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Riedesel, M. L.

L977.

OF BATS VOLIN,{E 651p.

Blood Physiology Chapter 4 pp 485-517 In BIOLOGY III, William Wimsatt, Editor. NY: Academic Press.
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Chapter 4 elood Physio!ogy Ried.esel, M. L. Ig74 PP 485-517 Tn BIOLOGY 0F Chapter BATS Volume I I I , I\Ii 11i am Wims att , Editor. Academic Press, NY. 651P.

Bl,ood Plrysiology
Mansin L. Ried.esel

I. Introduction ..... II. FormedElements ....... III. Blood pH and Gases lV. WaterandElectrolytes..... V. Lipids,Carbohydrates, andProteins A.Lipids B. Carbohydrates C. Proteins Relerences

..., 4g5 ....,.489 . . . . 500 ....500 .,.,.. 509 .....510 ..... 511 ... 511 .... 514

I.

Introduction

Application of conditions of stress to biological systems is frequently a tool employed by interested biologists describing physiological systems. The characteristics of a system can often best be made apparent by pushing the system to its physiological limit. During the course of evolution there apparently have been innumerable situations in which the physiological systems of bats have been pushed to extremes in a wide variety of directions as evidenced by the wide variety of specialists among bats. Authors of other chapters have noted that bats comprise animals adapted to (l) restricted diets (insects, nectar, blood, etc.), (2) cold, (3) heat, and (4) locomotion, ranging from extreme acrobatic and swift flight to sustained migratory flight. The biological diversity of bats becomes all the more impressive when one reflects that all of this diversity is accomplished
485

486

MARVTN L. RTEDESEL

by mammalian

organisms. Remembering, of course, that mammalian cel1s require a constant environment, homeostatic mechanisms, which are characteristic of mammals, have been and currently are placed under considerable stress in

bats. Chiroptera, more than any other mammalian order, provides an opportunity to examine physiological systems operating under diverse conditions. Among bats there are animals that can exceed or at least equal the capacity of any other mammal to (l)mobilize energy within a brief period of time,
(2) tolerate high rates of water loss through evaporation, and (3) concentrate urine. These remarkable characteristics emphasize the fact that blood composition and chemistry may be the result of physiological systems adjusting under considerable stress. The extent of physiological adjustment is determined not only by the extent of environmental stress but also by remarkable integration of diverse behavioral, physiological, and biochemical activities. An example of the physiological diversity of these mammals is given by considering some of the features of a few insectivores, vampires, and fish-eating bats. The necessity to spend considerable time without food or water plus periods of rapid energy expenditure and high water loss are examples of environmental
stresses imposed on vampires, insectivores, and fish-eating bats. The vampire and

the insectivorous bats take in large amounts of food at a single feeding. A


30-gm vampire may consume 50% of its body weight. The 7-gm little brown bat may eat 2 Io 4 gm of insects within 20 to 30 minutes in captivity and 1 or 2 hours in nature. This iarge, single intake of food places extreme demands on the circulatory system, osmotic-regulating system, excretory organs, and water balance. Whereas the insectivorous bat drinks free water, the vampire may drink under some circumstances (Crespo et al., 1961), but can be kept in captivity for

without drinking free water (McFarland and Wmsatt, 1969'). Apparently the kidney can compensate for the behavioral difference of drinking and not drinking. The physiological characteristics which are responsible for the rapid mobilization of nutrients involved in absorption and storage of large meals have not been described to date. The fact that arginase and carbamylphosphate synthetase concentration in liver tissue of the big brown bat (Eptesicus fuscus) and the little brown bat (Myotis lucifugus) is the highest recorded for any animal (Cohen and Brown, 1960) is an example of the vast amount of physiological data which is yet to be learned from the study ofbats. High rates of evaporative water loss are associated with flight among bats. This is particularly true of the bat that has just eaten a meal equivalent to 25% or 5O% of its body weight. The evaporative water loss reported by Carpenter (1968) for bats in flight, on a per gram body weight basis, exceeds the evaporative water loss for all other mammals. A wide range of renal activity is perhaps best exemplified in studies conducted on Desmodus rotundus murinus by McFarland and Wimsatt (1969).
several years

4.

