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TITLE

Physiological adaptation for milk production' in desert ruminants

FIKAL REPORT FOR THE PERIOD

1977-12-15 - 1980-12-14

AUTHOR(S)

A. Shkolnik

INSTITUTK

Tel Aviv University , Department of Zoology Tel Aviv, Ramat Aviv Israel

INTEPKATIONAL ATOMIC ENEPCY ACEMCY

"" DATE August 1981 l

Water Metabolism and Productivity in the Black Bedouin Goat, The Nubian Ibex and the Desert Gazelle

Final Report to the International Atomic Energy Agency Contract No. 2138/RB

Investigators:Pro£. A. Shkolnik Dr. I. Choshniak Dr. E. Maltz Department of Zoology, university of Tel Aviv ISRAEL - l -

Prinking capafi fry in dgserfc harbivores- In areas where food rssources are meager and water holes are widely spaced, the ability of an herbivore to withstand water deprivation largely determines its stocking rate. Animals able to graze far away from water holes can exploit the desert pasture evenly and are consequently more efficient (Schmidt- Nielsen, 1958; Squires, 1973). Complementary to this characteristic is a drinking capacity large enough to enable a desert animal, dehydrated as it might be, to rapidly replenish the water lost during its continuous grazing in the arid desert. Such a capacity was first described in the camel (Schmidt- Nielsen, 1956) and later in the Somali donkey (Maloiy, 1970). Both these desert-adapted herbivores, whan given free access to drinking water following severe dehydration, imbibed volumes of water than amounted to 25-30% of their body weight. Voluir.~r.ous drinking (up to 15-2056 of body weight) was also described in the guanaco (Rosenman and Morrison, 1960), in cattle (Siebsrt and Macfarlane, 1975) and in sheep (Macfarlane, 1968). In 1972 a capacity for rapid rehydration that exceeded even that described for the camel was first reported for a breed of black goats herded by the Bedouins in the extreme deserts of the Middle East (Shkolnik et al., 1972). In the Megav desert of Israel, in eastern Sinai and in the Hejaz these small body sized goats (15 - 22 kg.) may often be observed grazing in the dry sun-scorched desert even at two days walking distance from any water source. When observed upon their arrival at a water hole, th«s« goats have often been seen to imbibe volumes of water that - 2 - often exceeded 40% of their dehydrated body weight (Table 1). Soon after quenching their thirst, several minutes after arrival at the water hole, the goats usually embarked again on a grazing trip of several days in the barren desert. Applying the dilution method, tritiated water (HTO) and Evans Blue (T-1824) were used to respectively assess the total body water and blood plasma volumes in the Bedouin goats.. Follow- ing drinking, HTO space measured in 10 goats amounted to 16% of their body weight and Evans Blue (E.B.) space to 6.8% of their body weight (Fig. 1). Following 4 days of water deprivation in the desert environment the animals lost 28 + 0.3% of their body waight. Both HTO and E.B. spaces were at that time still well within the range considered "normal" even for mammals fully hydrated (Hix et al.f 1959; Richmond et al., 1962; Siebart and Macfarlane, 1976). Throughout the period of water deprivation, however, the body solids of the goats were maintained at the initial value. Animals that "store" water. Th* volume of water consumed by the goats during their short visit to the water hole was sufficient to replenish the entire loss from the prolonged grazing period and to reestablish the body water content at a level higher than chat reported for mammals in general. This high body watercontent we regarded as a "store" that is utilized during the time of water deprivation. Throughout the cycle of dehydration - rehydration that conti- nues unceasingly in the desert, the goats continue to eat and maintain their regular activity. In no case was hemoIysis or other ill effects observed following the voluminous drinking. n r - 3 -

