Osmotic fragility of desert bighorn sheep red blood cells

0300.9629

Cmnp. Brochem. Physiol.. Vol. 64A. pp. 161 to 175 0 Pergamon Press Ltd 1979 Printed m Great Britam

OSMOTIC

FRAGILITY RED

OF DESERT BIGHORN BLOOD CELLS

79.0901-0167102

00.0

SHEEP

JACK C. TURNER Department

of Zoology

and Physiology, (Receiced

University

of Wyoming,

22 November

Laramie,

WY 82071, U.S.A.

1978)

Abstract-l. Desert bighorn sheep, Otis canadensis cremnobates, exposed to 5 days dehydration lost 17-22x of their body weight which they were capable of replacing within 1 hr after water was made available. 2. Dehydrated bighorn tolerated a 48% loss of their initial plasma volume. After less than 4 hr postrehydration, more than 50% of the lost plasma volume was replaced. 3. The absorption of water from the postrehydration rumen occurred at moderate rate (l-2 l/hr) with 13% of the initial postrehydration fluid volume absorbed during the first hr of rehydration. Within 9 hr postrehydration, less than 50% of the imbibed rumen volume remained. 4. The osmotic fragility of the desert bighorn’s RBCs improved with increased dehydration. Control values for 50% lysis in hyposmotic saline decreased from 77 mM NaCl to 68 mM NaCl after 5 days dehydration. 5. Plasma concentration increased from 304 mOsm/l to 345 mOsm/l after dehydration and became regulated to control levels 4 hr postrehydration. 6. Red blood cell osmotic concentrations remained constant at an average of 252 mOsm/l during dehydration, rising to 279 mOsm/l 1 hr postrehydration and achieved control levels 5 hr postrehydra&on.

INTRODUCTION Penninsular cremnobates,

desert

bighorn

sheep,

Ouis

(Choshniak & Shkolnik, 1977; Perk, 1963, 1966; Yagil et al., 1974c). Rumen volume of the desert bighorn approximates 18% of the total body water (Turner, 1973) and differs little from that of other ruminants (Hecker et al., 1964). Imbibed water, once taken into the rumen, is disseminated into the blood and other fluid compartments with considerable fluidity (Turner, 1973; Wells & Wells, 1961). This potentially exposes the desert bighorn’s RBCs to osmotic stress similar to that experienced by the camel and Bedouin goat with the rapid flux of water from the rumen to the circulatory system. However, the RBCs of domestic, xeric adapted breeds of sheep are more fragile than those of either the camel, goat or human (Evans, 1961; Perk et al., 1964; Schalm, 1967). Consequently, the mechanism(s) by which the desert bighorn tolerates the large amounts of water entering the blood stream during rapid rehydration are presumably different than those demonstrated for either the camel or Bedouin goat.

canadensis

in the low, arid, are sparsely distributed precipitous mountains of the Sonoran and Baja Deserts of southwestern North America. Due to their size (6&l 10 kg) they must tolerate the environmental extremes of seasonally high air temperatures and radiant heat loads combined with decreases in food and water availability. Much of the year the desert bighorn can survive on the preformed and oxidative water found in its diet, however, the escalated demands for water, commensurate with the advance of summer temperatures, requires an additional influx of water resulting in a dependence upon surface sources of water. They require a minimum of 4-S’% of their body weight per day (Turner, 1973). Frequently, during the summer months, bighorn go without drinking for periods of 515 days (Turner, 1973; Wells & Wells, 1961) resulting in a loss of at least 20% of the hydrated body weight (30% total body water) (Turner, 1973). Similar to the camel (Schmidt-Nielsen et al., 1956) and the Bedouin goats (Choshniak & Shkolnik, 1972) the desert bighorn is capable of briefly consuming sufficient water at one visit to a waterhole to restore the lost body water. Presumably, the capacity for rapid rehydration is adaptive in reducing the time an animal is susceptible to predation at a waterhole (Schmidt-Nielsen, 1964). The camel, Bedouin goat and other desert ungulates, lose body fluids at the expense of maintaining a constant blood volume and osmolality (SchmidtNielsen, 1964; Shkolnik et a[., 1972, 1975; Yousef et al., 1970). Their ability to tolerate dehydration and rapid rehydration has been related to the tolerance of their red blood cells (RBCs) to osmotic stress