BLOOD PHYSIOLOGY 487

There was a tenfoid increase in osmotic concentration of urine, a sixfold increase chloride concentration, and nearly a 100-fo1d increase in volume of urine flow (Fig. 1) following consumption of large amounts of food. Most small mammals feed frequently, but this is not necessarily true of many bats' Long intervals between feeding is common among vampire bats (McFarland and wimsatt, 1969). Insectivorous bats usually feed once or twice per 24 or more hours. In view of the periodicity of feeding and the large food iniake (20% to 40% body weight) associated with each feeding, the rapid food passage

in urine

to
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Fig. L Chronological relationship between the rate of urine flow, the osmotic, the chloide, and the ured concentration of vampire bot urine cluring and foilowing feeding
(reproduced from McFarland and wimsatt, 1969 with permission from pergamon press).

488 MARVIN L. RIEDESEL


through the gastrointestinal tract is impressive (Table I). The absorption of nutrients from the gastrointestinal tract and deposition of nutrients in storage
depots place stringent demands on the circulatory system. These requirements can result in rapid changes in blood chemistry. Data collectedonMyotisvelifer to be presented in Section V and Table X describe these bats as being capable of increasing oxygen consumption by as much as 130-fold while confined to small chambers. Assessment of environmental stresses, rapid food-passage time, and oxygen-consumption data support the hypothesis that there must be a great capacity for change in blood morphology and biood chemistry of bats. Thus, bats are choice experimental animals for mammalian physiological studies. Despite their small size these mammals tolerate a wide range of environments and severe metabolic demands. How can the physiological systems of bats maintain the "constant milieu," a characteristic requirement of a specialized mammalian cell? This question has stimulated biologists to study bat blood composition and chemistry. I shall try to point out some of the innumerable challenges and opportunities which exist in the field for present and future investigation. A statement I am tempted to make too many times throughout this chapter is that there are limited data available, therefore I say it now and hope readers wiil bear in mind this important limitation and challenge' Early in the preparation of this manuscript the objective was to present the physiological uuiu.r fo'. the morphology and chemistry of bat blood collected under standard or natural conditions. Unfortunately, such an objective had to be abandoned because (1) there is a lot of variation in the time interval between time of capture and time of taking blood samples, and (2) there is a vast difference in the laboratory procedures utilized. Attempts have been made to indicate whether blood samples were collected in the laboratory or in the field. The data plesented are leplesentative of the literature but certainly not inclusive. Some data are not included because they were collected under very special circumstances, for instance, various times of day and various elevations. My
TABLE

I.

FOOD.PASSAGE TIME THROUGH GASTROINTESTINAL TRACT


Passage

Time (min)
Quiet bats
Reference

Species

Active

bats

Myotis lucifugus Nyctalus noctula


Eptesicus fuscus Molossus major Chilonlt c teris rubiginosa (=Pte/onotus parnellii)

3s-54
28

122-t60

90
15 15

Buchler,1975 Cranbrook,1965 Luckens et al., l97l

Klite, 1965 Klite, 1965

4.

BLOOD PHYSIOLOGY 489

apologies to authors for omissions in this compilation. Serious investigators should seek the original publications referred to in this chapter and thereby obtain nearly complete coverage of these subiect matters. Thus, rather than presenting standard values for bat blood analyses, a rather comprehensive sampling with considerable emphasis placed on the various aspects of bat biology and bat habitat which may result in modification of blood morphology and blood chemistry is given.

II.

Formed Elements

Biologists who have studied the formed elements in the blood of bats would most certainly be unanimous in pointing out or recognizing the extreme importance of the following facts regarding collection and interpretation of data. (1) The small mass and relatively large surface area of many bats make them susceptible to dehydration. (2) Collecting blood from carotid artery, leg vein, brachial artety, heart puncture, or open heart may account for data differences as great ar 50%. (3) Activity of the spleen of some bats undoubtedly results in marked (as much as 50%:) changes in the number of circulating elements. (4) Circadian rhythms may result in great differences in data, particularly because bats may frequently be in cool environments and have low body temperatures. (5) Differences in blood values among species may vary as much as their diets and habitats do. (6) Subclinical diseases and malnutrition may be prevalent