Osmotic stability of red blood cells - a mechanism undarlvinq drinking capacity of desert "herbivores? A possible trait, offering an explanation of the desert animals' capability for rapid rehydration was first suggested for the camel by Pork (1963), Bianca (1970), Yagil (1974) and others. These authors related this capacity of the camel to the high osmotic stability of its red blood cells when sub- J merged in a hypotonic solution, a characteristic first described by Ponder et al in 1928. Surprisingly enough, the osmotic stability we found in the red blood cells of the goats was very low (Table 2), but similar to that found in other bovids, whether living in the desert or inhabiting mesic and humid areas. A comparison of the osmotic stability of red blood cells in a variety of different herbivores indicates that similarities in their osmotic stability can be more significantly related to the taxonomic-phylogenetic grouping of animals than to their ecophysiological pattern. Furthermore, the change in plasma concentration during the entire dehydration-rehydration cycle, that amounted to only 33.6 mOsm Kg-1 made us wonder whether the osmotic stability of the red blood cells is at all challenged under in vivo conditions in this goat (Table 2). Osmotic changes recorded in the donkey and the camel following their dehydration were also of small magnitude. Water retention in the rumen; a wav to circumvent hazards likely to follow rapid re.1 /dration. Schalk and Amadon in their "study of the dynamic factors of bovide rumen" published in 1928, pointed out that the raticulo- - 4 - rumen may play a role in controlling the distribution o£ water a ruminant consumes. Employing X-ray techniques, Nand and Singh (1941) found that most of the water imbibed is first retained in the rumen and only a small fraction, less than 10% of it, directly passes to the omasum. Hecker et al. (1964) used phenol red dilution in serial determination of changes in the ruminal fluid of Merino ewes. They concluded that "the water balance of the body proper is kept virtually unaltered by fluids drawn from the alimentary^tract during the first day of water deprivation, and that for this reason the rumen may be regarded as a water store in sheep". Following this line of thinking we too conducted serial determination of the rumen's fluid content in our goats, bsfora and following drinking (Choshniak and Shkolnik, 1977). Animals with chronic ruminal canulae were used and Cl EDTA was amployed as a non absorbable marker (Hyden, 1961; Warner and Stacy, 1968). Five hours following voluminous drinking 81% of the volume consumed was still retained in the reticulo-rumen complex. During this time the concentration of the ruminal fluid, that was 90.6 mOsm.Kg immediately following drinking, increased to 131.4 mOsm.Kg"1. The rate of flow through the reticulo omasal orifice, that is, the passage of fluid from the rumen to the more permeable parts of the gastro-intestinal tract (Engelhardt, 1969) was assessed by calculating the rate of disappearance of the C EDTA between injections, as was suggested by Warner and Stacy (1969). From a value of 73 ml per hour during the first hour following rehydration the outflow from the rumen increased continuously to - 5 - a rate of 250 ml h"1 during the fifth hour (Fig.3). Whan dehydrated goats consumed saline instead of tap water the outflow during the first hour amounted to 600 ml. The increase in E.B. space that was recorded following the drinking of saline considerably exceeded that recorded in the same animal following the drinking of tap water. Changes in plasma concentration in both cases were similarly minor. Presumably a factor related to the osmotic difference between the ruminal and body fluids controls the outflow from the rumen and adjusts its rate, in order to avoid osmotic shocks that are likely to follow the consumption of volumes of water that are equal to some.80% of the animal's total body water content. It is suggested therefore that the rumen, commonly regarded as a specialized compartment of the gut related to cellulose digestion, plays a major role also in the water economy of desert ruminants. It provides the essential mechanism without which a desert herbivore would not have been able to "store" water and circumvent the hazards likely to follow rapid rehydration. fiffat3 ypfsus iboxos and gazelles. At this point we were interested in finding out whether th«i wild ruminants, sharing the same desert area with the goat, possess similar adaptive responses to those of the Bedouin goats. In the areas mentioned there are two such species, both haVing a body size similar to that of the goat. The ibex (Capra ibex nubiana) a closes relative of the goat, lives on the steep escarpments bordering tha Dead Sea and the Rift valley further south, as well as steep canyon walls in adjacent territories. Shaded shelters 1 - 6 -

are available to these animals throughout the day. Field zoolo- gists have observed that several ibex populations move closer to water sources once the pasture dries out. The other species, the Dorcas gazelle (Gazella dorcas) may ba seen on open plains, on flat wide wadi beds and barren basins between mountains, where no effective shade is available. They are often seen tens of miles away from any water source. Hand-reared ibexes, dorcas gazelles and goats were kept outdoors in open pens exposed to desert climatic conditions. The animals were fed dry alfalfa hay, were watered once daily and maintained a constant body weight. Daily water consumption was measured and HTO was applied to assess water turn-ovsr (WTO) from the dilution rate of the tritium in the animals' body fluids. Water consumption was 116 ml per Kg body weight per day in the goats, 65 in the ibexes and 37 in the gazelles (Table' 4). The goats were found to have a turn-over of 140 ml water per kg body waight per day, the ibsxes 76 ml and the gazelles only 58 ml. After a coupl* of weeks under the regime describad, no water was offered to the animals fed on the dry diet mantioned. All ths animals, deprived of drinking water, lostwaight (Table 5),. The highest loss was recorded in the goat, the lowest in the gazelle. The hierarchy represented here reflects the differences in WTO previously described. 4 days following last drinking all animals were in good condition. On the fifth day gazelles and ibexes lost their appetite and tha experiment was terminated by offering water ad. lib to all animals. The goats and gazelles fully rep- lenished their loss after one continuous drink; the ibex failed l - 7 -

