungary (2), Ireland (2), All responding zoos fed some concentrate. Almost all (96%) of
Israel (2), Italy (2), Lithuania (1), the Netherlands (8), Poland (3), the facilities stated that they used compound feed; 50% of the
Portugal (1), Serbia (1), Slovakia (1) Slovenia (1), Spain (3), Sweden products were declared to be specific for browsers or giraffes.
(2), Switzerland (1), the United Arab Emirates (1) and United Dehydrated lucerne pellets were provided in 30% and a pelleted
Kingdom (12). The geographical distribution of the responding “browse-based” product in 11% of the facilities. In 19% of the
zoos was representative for the geographical distribution of all facilities sugar beet pulp was used. Energy-rich cereal grain
EEP member zoos contacted with 65% respondents from Western products (wheat flakes, oat flakes, barley flour, corn meal, broken
Europe, 9% from Northern Europe, 16% from Eastern Europe and corn, whole corn) and fibre-rich cereal grain products (crushed
10% from Southern Europe including Middle East. The groups of oats, wheat bran, oat bran) were part of the diet in 33% of the

64 Journal of Zoo and Aquarium Research 5(1) 2017


Feeding practices for giraffes in Europe

Table 3. Combinations of forage fed in the percentage of respondent zoos.


Fresh forage (lucerne,
Lucerne hay/ chopped/ Grass hay/ grass,nettles, blackberry, Browse fresh/
ensiled/molassed haylage/silage Grass-clover hay thistle, rose leaves) frozen/dried/ensiled Fed in % of zoos
* * 40
* * * 26
* * * * 19
* * * 5
* * * 4
* * 2
* 1
* * * 1
* * 1
* * * * 1

zoos, with 26% of those feeding energy-rich, 37% combining and celery (30% each), onions and beetroot (29% each), salads
energy- and fibre-rich and 37% feeding only fibre-rich cereal grain (26%), kohlrabi (19%), herbs (10%), radish, leek and potatoes (9%
products. Nine percent of the respondents fed soybean meal and each), fennel and chard (6% each), celeriac, chicory and peppers
16% fed linseed as supplement. Additionally, “giraffe cereals” (4% each), tomatoes, cucumber, maize cob, scallions, endive and
and a “pasture mix” were used, each in one case. Regarding zucchini(courgette) (3% each) and pumpkin, spinach, aubergine,
combinations of concentrate feeds (Table 4), the exclusive use of fodder beet, garlic, cole and turnips (each in single facilities).
compound feed was most common (26% of the zoos). The next Produce was fed once per day in 43% and twice per day in 49%
most frequent combinations were feeding of compound feed with of the zoos. Three zoos stated they fed fruits and vegetables
cereal grains (14%), with dehydrated lucerne pellets (12%), with three times per day and another three zoos provided them during
a pelleted “browse-based” product (7%) or with sugar beet pulp training sessions.
(7%). The remaining 30% of the zoos provided further combinations
resulting in mixtures of up to five ingredients. Forty percent of the Dry matter intake and forage-to-concentrate ratio
zoos provided concentrate feeds once per day, 52% twice, and 7% Thirty-eight percent of the respondents gave separate information
three times, while one facility stated that it fed concentrate feeds for feeding of concentrates and produce in summer and winter
five times per day. season, respectively, but there was no statistically evident
Of all participating zoos, 85% made use of produce in their seasonal difference. During summer season a median content
giraffe diet. Fifty-three percent of those provided both fruits and (1st  quartile/3rd quartile) of 35% (23/50) of concentrates and
vegetables, 46% vegetables only and 1% fruits only. Except for five 2.2% (0.5/4.2) of produce in diet DM was estimated. Accordingly,
facilities, all zoos stated that they fed produce year-round. In the the median estimated forage content was 62% (48/72). During
produce-feeding zoos, apples (59%) and bananas (26%) were most winter season an amount of 41% (28/57) of concentrates and
commonly fed, followed by citrus fruits (9%) and others (7%). The 2.2% (0.6/4.5) of produce in diet DM was estimated and the
following types of vegetables were used: carrots (77%), cabbage median content of forage was 54% (41/69). A reasonable estimate

Table 4. Combinations of concentrate feeds fed in the percentage of respondent zoos.


Cereal grain Dehydr. lucerne Browse-based
Compound feed products Protein supplement pellets product Beet pulp Linseed Fed in % of zoos
* 26
* * 14
* * 12
* * 7
* * 7
* * * 4
* * * 4
* * * * * 4
* * 4
* * * * 2
* * * 2
Combinations fed in single facilities 14

Journal of Zoo and Aquarium Research 5(1) 2017 65


Gussek et al.