among recently captured bats. (7) A great deal of fundamental knowledge regarding principles of hemodynamics could be learned by studying the formed elements in blood and the circulatory systems of bats. Most reports on the number and size of erythrocytes and white blood cellsin active bats give values similar to those reported for other small mammals (Baker and Kline, 1932; Worth, 1932; Evans, 1934;Martinez, 1939a,b,1941; Quay and Reeder, 1954; Lidicker and Davis, 1955; Quay and Miller, 1955; Krutzsch and Hughes, 1959; Kallen, 1960; Krutzsch and Wimsatt, 1963: Mitchell, 1966; Sealander, 1964; Andrew ,1965; Dunaway and Lewis, 1965). Hibernation, flight, dehydration, and feeding habits of bats are important variables considered in
some studies (Eiiassen and Egsbaek, 1963;Davis et

al., 1967).

The data on formed elements of bat blood presented in Tables II and III are representative of the literature. Differences in techaique, experimental conditions and the extent of pooling samples from several bats make it difficult to compare data from different investigators. However, the data in Tables II and III present a compilation that can be an aid in understanding bat hematology. The range of erythrocyte counts from 8.14 million to 14.25 million can be expected for animals whose body weights range from 7 to 50 gm (Andrew, 1965).

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species have a wide range of erythrocyte counts. Until data on the rate of hemopoiesis and of mobilization of erythrocytes become available from hemopoietic tissues, I assume the 50% to 100% changes in erythrocyte counts are a lesult of storage of erythrocytes in the spleen and perhaps the peripheral vascular beds. Handling bats can result in gross activation of the sympathetic nervous system during collection of blood samples. High sym-

Apparentiy most bat

pathetic activity can cause splenic constriction, and dilation of arterioles in

membranous wings and skeletal muscle. studier and Ewing (I97 1) reported on hematocrit, percentage of body water, spleen weight, and kidney weight of Myotis lucifugus and the tropical M. nigricans. The hematocrit and percentage of water of M. lucifugus did not change during the course of a day, although body weight loss exceeded 16% of initialbody weight. There were changes in the hematocrit of M. nigricans, but no changes in body weight, percentage of body water, spleen weight, or kidney weight. The data reported by Valdivieso and Tamsitt (l9ll) are of particular interest and are reproduced in Tables IV, V, and VI. These data are unique because (1) they represent samples on a wide variety of bats, and blood samples wele collected by the same technique, namely, venipuncture from the wing or interfemoral membrane; and, (2) they represent most of the hematological data collected on bats from the American tropics. Except for the lepolts of Martinez

(!939a,b, 1941) on three species of Mexican bats (the frugivorous phyliostomatid Artibeus jamaicensis, the sanguivorous vampire Desmodus rotundus, and the insectivorous molossid Tadqrida brasiliensis), there are no othel data
available on Amedcan tropical bats.

chiropteran biology often tends to regard the tropics as representing an apparent "ideal" habitat for bats. The large incidence ofhemopathology (valdivieso and Tamsitt, 1911), including (1) polychromatophilia @5-g3%); (2) normoblasts (22-33%); (3)basophilic granules in erythrocytes; and (4) Cabot rings (19-33%), usually present only in anemias, suggest there are adverse aspects of the envilonment which produce these hemopathological data' The higit incidence of this type of pathology may be an important factor in keeping bat populations down to their current leve1 in the American tropics. The only other report of polychromatophilia among bats was reported in 3 of 15 Myotis lucifugus examined by Worth (1932). She acknowledged that these little brown bats were not in very good physical condition. As noted by valdivieso and Tamsitt (1911), additional studies ale needed to clarify the extent ofpoor nutritional states in tropical bats. The 1ow erythrocyte counts,3.9l to 7.75 x 106 per mm3, in frugivorous bats (Table V) when compared with insectivorous bats, 14.33 X 106 per mm3, is not easy to explain. Valdivieso and Tamsitt (lglD suggest that temperature regulation and body size may be correlated with erythrocyte count. I propose that anatomic features of the circulatory system,

The student

of

4.