to do so. When changes of body solids ware assessed, it was found that 4 days of water deprivation had no effect on the body solids of the goats and the gazelles, while the ibexes lost 10% of their solids (Table 6). In addition to HTO, markers were employed to assess the distribution of the fluids in the different body compartments. Of these, the changes in blood plasma volume is of particular interest and is relatively well documented in ehe literature. The ability of the camel to maintain its blood plasma volume in face of great loss from other compartments, has given rise to the idea that this phenomenon is characteristic of desert mancnals (Macfarlane, 1964; Schmidt-Nielsen, 1967). This is certainly not the case with the Bedouin goat, as all body compartments contributed equally to the loss to. the environment (Table 6). Nevertheless, because of the high initial values, total body water and plasma volume are maintained within limits normal to mammals in general, even with a loss of 30% of the initial body weight (Fig.l). Because the water lass is evenly distributed from the entire body water pool, the osmotic conse- quences of the loss are minimised in spite of the large total water loss. Body water content in ibexes and gazelles when fully hydrated amounts to 72 and 70 % of body weight respectively - a level normal to mammals in general. Their Evang« Blue volume is only 4.5% of their body weight. In their case, conserving water is more essential than for goats, and maintenance of their blood plasma volume i» crucial. This is, however/ achieved ac the expense of L - 8 -

other compartments. In conclusion, both Bedouin goats and gazelles can withstand prolonged periods of water deprivation equally well. _The ibexes, as would be expected from their more favourable habitat, are less capable in this respect. The adaptive mechanisms which Bedouin goats and gazelles employ to achieve this end are, however, basically different. The Bedouin goat "stores" water and maintains a relatively high water turn-over; the gazelle con- serves water and maintains blood plasma volume at the expense of other water compartments. • Water turnover corresponds to energy metabolism and therefore also to production. The significance of selecting, through the process of domestication, a breed capable of maintaining high production and consequently a high water turnover even in the desert is obvious. In contrast, the gazelle and ibex are more vulnerable to predation and other ,hazards and obviously cannot afford "storage" and are better adapted for survival in the wild. "Storing" water for producing milk. The milk yield that the Bedouin goats were found to produce (Maltz and Shkolnik, 1971) is several times greater than the volumes measured in the ibexes and the gazelles (Table 7). This capacity of the goat supports our suggestion to relate its faculty of "storing" water and maintaining a high water turnover to its high productivity in the desert. Milk production adds a considerable burden to the water economy of a mammal. In a high milk producing ruminant this burden is obviously large. As if to meet their extra need for L r 1 r

-9-

water, the lactacing goats "increase" their "storage" and HTO space was found to average 83% of their body weight. This enlarged water storage helps them to avoid becoming highly dependent on frequent drinking when a high caloric demand is also imperative. Indeed, following two days of continuous grazing without drinking, the goats still maintained enough fluid to maintain their high milk production (Fig. 5).

The ailk yield we found in the Black Bedouin goat matches that reported for highest producing ruminants (Shkolnik et al. 1980). Being indigenous to the desert environment and highly adapted to it, we believe this goac possesses special potential for the development of desert dairy farming. Table I-. Water consumed by Bedouin goats following period of water deprivation (12 qoatsf n = 27) .

Body weight Dehydrated Vol.ccnsumed Vol. consumed B.W. - (as %-of ; (Kg) (Kg) (L) : oehyd. B.W.)