Table 5. Proportion of forage, concentrate and produce in diet dry matter (DM); based on reported amounts of non-forage feeds (concentrate and produce;
81 responding EEP zoos) and estimated proportion of forage derived from potential daily dry matter intake of the groups of giraffes during summer and
winter season.
% of dietary DM
Summer Winter
Forage Concentrate Produce Forage Concentrate Produce
Median 62 35 2.2 54 41 2.2
1 Quartile
st
48 23 0.5 41 28 0.6
3rd Quartile 72 50 4.2 69 57 4.5
Mean 58 39 2.8 53 44 2.9
SD 20 20 2.8 22 21 2.8
Minimum 2.2 2.9 0.0 2.2 10 0.0
Maximum 93 90 13 89 91 13

of DMI and FC ratio was not possible for six zoos due to feeding Particular differences between Western and Eastern European
of concentrates or produce for ad libitum intake or at a level zoos became clear, with 54% of Western European and only 15%
sufficient to meet energy requirements by concentrateand/or of Eastern European zoos being summarised in cluster 3 (high
produce offers alone. Detailed information on estimated DMI and forage proportion).
FC ratio is given in Table 5.
Index of feeding appropriateness
Influence on dietary proportions A mean index value (± SD) of 6 points (±5) was observed with
Aalysis of variance showed that the location of zoos had a a minimum score of -4 and a maximum score of 14 points. In
significant effect on the dietary forage (p = 0.003), concentrate (p a quartered scale, 13 facilities achieved a value ≤0, 31 facilities
= 0.007) and produce proportion (p = 0.020), with rations from achieved 1 to 6 points, 31 facilities achieved 7 to 11 points and
Western European zoos containing more forage (p = 0.009) and six facilities reached ≥  12 points. Taking the overall mean of 6
less concentrate (p = 0.028) than rations from Eastern European index points as critical value, 54% of the zoos were in the lower
zoos. The number or age of animals per group showed no effect and 46% in the upper half of the scale. IFA results higher than 6
on dietary proportion. The cluster analysis revealed clusters points were achieved by 59% of the Western European zoos, 38%
according to low, medium or high dietary proportion of forage of the Northern European zoos, 23% of the Eastern European zoos
(p < 0.001) or concentrate (p < 0.001), but produce proportions and 11 % of the zoos from Southern Europe including Middle East
did not differ between the clusters (p > 0.300). The number and (Table 8).
age of animals per group were likewise not different between
the clusters (Table 6). The distribution of zoos among the clusters Discussion
could be allocated based on their geographical location (Table 7).
The results of the present survey showed that feeding of giraffes in
Europe is in fact characterised by considerable variety, as previously
determined for other captive browsing ruminants (Clauss et al.
2002; Wright et al. 2001; Taylor et al. 2013). An established use of
preserved lucerne in 91% of all participating facilities, for the most
part as lucerne hay (89%), exceeds the number of zoos feeding
Table 6. Proportion of forage, concentrate and produce, number of
lucerne hay (81%) in the report by Hummel et al. (2006d) (Table
animals and age of animals in the clusters (mean ± SD; minimum/
maximum); significant differences (p <0.05) between clusters are labelled 9). In contrast, the use of grass hay decreased; less zoos made
with different letters in the same line. use of grass hay but more fed the recommended lucerne hay.
Furthermore, some zoos fed grass-clover hay that might likewise
Cluster 1 Cluster 2 Cluster 3 be more suitable for giraffes than pure grass hay due to similar
  (n = 11) (n = 32) (n = 33) patterns in fibre fractions compared to lucerne or browse species
20.8a ±11 59.5b ±8.1 73.9c ±7.9 (Jayanegara et al. 2011). During summer, 52% of the zoos in our
Forage (% of diet DM)
2.2/45.7 33.0/62.1 62.3/89.5 study used fresh forage, which is comparable to the percentage of
zoos feeding fresh forage in the survey by Hummel et al. (2006d).
Concentrate (% of diet DM) 75.5a ±12 48.0b ±7.7 23.2c ±8.0 Fresh forage did not undergo any conservation process, and thus
46.4/90.3 36.1/61.6 7.8/34.0 nutrient characteristics and energy content are higher compared
to the dried or ensiled product. However, in the former study
Produce (% of diet DM) 3.8 ±2.9 2.5 ±2.7 2.8 ±2.8
exclusively fresh grass was used, while 19% of the zoos currently
0.4/7.9 0/10.5 0/13.0
state that they feed fresh lucerne. Like its dried counterpart, fresh
5.3 ±2.7 5.9 ±2.9 5.5 ±3.6 lucerne is regarded as more appropriate for giraffes than pure
Animals (number)
1/10 2/15 2/18 grass (Hummel and Clauss 2006). Furthermore, fresh nettles,
thistles, blackberry and rose leaves were used in at least 12% of
Age (years) 8.8 ±3.2 8.5 ±2.7 7.3 ±2.4 the facilities. These unconventional fodder plants can also be good
4.4/13.9 3.8/14.3 3.9/14.3 quality complementary forage for giraffes due to similar chemical