BLOOD PHYSIOLOGY 493

particularly those involved in blood hemodynamics, are more apt to correlate with erythrocyte counts. The circulatory demands in darting insectivorous bats and hopping sanguivorous bats are different still. Pregnancy and lactation are usually thought to make severe demands on the circulatory system. However Valdivieso and Tamsitt (1911) were unable to demonstrate a statistical difference (P > 0.05) in hemoglobin concentrations, hematocrit, or differential counts between lactating, pregnant, and nongravid
bats.

There is great variation in the leukocyte and differential counts reported in III. This is most likely to be the result of subclinical disease processes or of natural day-to-day fluctuations. Some variation may be reduced when more data on domesticated animals or animals housed under standard laboratory conditions become available. The data collected in the field are of particular value because despite the variation they are representative ofthe physiology ofbats in their natural habitats. Although data on the erythrocytes indicated some disease or malnutrition among recently captured bats, most of the white blood cell data do not suggest prevalence of disease or infection. The large standard error of the mean values implies that a few bats have high white blood cell counts. However, the general pattern of low, mean white blood cell counts supports the lack of evidence of infection indicated by the differential counts. The leukocyte response of bats may be similar to antibody response, which is minimal. The importance of environmental stresses on the blood picture of bats has been examined by Martin (1973). She collected hematological data on cold-exposed and isolated bals of Myotis lucifugus and has correlated the hematological changes with the General Adaptation Syndrome (Selye, 1950). The conclusions from this study are summarized in Fig. 2. As more data become available, it will be interesting to learn to what degree capture and initial exposure to laboratory conditions represent a stressful situation for various bats. Eventually we may be able to quantitate the stress animals experience in their natural habitats by examining hematological data. Dehydration and nutritional conditions of the animals are variables often neglected and not apparent in the data presented in Tables II-V. I believe differences which were at first thought to be species differences are in reality due to differences in time between capture and sample collection and other variables which influence the extent of dehydration, starvation, and the overall nutritional condition of the animal. Studies conducted within the past l5 years describe a reduction @V 5O%)in the number of circulating red and white blood cells during hibernation. These observations appear to contradict the classic description given by numerous investigators that the blood of the hibernating animal is viscous (Aeby, 1875; Dubois, 1896). The high viscosity of the blood during hibernation must be the
Table

494

MARVTN L. RTEDESEL

TABLE

IV.

HEMOGRAMS OF NEOTROPICAL BATSA Hemoglobin concentration (e/100 m1)

Locality
Species

Sex and state

No.

no." 2,4
2 4

of maturity

specimens X t
4 4

S.E.

Range

Phyllostomus

discolor

Adult Adult

?
Q

Lactating

13.0c 14.3c 15.6

t4.8,16.4

4 Glossophaga
2 2

Gravid, lactating

t5.0

Aduit
Gravid Gravid

soricina

I
Q

Lonchophylla
robusta Carollia perspicillata

2
2

Adult
Gravid

4 2 2
8 8

I
? 2 3 e

10.4 9.6

9.3-11.s

Lactating

Sturnira lilium Brachphyllo


cavernatum Uroderma

Adult Adult Adult


Gravid

d
e

18.3

t7.6
15.5

8 2 2
2 2

I
d
? ?

4
3
1 1
1

18.2,18.4 16.8-18.6 15.3-15.7

Adult

bilobatum

Lactating

Young adult Juvenile Q

Artibeus
jamaicensis (Colombia)

2,4
2

Adult Adult

6.0c

2 2
9

I Gravid I
Lactating
? d

2
5

I
9
1

Artibeus
iamaicensis (St. Croix)

Aduit Adult
Gravid

15.7

0.5

12.8-17.5 13.8,16.1

9 9
9

Young adult

t7.5
15.0
14.8

I
Q

2
1

Artibeus lituratus

2,3,4
2

Adult Adult

d
d

l4
t1
11 J
1 1

13.8

0.9

8.4,I',7.4

Young adult

13.4c

2,3,4
3 2

74.2 x
13.8

l.I

10.2-t6.9
12.6-1s.0

Stenoderma rufum Erophylla bombiirons Myotis nigricans Eptesicus brasiliensis Molossops

6 5
1

Gravid ? Juvenile g Gravid I Gravid Q

20.0
18.9

r7.3,19.9

Adult

1 1

2
2 7

Gravid ?

Adult Adult

temminckii
Molossus molossus

19.2

4.