MATERIALS AND METHODS Captive desert bighorn sheep (3 VF: 13) averaging 47 kg body weight (35-51 kg) were kept under ambient environmental conditions in an open corral enclosure at the P. L. Boyd-Deep Canyon Desert Research Station, near Palm Desert, California. The bighorn were maintained under continuous veterinary supervision on a ration of Alber’s Roundup (Carnation Co., Inc.) and alfalfa hay offered once a day (ration according to Siegmund, 1967); water and shade were available ad libitum. The four bighorn were individually denied free water for 5 days at summer ambient temperatures ranging from 3%45”C and a relative humidity of l&29%. Bighorn had access to shade and, therefore, were able to behaviorally thermoregulate during the dehydration regime. Postdehydration, bighorn were allowed water ad Ii&turn for 1 hr. 167

0 5. cremnabates

/

1-1

I

POSTREHYDRATION

(HRS)

Fig. I. Rumen tltud YoIumc (range ;tnJ mean) 01 -1 dewrt bighorn sheep after 5 day\ crf chronic &hydration IbcforL’ drinking). immediately aft~ drinking 10 hri. and :It 2 /jr IW tcr\:lls ;liirr rlrlnkin~

0 cremnobates _~c --~

34 i

DEHYTROL. DRATION CON-

POST-

HtHYDRATlON CHRS)

Fig. 2. Hematacrit values (range and mean) of 1 &set-t bighorn sheep when watered ~rd lihitctrrl (control). alter 5 days chronic dehydration. :tnd at hpecified time increments after being allowxi 1~1drink lyc)rtrehytlratiorI).

Osmotic fragility of desert bighorn sheep red blood cells

100

0.~. cremnobotes i

169

Table 1. Concentration of NaCl (mM) which produced 50”/, hemolysis of desert bighorn red blood cells during the dehydration regime. Control values are not signifi-

cantly different from values obtained on day I or 2. Day 3 values differ significantly (P < 0.05) from control vjalues

Fig. 3. Plasma volume (range and mean) of four desert bighorn sheep when watered ad libitum (control). after 5 days chronic dehydration after being allowed

and at specified time increments to drink (postrehydration).

values, 77 (SE + 1.71) nm NaCl (138 mOsm/l). Dehydration decreased the mean critical hemolytical volume (V,) from 1.98 to 1.93 after 5 days dehydration. No significant variation occurred in V, during the first 2 days of dehydration. However, V, values differed significantly (P < 0.01) from control levels on days 3 and 4. Values for V, on day 5 of dehydration were highly significant from controls (P < 0.001). V, did not change significantly between days 3 and 4. Rehydration did not completely (68%) restore V, to control levels during the postrehydration examination period. Plasma concentration averaged 304 mOsm/l for control animals and did not change significantly (306mOsm/l) during the first 2 days of dehydration. However, the plasma concentration increased (P d 0.05) an average of 13 mOsm/l.day-’ to a mean of 345 mOsm/l (337-350 mOsm/l) after 5 days of the dehydration regime (Fig. 5). This was an increase of 137: above control values. The RBC cytoplasm osmotic concentration remained constant and considerably below that of the plasma during dehydration, averaging 252 mOsm/l, which was similar to the control values (Fig. 6). One hr after drinking, the plasma concentration was decreased by 50% of the dehydration gain to a concentration of 325 mOsm/l. Control plasma concentrations were again achieved 4 hr postdehydration. RBC osmolarity increased significantly (P < 0.001) above control values to 279mOsm/l 1 hr postrehydration. During the second hr the RBC lost almost SO’/;, of the first hr gain, and continued to decline through the fourth hr. achieving predehydration levels 5 hr after drinking. control

DISCUSSION

The varying levels of summer dependence on surface water by most large desert ungulates to maintain

Animal No.