66 Journal of Zoo and Aquarium Research 5(1) 2017


Feeding practices for giraffes in Europe

Table 7. Distribution of zoos in the three clusters according to geographical feeds like unmolassed sugar beet pulp or dehydrated lucerne
location (cluster 1 = high concentrate proportion; cluster 2 = medium pellets is additionally recommended (Hummel and Clauss 2006).
concentrate proportion; cluster 3 = low concentrate proportion). In particular, unmolassed sugar beet pulp has been reviewed as a
Cluster 1 Cluster 2 Cluster 3 suitable energy source for browsers (Hummel et al. 2003; Kearny,
(n = 11) (n = 32) (n = 33) 2005). Instead of starch it contains pectins as an easily fermentable
component of the cell wall, which shows a higher cation exchange
% of Western European
8 38 54 capacity and more even gas production during fermentation
zoos
(Van Soest et al. 1991; Jeroch et al. 1993). Nevertheless, only 16
% of Northern European facilities made use of it.
25 75 0
zoos
Whether or to what extent the feeding of produce is really
% of Eastern European
39 46 15
required for large herbivores has been discussed repeatedly
zoos (Oftedal et al. 1996; Hummel et al. 2003; Clauss and Hatt 2006;
% of Southern European Hummel and Clauss 2006). Due to high amounts of rapidly
12 44 44
zoos incl. Middle East fermentable sugar, produce shows an immediate, explosive
fermentation, which can potentially trigger acidotic conditions in
the rumen (Van Soest 1987; Oftedal et al. 1996). This was recently
shown to be the case in various zoo ruminant species fed diets high
in easily fermentable carbohydrates (Schilcher et al. 2013; Ritz et
characteristics compared to lucerne and high nutritive values al. 2014). In the present survey, 85% of the participating facilities
(Hummel et al. 2009; Nijboer pers. comm.). made use of produce as a more or less relevant diet component.
The number of zoos that provided some browse with the diet, Twenty-six percent exceeded the recommendation of at most
especially during winter, increased compared to the survey by 1% fruits in dietary DM; 16% exceeded the recommendation of
Hummel et al. (2006d) (84%) and the study of Sullivan et al. (2010) at most 4% vegetables in dietary DM (Hummel and Clauss 2006).
(65%); fresh branches and/or trees were commonly used in 96% Obviously the use of commercial fruits and vegetables is still
of the current zoos, and dried or ensiled browse was also fed in common, even though from a purely nutritional point of view, it
several facilities. Three facilities stated that they feed fresh browse should not be considered as a desirable or even necessary part
since the giraffes are able to browse from natural vegetation of the diet. The main reason for feeding fruits and vegetables
around the enclosure. Individual cases may differ, but vegetation is probably their high palatability, which makes produce useful
in or around giraffes’ enclosures is typically cropped in a short during training and medical treatments.
time and does not appear sufficient to provide a quantitatively The distribution of concentrate portions over the day is
relevant intake of browse. While this may still be advantageous for important for ruminal conditions. It must be noted that 35% of
giraffe activity budgets, foraging would be reduced to extensive the zoos provided non-forage feeds in one large portion per day,
searching for browse over fences instead of actual feed intake. which increases the probability of a considerable pH drop in the
To prevent oral stereotypies (Koene and Visser 1999; Bashaw et rumen (Hummel et al. 2006b). Feeding of concentrates (including
al. 2001; Hummel et al. 2006a) and maximise browse intake, an produce) in smaller portions has beneficial effects on rumen pH
additional supply of browse should be considered essential in the (Kaufmann 1976) and the time span for food consumption can be
nutrition of browsing ruminants irrespective of the natural browse elongated. Therefore, feeding of non-forage feeds in at least two
availability around an enclosure. portions and with a maximum time lag between feeding times is
Feeding concentrate feeds is an efficient and easy way to recommended (Hummel and Clauss 2006).
supply energy and nutrients of constant quality (Sullivan et al. The present study estimated a non-forage proportion of 37% in
2010). To improve feeding of concentrates, composition and summer diets and 43% in winter diets (median). Correspondingly,
amounts supplied need to be considered. Fortunately, the use of the amount of forage was above the limit of 50% of dietary DM
compound feeds has become more common in European zoos (Table 5) and in line with EAZA recommendations (Hummel
during the last few years. It can be assumed that these products and Clauss 2006). Therefore, the current potential FC ratio has
are mostly suitable to meet the animals’ demands with a higher improved in contrast to former results by Hummel et al. (2006d),
suitability and safety regarding rumen physiology as compared who estimated a non-forage proportion of 51%) and is in line
to pure cereal grain products. Starch as a rapidly fermentable with the results of Sullivan et al. (2010), who estimated a non-
carbohydrate is characterised by a high acidogenicity value, forage proportion of 44%. At the same time a very large variance
indicating the potential to trigger unphysiological conditions in in potential FC ratio, similar to the results of Sullivan et al. (2010),
the rumen (Menke and Steingass 1988; Van Soest et al. 1991; was observed, showing that giraffe feeding in European zoos is
Odongo et al. 2006). Therefore, the use of fibre-rich non-forage still of considerable heterogeneity. The estimated proportion