BLOOD PHYSIOLOGY 495

TABLE IV. (continued) Neutrophiis

Lymphocytes

Eosinophils

Basophils

.F

t S.E.

Range

t S.E.

Range

t S.E. Range X b S.E.

Range

9.5 20.s 13.0 44.0


r
76.0 32.0

46.8 45.0

i 9.5

25-65
22-63

50.5

t9-22
8-84

72.s 79.0 54.7


24.0 63.0

r 10.2 49.0+9.1

33-74
72 '72, 13

34

3.0t1.3 0 6

1.3 1

0.5

0-2

1.5

0.5t
1.0

0.5

0-2

1,2

5.0

2.0
0 0 0 0 0 0 0

16-88

0
0

2.0

61.3
34.0

s0-70

38.7
63.0 s 9.0 6s.0

30 50

2.0
0 1.0 2.0 2.0

40.0

70.5 60.0 56.8 t 2.8 42.3


32.0 24.o 38,0

28.0

0, 7I s5--65
7

5144
34-50

24.0 34.7 38.5 L2.4 sl.1 45.'7 56.0 49.4 t8.B


36,0 32.1 x 22.0
37

24,24
32-37

t,3

32-42
44,61

3.0
1.0

1.1

t_6

1-3

0.5 0.3
0 0

0, 1 0-1

02

53.3 43-68 34.0 24,44 49.2 x 8.6 22-72 60.0 62.4 x 1.7 55-70 70.0 s4.5 50,59
60.0

6s.0 69.0 60.0

3.0
2.0 1.0

29-s'1

36,76 26-78

I.'7

22
33,

39

.0

4t

45.9 40.5

5.4 36.7 ! 6.0 33.0


r

t 5.1

20-8'7

20-70 14-68 20-44

4.8 5.5 60.2 x 6.1 61.3


56.9

35.0 49.9 +

12-78
28-76

29-84

49

74

0.2 0-1 2.4 x 0.5 1-5 4.0 4.5 4,5 5.0 1.1 1 0.4 0-4 0"9 r 0.4 0-4 1.5 t 0.6 V7 2.7 0-7
0.2
0

0 0 0 0 0
0 0

0.4

0.4 0.'7 x 0.4


r
1.0
0

0--2

0-3

0.2 x 0.2 t 0.4 x


0

65.0
5',7.0

2.0
1.0 1.0
0 0

0.2 0.2 0.2

W2
O-2

0-2

04

59.0
28.0 62.0

29.0 39.0

ss, 63

32.5
60.0 34.0 40.0 37.0

1.0 2.0

29, 36

2.5
0

t,4

1.0

47.0
62.0

5.0
0

(continued\

TABLE IY. (continued)


Monocytes

Locality
Species
no.
h "

Sex and state

No.

of maturity

specimens
4 4

-?

S.E.

Range

Phyllostomus

2,4
2

discolor

Adult Adult

d
e
Q

0.8
4.5 1,0
1.3 0

2.5t

0.5 1.0

0-2 0-4
3,6

Lactating

4 Glossophaga
2 2 2 2

Gravid, lactating

Adult
Gravid Gravid

d
?
Q

J
1

0-4

soricina

Lonchophylla
robusta Carollia perspicillata

3.0
0

Adult
Gravid

3
1

4 2
2 8 8 8

I
?

2.0
1.0

Lactating

1 1

Sturnira lilium Brachphylla


cayernarum Uroderma

Aduit Adult Adult


Gravid

I
d

2 3

I
? d ?
Q

4
3

2
2 2 2

Adult

3.5 2.3 1.8 t0.5 2.7


0

6.0

3,4

2,s
1-3 0-5

bilobatum

Lactating

Young adult Juvenile ?