Control

I 2 3 4 r

75 77 76 79 77

Day of dehydration I 2 3

4

5

76 76 78 79 17

71 67 69 70 69

70 67 67 68 68

77 77 75 76 76

73 71 73 72 72

water homeostasis has been well documented (Choshniak, 1972; Maloiy, 1970, 1972; Rosenmann & Morrison, 1963; Schmidt-Nielsen, 1964; Schoen, 1968; Shkolnik et al., 1975; Taylor, 1969a,b). The desert bighorn is no exception to the general trend (Blong & Pollard, 1965; Halloran & Deming, 1958; Jones et al., 1957; Turner, 1970, 1973; Wells & Wells, 1961). Only the dik-dik (Madoqua kirki), oryx (Oryx heisu), the eland (Tuurotarugus oryx) and Grant’s gazelle (Gaze/la granti) are known to be free from summer drinking since they satisfy their water demands by feeding at night on dew enhanced vegetation (Buxton, 1924; Taylor, 1968, 1969a,b, 1970; Tinley, 1969). The extent to which a desert ungulate is restricted by a source of free water is related, in part, to the animal’s tolerance to dehydration and ability to economize its avenues of water loss. The advantage ruminants have over other desert mammals is the expansive rumen complex which is capable of containing a large volume of water, 10-309: of the total body water (Hecker et al., 1964) which most desert ruminants are capable of consuming at a rapid rate (Choshniak & Shkolnik, 1977; Maloiy, 1970, 1972; Schmidt-Nielsen, 1964; Turner, 1970, 1973). Rapid rehydration from extended periods away from water can reduce the amount of time exposed to predation at a waterhole (SchmidtNielsen, 1964), the osmotic shock of a large amount of water rapidly absorbed from the gut into the circulatory system can result in hemolysis. The camel’s rumen volume contributes 149, to the total body weight. When experiencing dehydration, the camel draws upon the cellular and alimentary fluids to supply 307: and 50”; of its water demand, respectively. Similarly, the desert bighorn’s rumen volume constitutes almost 20% of the total body water (1 l”/, total body weight) and suffers the greatest depletion of any of the various fluid compartments during dehydration. After 5 days dehydration the rumen fluid becomes reduced by SOP,,, the lost fluid contributing to almost half of the total water loss (Turner, 1973). The first 2 days of water deprivation, rumen fluid contributes almost the total water loss, Only after 607; reduction in the initial rumen volume do fecal and evaporative mechanisms directed toward water conservation become effective. The ruminal-alimentary thyme averages 831,) water in most animals (Macfarlane. 1964). Since rumen water contains about llOm-equiv/l Na+, it is most likely that the Na+ is excreted when alimentary water is mobilized to meet physiological demands. Sheep and the camel excrete increased amounts of Na+ dur-

VI 60 ;ii 2 40 5 I 20 lri 0 8 100 a 80 60

60

Fig. 4. Osmotic fragility curves [or the RBCs of 4 desert bighorn sheep. Open symbols (0) are control values, solid symbots (0) are vaiues from animals dehydrated for 5 days. The hemolysis produced in the various mM NaCl concentrations is expressed as a percent of the maximum hemolysis produced by sonication. Dehydration values for osmotic fragility are significantly different (P < NJ0ii from control levels in individual bighorn.

ing dehydration (Macfariane QI 1972; Turner, 1973). The rate water ts absorbed from the rumen greatly determines the extent the red blood cells are exposed to the potential of hemofysis. The rapid absorption of water from the rumen appears to be proportional to the correlated functions of water and oxygen turnover (Macfarlane et nl., 1963: Macfartane PI al., 1971: Macfarlane & Howard, t972; Mullen. 19731. Half time vaiues for the equilibration of tritiated water (t,J moving from the rumen to the circulatory system are 0.5, l-2 and 3-4 hr for cattle, sheep and the camel respectively (Macfartane & Howard, 1972). Rumen Auid of the desert bighorn is transferred to the circuiatory system at a tl:2 vdiue of 0.5-0.75 hr which corresponds to a flux of I -2 l/hr (Turner, un-

published data). The Bedouin goat. however, extublts no appreciable change in the ruminal fluid volume during the first hr of rehydration and only a slight volume change within the next several hr (Choshniak & Shkolnik, 1977). Similar to the Bedouin goat, the domestic sheep absorbs water from the rumen at a slow rate, 300 ml/hr (Parthasarathy & Phillipson. 1953). The rate of water absorption from the rumen, and presumably the remainder of the alimentary tract, not only depends upon the initial gut contents and fill, but also upon the hydration of the animal. The slow absorption of ruminal wafer by hydrated animals conveys the ability to subsist for days {weeks) without necessitating return to drinking water. The duration of the freedom from water is predicated upon the ani-

Osmotic

fragility

of desert bighorn

sheep red blood

171

cells

Q.c. cremnobates

350 1

I

control

I I

I

I

I

I

I I I I I 3 4 5 6 7 POSTREHYDRATION (HRS)

I

I

I

2 3 4 5 DAY OF DEHYDRATION

2

I

I

8

9

Fig. 5. Plasma concentration (range and mean) of 4 desert bighorn sheep when watered ad libitum (control), on each of 5 days of chronic dehydration and hourly for 9 hr postrehydration.

mal’s capacity to (1) parcel rumen and alimentary fluid to meet the physiological demands and (2) tolerate the physiological stress imposed by dehydration. Once dehydration has reduced the various fluid compartments to their physiologically tolerable limits, rehydration would provide its greatest adaptive value by occurring rapidly once water has been imbibed.