Table 8. Distribution of zoos (% of zoos) in scoring ranges in the evaluation of feeding practice using an index of feeding appropriateness (IFA) (increasing
value = increasing feeding appropriateness; evaluation scale = -12 to 16 points).
IFA scoring range All regions Western Europe Northern Europe Eastern Europe Southern Europe incl. Middle East
≤0 points 16 10 12 46 11
1 to 6 points 38 31 50 31 78
7 to 11 points 38 47 38 23 11
≥12 points 8 12 0 0 0

Journal of Zoo and Aquarium Research 5(1) 2017 67


Gussek et al.

Table 9. Feeding of forage as found by Hummel et al. (2006d) compared to half of the zoos from Western Europe and a comparatively high
information from the participating zoos in the present study. number of zoos from Northern Europe reached the upper half
Hummel et al. Present of the scale, indicating a high level of feeding appropriateness.
(2006d) study Due to considerable amounts of non-forage feeds, many zoos
from Eastern Europe could not reach a value greater than six
Grass/lucerne
index points. Based on the IFA results, feeding practices in zoos
Lucerne hay 81% 89% from Southern Europe including the Middle East appeared less
Grass hay 40% 27% positive than in the cluster analysis. Even though these zoos
showed medium to high forage proportions, feeding practice
Ensiled lucerne/grass — 4%
lacked concordance with recommendations, as grass hay and/
Browse or cereal grains were part of the diet in 90% of the facilities.
Fresh browse (trees and branches) 80% 96% Furthermore, the use of additional fresh forage was practised in
only one zoo from Southern Europe including Middle East. The
Dried/ensiled/frozen browse 4% 47%
results of the cluster analysis and the index evaluation should
Fresh forage be taken as a clear indication of differences in feeding practice
Grass 53% 31% across Europe, with higher improvement potential being visible
in zoos from Eastern and Southern Europe including Middle East.
Lucerne — 19% This raised the question of reasons for geographical differences
Nettles, thistles, blackberry, rose leaves — 12% in feeding practice. As precondition for improvement, it would
be highly desirable to further investigate if tradition, finances,
management or even some climatic causes were of reason here.
An IFA as developed in this study may be a useful tool to identify
striking and improvable factors in practical feeding management
of concentrates was a decisive variable for distance calculation of giraffe facilities, as strength and weaknesses become more
in the cluster analysis, whereas no difference was found for the clearly visible by scoring individual factors orientated on feeding
proportion of dietary produce. Obviously the use of fruits and recommendations.
vegetables is independent from other diet characteristics and
evenly represented across zoos, whereas the quantitative use of Conclusions
concentrate feeds varied between zoos.
The calculation of the potential FC ratio was done assuming The motivation of numerous zoos to participate in the survey with
the complete intake of concentrates and produce as supplied. personal queries and suggestions mirrored the high interest in
Therefore, an overestimation of the respective amount of non- issues of giraffe feeding in European facilities. A large number of
forage proportion in certain diets was possible, if the amount feedstuffs and combinations of feedstuffs were documented and
of concentrate and/or produce was particularly high and proportions of feeds varied considerably. Preferable trends and
potentially not completely consumed by the animals. This could desirable developments were clearly visible, but improvement