5.0
1,0
2 5

Artibeus
jamaicensis (Colombia)

2,4
2 2
2

Adult Adult
Gravid

1.0
0

0-3
0*2

I
? ? d d

0.8

t 0.5

Lactating

I
9
1

Artibeus
jamaicensis (St. Croix)

9 9 9
9

Adult Adult
Gravid

Young adult

4.0 2"3 x 4.0

0.7 0.8

0-6

I I
d d

2
1

ln
0

Artibeus lituratus

2,3,4
2

Adult Adult

t4
11 11 3

Young adult

2,3,4
3

3.0 1.5 1.3 5.0

Stenoderma rufum Erophylla bombiirons Myotis ntgricans Eptesicus brasiliensis Molossops

6 5

Gravid I Juvenile ? Gravid Q Gravid I

1.3 5.0
12.0 2.0 8.0
1.0 1.0

t 1.3 0-4 t 0.5 04


0-2

0-I2

I
1

4,

Adult
Gravid

d
Q

1 1

2 2 7

Adult Adult

d e

temminckii
Molossus molossus
1

aValdivieso and Tamsitt, 1971. (Reproduced by permission of the National Research Council of Canada ftom The Canadian Journal of Zoology, Volume 49, 197I, pp. 31,36.) Dlocalities: Colombia; 1, Bogota; 2, Melgar; 3, Pacho; 4, Villeta, Puerto Rico; 5, Corozal; 6, Luquillo National Forest, St. Croix; 7, Fredericksted; 8, Ham's Bluff;9, Mount
Stewart Estate. cOne specimen.

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498 MARVIN L. RIEDESEL

TABLE

VI.

ERYTHROCYTE DIAMETERS (PM) IN BATS FROM PUERTO RICO AND ST. CROIX4 Erythrocyte diameter

Species
B ra chy p hy

Locality Sex and state no.D of maturity


8 8

No.
sPecimens
9 8

f t
5.5
5.5 5.6

S.E"

Range

lla

cav e rnarum

Adult d and
Gravid e

Artibeus iamaicensis

9
9
9

Adult d and

t6
1 1 1

Stenoderma rufum

6
5 7

Erophylla bombifrons
Molossus molossus

Gravid I Young adult d Gravid 9 Gravid 9 Adult d and I

2 2

t 0.04 4.1-7 .7 j 0.06 4.1-7.6 t 0.73 4.1-'7.'7 5.5 r 0.13 4.5-6.8 5.6 t 0.17 4.1-'7 .2 5.4 t 0.11 4.5-6.8 5.7 r 0.05 4.I-'7 .7 s.B r 0.09 4.5-8.1

avaldivieso and Tamsitt, 1971. (Reproduced by permission of the Nationai Research Council of Canada from the Canadian Journal of Zoology, Volume 49,19'7I. pp. 31-36.) blocalities as given in Tabie IV.

result of low temperatures on plasma, a heterogeneous fluid (water, inorganic elements, lipids, proteins, and formed elements). The clotting time increased by as much as 2S-fold during extended hibernation of M. lucifugus (Smilh et al., 1954). The specific cause or causes of the changes in viscosity and clotting time have not been identified. The spleen and the endothelial reticulirr system of the bat represent interesting tissues. Kallen, in Chapter 3, reviews work already conducted and in progess regarding these tissues. Such studies have very important implications for the physiology of the bat circulatory system. Changes in spleen size, as much as fivefold, are considered important during arousal from hibernation (Lidicker and Davis, 1955), and may be significant during flight. Flight, like arousal from hibernation, demands a large expenditure of energy and a large gaseous exchange. The metabolic cost of flight for bats is greater than the cost for birds, where it is relatively small. Increases in the volume of circulating blood which result from splenic constriction must be a critical process in meeting increased demands on the circulatory system. Responses of the spleen and other structures to flight need to be better defined, and most certainly offer an interesting challenge for future study. The extent to which dehydration and starvation change bat blood values should be systematically described. A4O% weight loss from food or food plus water deprivation in mice with a mean control weight of 33 gm has been reported (Archambeau et al., 1968) to result in (1) an absolute decrease in the total circulating lymphocyte and platelet counts while the total granulocyte count remained unchanged or increased, (2) a blood volume decrease while the

4.