Mean 17 .65 V" 13.11 4.3 30 . 10 ±.S.E. 1.42 o.ea 0.27 1.43 Range 8.2-28.1- 5.85-22.7^ 2.0-7.1 19.1-44.2

(From Choshniak and Shkolnik, 1977) r

Table 2 ' Osmotic fragility of red blood cells in NaCl Solutions of various concentrations, as reported by different authors for a variety of mammals, a-Ponder et al. (1923). b - Perk, 1964. c - Yagil et al. 1974. ol - "Wie

Concen. (mM) at which Heaolysis occurs Animals Ref. . Beginning Maximal SO5;

CAMELIDAE Camel (C. dromedarius) 47 a it if u 51 36 b ti n n 68 47 SO C " (C. bactarianus) 45 a Llama Q. lama) 47 a " (L. pocas) 47 a Guanaco (L. huanacus) 60 35 47 d EQUIDAE Donkey 92 60 b Donkey .. 110 70 9S d Horse .92 53 b BOVIDAE Cow 100 65 b Sheep (Awassi) 130 90 115 d ' Goat 112 75 b Mountain Goat 130 90 117 d ! i -l.

Somali donkevs and Bedouin croats.

Animal Dehydrated to Following Reference 70% initial rehydration body weight

CMMlS 340 290 Hoppe at al., 1975

M 320 289 Yagil et al . , 1974 Somali donkey« 345 298 Maloiy and Boarer . 1971. Bvdouin goats 336 302 Choshniak and Shkolnik, 1977. Table 4. Prinking water and water turnover in desert ruminants.

Animal Body Weight Drinking , W.T.O. , tl/2 Kg ml (kg..day)" ml (kg.day)" days

Goats 23.5 116.0 140.7 3.2 Ibaxes 22.9 64.6 75.6 5.0 Gazelles (Dorcas) 16.8 37.4 57.9 3.7 Table 5. weight loss during 4 days of water deprivation and drinking capacity following rohvdration in desart ruminants.

Animal Body Weight Weight loss Drinking capacity kg kg % of init. liters Aver. Max.

Goats 23 7.0 30 5.8 8.0 Ibexes 23 4.5 20 2.1 3.1 Gazelles (Dorcas) 17 2.3 14 2.2 2.6 Table 6. changes (in % of initial values) of body weight, body solids. and body fluids in desert ruminants following 4 days of water deprivation.

Animal Body Weight HTO space E.B. space Body solids

Goats 76.4 66.7 50.8 100.5 Ibexes 86.1 74.5 66.8 90.7 Gazelles (Dorcas) 88.7 78.9 84.0 109.0 Table 7. MiUf yield anrt mi IV gonstifaignts (gr per kg bodv weight per dav) of Bedouin goats, ibaxas and desert gazelles

(Mean + S.D.)

Animal« M B.W. Milk Total Protein Fat Lactose kg yield solids

Bedouin goats 23.1 86.28 10.85 2.79 3.68 3.74 4 +2.5 ±8.49 ±1.07 +0.27 +0.36 +0.37

Ibexes 30.3 21.10 4.34 1.16 2.54 0.90 6 +6.3 +8.13 +1.67 ±0.43 +0.95 ±0.34

Gazelles 20.6 27.21 6.64 2.41 2.41 1.55 4 +2.8 +3.26 +1.66 +0.60 +0.60 +0.39 Figure legend

Flg. 1. Body weight, total body water, plasma volume and bodv | sol Ids of normally watered, after 4 days of water deprivation and ia-adiately following drinking, 1n 10 Bedouin goats.. Numbers in bars Indicate * of body weight (x + SD). !

FIg. 2. Rucrinul fluid volune in Bedouin goats after dehydration and rehydratlon (From Choshniak and Shkolnik 1977).

Fig. 3. Outflow of fluid from the rumen to the intestines in Black Bedouin goats following the drinking of tap water and following the drinking of saline (From Choshniak and Shkolnik, 1977).

Fig. 4. U change of plasma volume (Evans 31ua Space) as measured in iJlack ueeouin ooats during rehydratlon following the drinking of tap water and following the drinking of saline (From Choshniak and Shkolnik, 1977).