lead to questionable results regarding extreme outliers (Table opportunities were also obvious, as in former investigations.
5). Nevertheless, in these cases concentrates and/or produce The use of lucerne hay provided for ad libitum intake was nearly
would have been provided more or less for ad libitum intake, standard in the participating facilities and a higher percentage
which is critical. Regulation of DMI in ruminants is described as than in a previous survey supplied browse year-round. The use
happening due to energetic satiety in easily digestible diets with of fresh forage or preserved browse might be possible for more
energetic density (Conrad 1966; Waldo 1986; Jung and Allen zoos if unconventional fodder such as nettles or dried browse was
1995). Increasing dietary energy values due to high amounts of used.
concentrate and produce may therefore adversely affect forage As recommended, the estimated forage proportion represented
intake, resulting in the consumption of a lower forage proportion. more than 50% of dietary DM. Nevertheless, the potential extent
The IFA shows that 54% of all participating EEP member zoos did of non-forage feeds in the diets differed significantly, resulting
not reach a score higher than 6, and therefore there is potential in varying dietary proportions. Concentrates should be dosed
for improvement in feeding management. On the other hand, and chosen with due care. The use of pelleted compound feeds,
approximately half of the zoos showed an adequately calculated unmolassed sugar beet pulp and/or dehydrated lucerne pellets is
proportion of non-forage feeds in the diet and an extended use of recommended and at least the former was used extensively. The
various forage sources. On a quartered scale, six zoos from Western feeding of less cereal grain-based diets would be highly desirable.
Europe achieved ≥12 index points. These zoos stood out for an Even though fresh fruits and vegetables should not be part of
adequate non-forage proportion, the choice of recommended giraffes’ diets, more than three-quarters of the zoos stated they
concentrate feeds and an ambitious use of preserved browse and used them regularly. In terms of rumen physiology, produce is not
additional fresh forage in the diet. recommended for giraffes, and intake should be limited to specific
Regarding the regional distribution of zoos in the clusters purposes such as medical treatment.
(Table 7) it was noticeable that zoos from Eastern Europe were Effects of the geographical location of zoos were shown for
mainly summarised in Cluster 1 (high concentrate proportion) and dietary proportions and IFA results, with zoos from Eastern
Cluster 2 (medium concentrate proportion,) whereas zoos from and Southern Europe including Middle East revealing a higher
Western Europe were mainly summarised in Cluster 2 and Cluster potential for improvements than Western European zoos. The
3 (medium and low concentrate proportion). Apparently feeding use and advancement of an index system to evaluate feeding
concentrate in high amounts was more common in Eastern appropriateness could help to identify weakness and strength in
European zoos. Supplementary feeding of high energy feeds particular management aspects of single facilities.
could rather be assumed for Northern European facilities due
to potentially higher energy requirements for thermoregulation Acknowledgements
in the boreal area, which was not confirmed tough. Looking at Sincere thanks are given to the staff of all participating zoos for
the IFA results, and thus feeding practice as a whole, more than contributing interest and effort in answering our questions.