BLOOD PHYSIOLOGY 499

hematocrit and specific gravity of the blood increased, and (3) a mean survival time of five days. .A. similar study of bats would be helpful in comparing data in which the time interval between capture and blood collection vary. Too often in the past, authors have failed to provide or recognize the importance of data regarding the nutritional state of animals. Very often body-weight data can help to assess the nutritional state of bats. Definition of the nutritional state does assist in the interpretation of the hematological data, for instance, if the animals have been dehydrated over a period of several hours in transit from collection site to laboratory, passive increases in the concentration of plasma may result. Simpiy weighing animals prior to and after making water available helps to define the extent of dehydration. Clotting is one of the physicochemical processes markedly changed during hibernation. Although prolonged clotting time during hibernation has been recognized for many years, the specific physicochemical changes resuiting in increased viscosity and clotting time have not been defined. The prehibernation clotting time of 7.4 minutes was increased to as much as 210 minutes during hibernation of Myotis lucifugus (Smith et a|.,1954). The effect of low temperature on the clotting mechanism appears to account for most of the increase in the clotting time during hibernation. Unidentified chemical factors may also be involved in the long clotting time during hibernation because 2 to 3 days after removal of bats from a 5o C environment the clotting time was 19 Io 26 minutes, a clotting time 2- to 3-fo1d longer than the prehibernation value of 7.4

Po

lter

of Hemotologicol
Response

ofl

Onsetl

tt.

to Stress

siress

\--'z\a \-/

./

at'

,,'

.'

Fig. 2. Temporal sequence ofhematological responses to stress in cold and isolated ltttle brown bats. (A) Alarm reaction (few hours to few days). (B) Recovery phase (few days to weeks or months). Straight line, cold and isolation stress; severe redction involving elements of white and red series. Small dashed line, cold stress; moderate reaction involving predominantly white cells. Large dashed line, isolation stress; mild reaction involving predominantly red cells. *, includes wbc count, rbc count, hematocrit, and ftlymphocytes.

500

MARVTN L. RTEDESEL

minutes. Krutasch and Hughes (1959) did not tabulate clotting times but concluded that the prolonged clotting time during hibernation is a result of the platelets being concentrated in the spleen.

III.

Blood pH and Gases

The limitations of small body size, the demands of flight, high respiratory water loss, and high ammonia concentration in habitats make information regarding the blood pH and respiratory gases in bat blood of particular interest.
The blood buffering systems of bats are unique.

Some bats at least are not disturbed by ammonia until the concentration exceeds 3000 ppm (Mitchell, 1963,b), whereas human subjects experience serious difficulty with a concentration of 300 ppm. A large flow of mucus (Studier, 1966) and the retention of carbon dioxide in the blood (Studier and Fresquez, 1969) have been described to be responsible for the constant pH of the blood and the high tolerance of bats (Myotis lucifugus, Eptesicus fuscus, and Tadaida brasiliensis) for ammonia. It may be pertinent to note that a high blood carbonic anhydrase concentration has been reported for Pipistrellus subflavus and Myotis lucifugus (Larimer and Schmidt-Nielsen, 1960). In contrast to the high tolerance to ammonia, carbon dioxide concentration appears to have a strong influence on the respiratory system of bats. Exposure of bats to 5%carbon dioxide resulted in a 200% increase in respiration rate although there was no increase at 2% concentrations (Mitchell, 1963b). The oxygen-carrying capacity of bat blood is well within the range of most mammals (Burke, 1953). Future application of microtechniques for blood and respiratory gas analysis should provide interesting information regarding blood gas values in
bats.

lV.

Water and Electrolytes

Their small body size and the wide range of thermal environments to which bats are exposed make water balance and electrolyte metabolism an interesting biological problem. Hemoconcentration can be expected to be one of the first effects of negative water balance. The standard deviation and standard errors of mean hematocrit, erythrocyte, and white blood cell data given in Tables II-VI are similar to data on other small mammals (Baker and Kline, 1932). The data in Table VII present most of the literature and support the hypothesis that, namely, as a result of behavioral, physiological, chemical and physical factors, bats maintain a near-constant chemical microenvironment for tissues.