F1g. 5. Body weight, HTO and Evans Blue spaces (x + SO) 1n lactating goats (*r4), watered daily (N) and following 4 days of water deprivation (D). (From Maltz and Shkolnik, 1930). L^ r

Kg. 16

76.3±2.i 68.8±2.2

Normal Dehydration Rehy drat ion

dl HTO space ESO T-1824 space O Solids laoal Drinking volume n. 13 6 in 4 animals t 4 i T , T , i 1 I i T ; 1 1 T 1 : 4 • t 3 • i "3 C 'l 2 T ! £ 1 j - -

it o— \ Ol 35 i t * drinking Time after drinking (hr) i * •j Jr* • 2- Ö00|- CZl Tap water y- O 03% NaCI. I ~

~ ^1 ;

c 400 - O) 1 T n r I - r. '; t i Hi M J 200 '•? ': ** 1 I ! O ( I •i Ii : 1n "ft k.. 1 1 I ; 0-1 1-3 3-5 0-1 1-3 3-5 Time after drinking (hrj •

30 v

~w» \ Tap water n «u • . E":il Q9 NaCI n*6 't i i 1 ^" i 20 M *• . ***!^ S- JT "3 "i a : i "1 • M -r : JS r' y Q. f •• ; O J•m i C- j I 10 I ' (C s i •M U I 1 ) k_A I X Ij. 1

[ j i T • C • I ' ir I I If f * J 1 -L ! f. ;• '

Time after drinking (hr.) 1

Kg space

E.B space

10 83.507,

72.18%

7.28% 3.77%

N l

References

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Maltz, E., and Shkolnik, A., 19f9. Milk production in the desert: Lactation and water economy in the Black Bedouin goat. Physiol. Zool. (in g»u.g»K ?1 •1 I'/^ Maloiy, G.M.O., 1970. Water economy of the Somali donkey. Am. J. Physiol. 219:1522-;1527. Maloiy, G.M.O., and Boarer, C.D.H., 1971. Response of the Somali donkey to dehydration: hematological changes. Am . J. Physiol. 221:37-41. Macrarlane, W.V., 1964. Terrestrial animals in dry heat: Ungulates, in: Handbook of physiology. Adaptation to the Environmant. Washington O.G., Am. Physiol. Soc. Sec. ... 4, VOl-I!509-539. . Macfarlane, W.V., 1968. .Comparative function of ruminants in hot.environmants, in: Adaptation of domestic animals. Hafez, .E.S.E., (ed.). Lea and Febiger, Philadelphia. Sand, P.N. and lingh, .&. ,..1941. ~A_ study.of .the factors governing tha passage of fluid» through .the stomach. Indian.J. Vet. Sei.. 11.-16-27. Perk, K., 1063. Tho camel's.orythrocytes*. Haturo, 200:272-273. Ponder, E.. Yeager, J.F; :and. Charipper, H.A;-,> 1928. Studies in comparative haematology. L, Canelidae. Quart. J. l:xp. Physiol. 19:116-126. Richmond, C.R., Langham, W.H. and Trujillc/, T.T., 1962. Comparative metabolism of tritiated water by mammals. J. CeI. Physiol., 59:45-53. r-

Rosenmann, M., and Morrison, P. R., 1963. The physiological response to heat and dehydration in the guanaco, Llama quanicoe. Physiol. Zool., 36:45-51. Schalk, A.F. and Amadon, R.S., 1928. Study of the dynamic factors of bovine rumen. N. Dak. Agric. Exp. Sta. BuI. 216. Schmidt-Nielsen, B., Schmidt-Nielsen, K., Houpt, J.R. and Jarnum, S.A., 1956. Water balance of the camel. Am. J. Physiol. 185:185-194. Schmidt-Nielson, K., 1964. Desert animals: Physiology problems of heat and water. Clarendon Press, Oxford, England. Schmidt-Nielsen, K., 1958. Animals and arid conditions, Physiological aspects of productivity and management in: The Future of Arid Lands pp. 368-382. The Am. Asoc. Adv. Sei. Washington, D.C. Siebert, B.D. and Macfarlane, W.V., 1975. Dehydration in desert cattle and camels. Physiol. Zool. 48:36-49. Shkolnik, A., Borut, A. and Choshniak, I., 1972. Water economy of the Bedouin goat. Symp. Zool. Soc. London. 31:229-242. Shkolnik, A., Borut, A., Choshniak, I. and' JIaltz, E., 1975. Water economy and drinking regime of the Bedouin goat. Ecological research on development of arid zones. Israel-France. Vulcani Centre, Special Publ. 39:79-90. Shkolnik, A., Maltz, E., Gordin, S. 1980. Desert condition and goat milk production. J. Dairy Sei. 63:1749-1754. Squires, V.R., 1973. Distance to water as a factor in performance of livestock in arid and semi arid rangeland. Proc. Symp. Water-Animal Relations. 28-33.