68 Journal of Zoo and Aquarium Research 5(1) 2017


Feeding practices for giraffes in Europe

Thanks are directed to studbook coordinator Jörg Jebram, Zoom and diversication of ruminants: a comparative view of their digestive
Erlebniswelt Gelsenkirchen, for his kind support. Additional system. Oecologia 89: 443–457.
Hummel J., Bickel D., Ziegler T. and Fidgett A. (2009) Herbaceous forages as
thanks go to Peter Müller and Sammy Geis, University of Bonn, for
components in diets of herbivorous reptiles. In: Clauss M., Fidgett A.,
assistance in technical matters. The comments of Marcus Clauss, Janssens G., Hatt J.-M., Huisman T., Hummel J., Nijboer J., Plowman A.
University of Zurich, on an earlier version of the manuscript are (eds). Zoo Animal Nutrition IV. Fürth, Germany: Filander, 105–115.
gratefully acknowledged. The study was funded by Evangelisches Hummel J. and Clauss M. (2006) Feeding. In EAZA Husbandry and
Studienwerk Villigst e.V., Gesellschaft der Freunde der Agrar- und Management Guidelines for Giraffa camelopardalis. Arnhem, The
Ernährungswissenschaftlichen Fakultät der Christian-Albrechts- Netherlands: EAZA, 29–61.
Universität zu Kiel e.V and funds allocated to the Institute of Hummel J., Clauss M., Baxter E., Flach E.J. and Johanson K. (2006a) The
influence of roughage intake on the occurence of oral disturbances in
Animal Science, University of Bonn.
captive giraffids. In: Fidgett A., Clauss M., Eulenberger K., Hatt J.-M.,
Hume I., Janssens G., Nijboer J. (eds). Zoo Animal Nutrition III. Fürth,
References Germany: Filander, 235–252.
Agroscope (2013) Schweizerische Futtermitteldatenbank (online). Accessed Hummel J., Hörhager A. and Nawrocki D. (2003) Wählerische Laubfresser
25.11.2014: http://www.feed-alp.admin.ch/fmkatalog/katalog/de/ – Angemessene Ernährung von Giraffen und Okapis im Zoo. Zeitschrift
html/unit_78.html (in German). des Kölner Zoos 46: 67–80 (in German).
Baer, D., Oftedal O. and Fahey G. (1985) Feed selection and digestibility by Hummel J., Pfeffer E., Nørgaard C., Johanson K., Clauss M. and Nogge
captive giraffes (Giraffa camelopardalis). Zoo Biology 4: 57–64. G. (2006b) Energy supply of the okapi in captivity: fermentation
Bailey R.W. (1964) Pasture quality and ruminant nutrition. New Zealand characteristics of feedstuffs. Zoo Biology 25: 251–266.
Journal of Agricultural Research 7: 497–507. Hummel J., Südekum K.-H., Streich W.J. and Clauss M. (2006c) Forage
Bailey R.W. and Ulyatt M.J. (1970) Pasture quality and ruminant nutrition. fermentation patterns and their implications for herbivore ingesta
New Zealand Journal of Agricultural Research 13: 591–604. retention times. Functional Ecology 20: 989–1002.
Bashaw M., Tarou L., Maki T. and Maple T. (2001) A survey assessment Hummel J., Zimmermann W., Langenhorst T., Schleussner G., Damen M. and
of variables related to stereotypy in captive giraffe and okapi. Applied Clauss M. (2006d) Giraffe husbandry and feeding practices in Europe:
Animal Behaviour Science 73: 235–347. Results of an EEP survey. 6th Congress of the European Association of
BVL (2002) Mittlere Gewichte einzelner Obst- und Gemüseerzeugnisse. Zoo and Wildlife Veterinarians, Budapest, Hungary. EAZWV, 71–74.
In: Datenerhebung. Compiled by Prüße U., Hüther L. and Hohgardt Jayanegara A., Marquardt S., Kreuzer M. and Leiber F. (2011) Nutrient
K. Braunschweig, Germany: Bundesamt für Verbraucherschutz und and energy content, in vitro ruminal fermentation characteristics and
Lebensmittelsicherheit (in German). methanogenic potential of alpine forage plant species during early
Clauss M. and Dierenfeld E. (2008) The nutrition of “browsers”. In: Fowler summer. Journal of the Science of Food and Agriculture 91: 1863–
M.E. and Miller R.E. (eds). Zoo and Wild Animal Medicine: Current 1870.
Therapy Vol. 6. St. Louis, Missouri, USA: Saunders Elsevier, 444–454. Jebram (2012) European Studbook for the Giraffe (EEP), 7th edn.
Clauss M. and Hatt J.-M. (2006) The feeding of rhinoceroses in captivity. Gelsenkirchen, Germany: Zoom Erlebniswelt Gelsenkirchen.
International Zoo Yearbook 40: 197–209. Jeroch H., Flachowsky G. and Weißbach F. (1993) Futtermittelkunde. Jena,
Clauss M., Kienzle E. and Hatt J.-M. (2003) Feeding practice in captive Germany: Gustav-Fischer Verlag (in German).
wild ruminants: peculiarities in the nutrition of browsers/concentrate Jung H.G. and Allen M.S., (1995) Characteristics of plant cell walls affecting
selectors and intermediate feeders. A review. In: Fidgett A., Clauss intake and digestibility of forages by ruminants. Journal of Animal