Rapid absorption and rehydration would allow for the quick recovery of an otherwise languid animal whose condition might predispose it to predation or render it incapable of tolerating additionally imposed environmental stress. The rumen fluid, therefore, is an important component in the adaptive strategy of desert ruminants to equiponderate the physiological

r Q.E. pmnobatea

I

I I 1 I:

i?i 260 g 0 0

T

B 250

I 240

I

control

I I

I

I

I

11

2 3 4 5 DAY OF DEHYDRATION

I

1

2

I l 11 1 3 4 5 6 7 POSTRE!lYDftATlON (HRS)

l 8

l 9

Fig. 6. Osmotic concentration of RBCs cytoplasm taken from desert bighorn sheep experiencing water (control), and measured daily during 5 days of chronic dehydration and hourly for 9 hr during the postdehydration period (after drinking).

rrd libirum

172

.14(h: c

demands of dehydration in thermally stressful CI~vironments. Except for the camel. hematological values for most wild ungulates are undescribed in the literature. Camel. domestic sheep. Rocky Mountain and desert bighorn blood differs in numerous physiological and morphological avenues (Franzman & Thorn. 1970; Yagil at crl., 1974a.b: Blunt. 1975: Turner. unpublished data). Seasonal hematocrit changes have been observed in both the camel and desert bighorn (Turner. 1973: Yagil ef trl., 1974b). A summer hematocrit decrease of 11”” for both animals in concert with the camel’s stable plasma volume and the expanded plasma and blood volumes of the bighorn allows for a greater fluid (water) volume to be available to cope with the fluid dynamics of dehydration. Sheep, in general, are capable of tolerating reduced plasma volumes amounting to 44”,, and 4X”,, for domestic sheep breeds and desert bighorn. respectively. However. tolerance to a reduced plasma volume is not restricted to the ovine group. The guanaco. Llumtr yumicoe (a New World camelid). is also capable of enduring dehydration induced plasma volume losses (Rosenmann & Morrison. 1963). By contrast. this circulatory resilience is not shared by the burro and the camel who maintain a relatively constant plasma volume when dehydrated (Charnot. 1960; Schmidt-Nielsen et ul.. 1956: Yousef rt rrl.. 19701. With the exception of the camel. RBCs from dehydrated bighorn are significantly more tolerant to osmotic shock from buffered saline solutions than are other ungulates for which comparable data are available (Table 2). The 50”;, lysis value for desert bighorn RBCs occurs at 68 mM NaCI, 18 mM NaCl greater concentration than observed for the camel. The low IO”,, hemolysis value for donkey RBCs suggests this animal could surpass the bighorn’s capability to tnlerate osmotic stress. However. conflicting values for RBC fragility for the same species in separate studies suggests difficulties in comparing data from studies of differing methodologies. The osmotic fragility of RBCs from indicidually considered bighorn differed significantly (P < 0.001) from control values (Fig. 4). However. if values for osmotic resistance are considered collectively (Figs 7, 8) the level of significance decreased (P C 0.05):

Animal Camel Desert Bighorn Oxen Bedoum Goat Camel Donkey Domestic Cou Horse Domestic Sheep Domestic Goat

II

K\lK

although still ~igmticantl> diitcrclir 11111n ~\)ntioi \alucs. the le\cl of signiticance drhcrihing change\ 111 physiologlcal paramctci-\ \\hcn iliinc ,niall \amplc sires should hc guarde2

Tolcrancc

of RBC‘\ 10 o\mot~~ \trcss

tc and

the hemoglobin t! pe of domcxtic \hcep ha no al’parcnt effect on the RBC l’ragilit). the Hugh potashium er! throq tc t)pe IHK-type1 po\jcssed hy the highorn empart5 ;I reduced rcsistancc to o\molic shock than 111 sheep with I lo\% potaGum crythrc)c,yte tkpc. ILK-type (Evans. 1961 ), Howc~er. the HK-t>pe cell\
type cells. Desert bighorn RBC‘a arc \IT~I~;II-III ‘~IIC 10 those of domestic breeds of cheep. They arc somewhat thicker and not 50 disc-shaped ;I\ arc human RBC’\ Their 45 ji3 MCV is about one-third larger than that of the camel. Ilnlike the RBC\ ,)f the camel uhich become reduced in volume aith dehydration. dc\crt OI- ,lightl! inbighorn RBCs mamtain ;i contrail creased MCV. The reduced si/e 111rhc camel RBC‘ is attributable to water loss which L‘;III &cr~:~se ~)\IIIOtic fragility and acconini~~datt icll cypim\ion Jurlng rchydratinn (Yagil 1’1ii/ I c)74cl The factor of expan\~on to nl:iiunum \~~lutne 10 which an RBC can c\pand brforc lysis (I,) gi\e\ .~n The human RB(’ ha5 ;I L; index of ccl1 rcsilicnc\ of I .X bvhereas the I, ;<,I control R BCs of the camel is 2.3 IYagil or (~1.. 1974~) and I OX for the desert hip horn. The critical hcmol!trc volume is significantI>