M., Ganslosser U., Hatt J.-M., Nijboer J. (eds). Zoo Animal Nutrition II. Science 73: 2774–2790.
Fürth, Germany: Filander, 27–52. Kaufmann W. (1976) Influence of the composition of the ration and the
Clauss M., Kienzle E. and Wiesner H. (2002) Feeding practice in moose feeding frequency on pH-regulation in the rumen and on feed intake
(Alces alces) husbandry. Tierärztliche Praxis 30: 408–418 (in German). in ruminants. Livestock Production Science 3: 103–114.
Clauss M., Lechner-Doll M., Flach E., Tack C. and Hatt J.-M. (2001) Kearny C.C. (2005) Effects of Dietary Physical Form and Carbohydrate
Comparative use of four different marker systems for the estimation of Profile on Captive Giraffe. Masters thesis. Gainesville, Florida, USA:
digestibility and low food intake in a group of captive giraffes (Giraffa University of Florida.
camelopardalis). Zoo Biology 20: 315–329. Koene P. and Visser E.K. (1999) Tongue playing behaviour in captive giraffes.
Clauss M., Rose P., Hummel J. and Hatt J.-M. (2006) Serous fat atrophy Proceedings of the First International Symposium on Physiology and
and other nutrition-related health problems in captive giraffes (Giraffa Ethology of Wild and Zoo Animals, Berlin, Germany, 106–111.
camelopardalis). An evaluation of 83 necropsy reports. 6th Congress of Madgwick H.A.I. and Satoo T. (1975) On estimating the aboveground
the European Association of Zoo and Wildlife Veterinarians, Budapest, weights of tree stands. Ecology 56: 1446–1450.
Hungary. EAZWV, 233–235. Menke K.-H. and Steingass H. (1988) Estimation of the energetic feed value
Conrad H.R. (1966) Symposium on factors influencing the voluntary intake obtained from chemical analysis and in vitro gas production using
of herbage by ruminants: Physiological and physical factors limiting rumen fluid. Animal Research and Development 28: 7–55.
feed intake. Journal of Animal Science 25: 227–235. Mosig M. (2012) Fütterungstechnik. In: Dittrich L. (ed.). Zootierhaltung –
Demment M.W. and Van Soest P.J. (1985) A nutritional explanation for Tiere in menschlicher Obhut (Grundlagen), 9th edn. Frankfurt am Main,
body size patterns of ruminant and non-ruminant herbivores. The Germany: Harri Deutsch, 231–250 (in German).
American Naturalist 125: 641–672. Odongo N.E., Valdes E.V. and McBride B.W. (2006) Technical note:
Dinglreiter S. (2000) Eine Feldstudie über die Fütterung ausgewählter Acidogenicity potential and rumen acid load of common zoo animals
Zoowiederkäuer. Dissertation. Munich: Ludwig-Maximilians-University feed. The Professional Animal Scientist 22: 194–199.
Munich (in German). Oftedal O.T., Baer D.J. and Allen M.E. (1996) The feeding and nutrition
DLG (2010) Datenbank Futtermittel der DLG (online). http://datenbank. of herbivores. In: Kleiman D.G. (ed.). Wild Mammals in Captivity:
futtermittel.net/vorauswahlVolltext.do (in German). Accessed 25 Principles and Techniques. Chicago, USA: University of Chicago Press,
November 2014. 129–138.
EAZA Giraffe EEP (2006) EAZA Husbandry and Management Guidelines for Potter J.S and Clauss M. (2005) Mortality of captive giraffes (Giraffa
Giraffa camelopardalis. Arnhem, Netherlands: Burger’s Zoo. camelopardalis) associated with serous fat atrophy: a review of five
Foose T. (1982) Trophic Strategies of Ruminant Versus Nonruminant cases in Auckland zoo. Journal of Zoo and Wildlife Medicine 36: 301–
Ungulates. Dissertation. Chicago, USA: University of Chicago. 307.
Hatt J.-M. and Clauss M. (2006) Browse silage in zoo animal nutrition - Prins R.A and Domhof M.A (1984) Feed intake and cell wall digestion by
feeding enrichment of browsers during winter. In: Fidgett A., Clauss okapi (Okapia johnstoni) and giraffe (Giraffa camelopardalis). Der
M., Eulenberger K., Hatt J.-M., Hume I., Janssens G., Nijboer J. (eds). Zoologische Garten 54: 131–134.
Zoo Animal Nutrition Vol. III. Fürth, Germany: Filander, 201–204. Reason R. and Laird E. (2004) Weight gain and growth in captive juvenile
Hatt J.-M., Lechner-Doll M. and Mayes B. (1998) The use of dosed and giraffes (Giraffa camelopardalis). Animals Keepers Forum 31: 106–
herbage n-alkanes as markers for the determination of digestive 109.
strategies of captive giraffes (Giraffa camelopardalis). Zoo Biology 17: Ritz J., Codron D., Wenger S., Rensch E.E., Hatt J.-M., Braun U. and Clauss
295–309. M. (2014) Ruminal pH in cattle (Bos primigenius f. taurus) and moose
Hofmann R.R. (1989) Evolutionary steps of ecophysiological adaptations (Alces alces) under different feeding conditions: a pilot investigation.

Journal of Zoo and Aquarium Research 5(1) 2017 69


Gussek et al.

Journal of Zoo and Aquarium Research 2: 44–51. digestibility of legume and grass diets in sheep. Australian Journal of
Robbins C.T. and Moen A.N. (1975) Composition and digestibility of Agricultural Research 24: 889–898.
several deciduous browses in the Northeast. The Journal of Wildlife Universität Hohenheim–Dokumentationsstelle (1997) DLG-Futterwert-
Management 39: 337–341. abellen für Wiederkäuer, 7th edn. Frankfurt am Main, Germany: DLG-
Schilcher B., Baumgartner K., Geyer H. and Liesegang A. (2013) Investigation Verlag (in German).
on rumen health of different wild ruminants in relation to feeding Valdes E.V. and Schlegel M. (2012). Advances in giraffe nutrition. In: Miller
management. Journal of Zoo and Aquarium Research 1: 23–30. R.E. and Fowler M. (eds). Fowler’s Zoo and Wild Animal Medicine: St.
Schmidt D.A. and Barbiers R. (2005) The Giraffe Nutrition Workshop Louis, Missouri, USA: Saunders Elsevier, 612–618.
Proceedings. Chicago, Illinois, USA: Lincoln Park Zoo. Van Soest P.J. (1987) Soluble carbohydrates and the non-fiber components
Schmidt D.A., Kerley M.S., Porter J.H. and Dempsey J.L. (2005) Structural of feeds. Large Animal Veterinarian 42: 44–50.
and nonstructural carbohydrate, fat, and protein composition of Van Soest P.J. (1988) A comparison of grazing and browsing ruminants in
commercially available, whole produce. Zoo Biology 24: 359–373. the use of feed resources. In Increasing small ruminant productivity
Spalinger D.E., Hanley T.A. and Robbins C.T. (1986) The assessment of in semi-arid areas: 67–79. Thomson E.F., Thomson F.S. (Eds.). Aleppo,
handling time in ruminants: the effect of plant chemical and physical Syria: ICARDA.
structure on the rate of breakdown of plant particles in the rumen of Van Soest P.J. (1994) Nutritional Ecology of the Ruminant, 2nd edn. Ithaca,
mule deer and elk. Canadian Journal of Zoology 64: 312–321. New York, USA: Cornell University Press.
Spiekers H., Potthast V. and Nussbaum H. (2009). Erfolgreiche Van Soest P.J., Robertson J.B. and Lewis B.A. (1991) Methods for dietary
Milchviehfütterung. Frankfurt am Main, Germany: DLG-Verlag (in fiber, neutral detergent fiber, and nonstarch polysaccharides in relation
German). to animal nutrition. Journal of Dairy Science 74: 3583–3597.
Sullivan K., van Heugten E., Ange-van Heugten K., Poore M.H., Dierenfeld Waghorn G.C., Shelton I.D. and Thomas V.J. (1989) Particle breakdown
E.S. and Wolfe B. (2010) Analysis of nutrient concentrations in the diet, and rumen digestion of fresh ryegrass (Lolium perenne L.) and lucerne
serum, and urine of giraffe from surveyed North American zoological (Medicago sativa L.) fed to cows during a restricted feeding period.
institutions. Zoo Biology 29: 457–469. British Journal of Nurition 61: 409–423.
Taylor L.A., Schwitzer C., Owen-Smith N., Kreuzer M. and Clauss M. (2013) Waldo D.R. (1986) Effect of forage quality on intake and forage-concentrate
Feeding practices for greater kudu (Tragelaphus strepsiceros) in UK interactions. Journal of Dairy Science 69: 617–631.
collections as compared to diets of free-ranging specimens. Journal of Wright D.J., Omed H.M., Bishop C.M. and Fidgett A.L. (2011) Variations in
Zoo and Aquarium Research 1: 7–13. eastern bongo (Tragelaphus eurycerus isaaci) feeding practices in UK
Thornton R.F. and Minson D.J. (1973) The relationship between apparent zoological collections. Zoo Biology 30: 149–164.
retention time in the rumen, voluntary feed intake, and apparent

70 Journal of Zoo and Aquarium Research 5(1) 2017

You might also like