Hemolysis IO”,, 50”,, mM NaCl h2

50

IO?

fix

95 125 3X’ X6* ‘)4* Y4’ YY* ‘)9*

is related

cell \i/e and shape. membrane characteristic5 hemoglobin tpz (Perh (11 ~rl.. 1064). Although

90

I IO

Yagil (‘f trl., 1974, Presen( stud) Bianca. 1970 Clm\n~;~h& Sh’h
* Data given as point hemolysis begins (RBC minimum resistancel. This value was taken to be equivalent to the IO”,, hemoly+ values reported elre~ here

Osmotic fragility of desert blghorn sheep red blood cells ,OO

0,~

173

cremnobates

90 80-

/I

E $!I? 702 3 k Y g

6050-

/

I

4030ZO-

1 160

150

140

I30

120

100

I10

90

80

70

60

50

40

mM NaCl Fig. 7. Osmotic fragility curve for RBCs from 4 hydrated desert bighorn sheep. The range and mean of hemolysis produced in the various buffered saline solutions is expressed as a percent of maximal hemolysis produced by sonication.

100

Q. g. cremnobates

80

m

cn 70 ?I : I: I2 8 fj

60 50 40

160

150

140

130

120

110

100

90

80

70

60

50

40

mM NaCl Fig. 8. Osmotic fragility curve for RBCs from 4 dehydrated desert bighorn sheep. The range and mean of hemolysis produced in the various bufi’ered saline solutions is expressed as a percent of maximal hemolysis produced by sonication.

t P .. 0.05) reduced The duced

decrease changes

Differential has

blood 1976:

been

in RBC‘s from

is presumably in the tissue

RBC

due

to

Ho\% phenomenon

to

animals.

dehydration

in-

membrane.

hematocrits

hypothesized

dehydrated

(plasma

cuplain

(Asnno.

skimming)

regional

various

1973:

Idcura

(‘I 01..

Jodal & Lundgren. 1968. 1970: Lemmingson, 1972: Pappenheimer & Kinter. 1956: Rownblum. 1973). Embryological and gross anatomical consider-

atic)ns concerning the tract indicates, not only

the regionalization

\asculature

of

the

digestive

considerable similarity within of the gut of ;I given species. but

a similarity of architecture between most \ertebratc endothcrms. It has been demonstrated that a hematocrit gradient from high to low (30 40”,, dilrerencc) exists between the intestinal muscularis and mucosa. particularlq the villi, of the intestine. respectively (Jodal Xc Lundgren. 1968, 1970). The gradient could serve to protect RBCs from lysiz due to hyposmotic changes in the lumen contents. A similar mechanism could bc postulated for the entire ruminant gastrointestinal ((2.1.) tract, particularly the rumen. Plasma skimming in the lower G.I. tract could serve to mawimize absorption or water from alimentary thyme. allow for rapid absorption of water from the upper G.I. tract (rumen) yet protect RBCs from hyposmotic

Iysis. Reduced oxygen availability due to decreased RBCs could be compensated by greater oxygen affinity and hemoglobin,

loading unloading characteristics of the i.e., HK-type RBCs. Similarly, increases in plasma osmolarity (Fig. 5) would allow for an increased rate of transfer of water from the (2.1. tract and thereby facilitate rapid rehydration and allow for volume expansion before critical greater plasma hcmolytic concentrations are achieved. Such ;I mech-

anism gains impetus by the observation that severe heat stress reduces blood Roa to the rumen (Hales. 1973) yet water absorption from the gut appears not to be impaired.

Physiology. Dlwsion of Basic Research. University of Wyomine and NSF Grant DEB 76.21414 are acknowle&ed fcyr their support. The P. L. Boyd-Deep Canyon

Desert Research Station, University of California. Riverside. CA. Living Desert Association, Palm Desert. CA, and California Department of Fish and Game are thanked for their logistical support and research permits. I am most grateful to Drs Kennington. Bagdonas and Harlow for their critical review of the manuscript.

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(1973)

On

plasma

cutaneous microcirculation Phniol. 35, 424425.

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in man

observed

and rabbits.

Jap.

in J.

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in

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