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503

5O4

MARVTN L. RTEDESEL

Most of the sodium and potassium values presented in Table VII are consistent from laboratory to laboratory and bat to bat. This uniformlty of values is particularly impressive in view of the water balance hazards encountered by bats to be discussed later in this section. The range of calcium and phosphate data reported by Bruce and Wiebers (1970) is explained by the authors as resulting

from mobilization of salts during periods of activity. The increase in serum magnesium during hibernation is one of the most consistent changes in electrolyte metabolism (Riedesel, 1957). Ratlis (1964) describes sodium, potassium, calcium, and magnesium metabo-

lism during natural hibernation in mammals. Although the hypotheses

he

presents are based on limited data, he points out that a wide variety of systems may be involved, for instance, the sympathetic nervous system, zona glomerulosa of the adrenal giand, aldosterone, and antidiuretic hormone. Raths notes that the mineral metabolism of bats differs from that in other hibernators. These

differences need to be related to body size, diet, and behavior. A perfusion solution for tissue of Rousettus aegyptiacus has been described (Pefistiany et al., te69). There is a tremendous scarcity of data on water and electrolyte values for bat blood. Future studies need to consider that water balance is accomplished in bats by integration of numerous mechanisms, for example: (1) behavior, such as

flight to water sources and avoidance of desiccating environments; (2) presence or absence of thermoregulation, such that by lowering body temperature in a cool environment, water ioss may be reduced 100% or more whereas by permitting body temperature to rise in a hot environment, thermoregulatory
evaporative water loss (EWL) can be reduced; and (3)anatomy and physiology of the kidney, which may result in water conservation, as in the vampire bat Desmodus rotundus (McFarland and Wimsatt, 1969), or salt conservation. Most of the studies on water balance involve thermoregulation problems. With limited reserves extreme heat and cold must be encountered and drinking water may be available only at limited times during a 24-hour period. To recognize the types of stresses to which bats are exposed, consider the little brown bat, Myotis lucifugus, weighing 5 to 7 gm and spending 14 to 16 hours in a barn loft where temperatures may reach 50oC during the hottest part of the day. With a blood volume of 1 to 1.5 ml (Kallen, 1964), these animals cannot afford more than a 0.5 to 1 m1 water loss between drinks. Bats infrequently leave roosts during daylight hours to seek drinking water; however, they do move to attic areas where wal1 temperatures are 40"C or below (Carpenter, 1969; Studier et al., 1970). Evaporation of 1 ml of water at a temperature of 40"C would result in a 574 g-cal cooling. The metabolic rate of bats at this temperature is apt to be 1.55 mi oxygen hour 1gm-r or 7.4 g-cal hourlgm-l (Riedesel and Williams, 1976). Thus a 10-gm bat could maintain heat loss by

4.

BLOOD PHYSIOLOGY 505

evaporation equivalent to metabolic heat by evaporating 1 gm of water over an S-hour period. High evaporation efficiency has been caiculated for Myotis yumanensis, Tadardia bresiliensis, and Antrozous pallidus by Licht and Leitner (1967) and for Natalus stramineus, Glossaphaga soricina, and Myotis nigricans by Studler (1970). Occupancy of attic habitats requires close integration of physical and chemical factors, physiological capacity, and behavior. Behavior patterns may be a key factor for the little brown bat in attics. There is no doubt that water loss by bats can be considerable in a number of environments. Herreid and Schmidt-Nielsen (1966) point out that hibernation may very well be a water-conserving as well as an energy-conserving mechanism for bats. These authors reported that torpid bats, Eptesicus fuscus arrd Tadsrida brasiliensis mexicana, lost one-half to one-third as much water by evaporation as active bats at a given temperature. At the same time oxygen consumption is reduced by a factor of 10. These data indicate an increase in the volume of urine formed per milliliter of oxygen utilized by the bat when body temperature is decreased. This would result in increased body water during hibernation. We are left with an unsolved problem because dehydration has been described as a characteristic of hibernation (Riedesel et al., 1964; Fisher and Manery, 1967). This problem may be resolved by additional study of renal function during hibernation (Hong, 1957; Kallen,1964). The extent to which dehydration or overhydration is a factor limiting the length of hibernation by bats has not been determined. However, successful hibernacula in the field and laboratory are invariably described as humid. In addition, movements of bats during the hibernation period have been associated with the need for drinking water (Folk, 1940). These and other related problems have been discussed by Davis (1970) and Rosenbaum (1070). On the hot end of the temperature scale there are numerous unanswered questions regarding the cooling efficiency of the water evaporated from the respiratory tract, wing membranes and fur tips. At present we can most likely accept the fact that bats can withstand considerable dehydration and that dehydration undoubtedly occurs in natural habitats. When expressed as percentage of body weight, bats without food or water intake lose weight at a rapid rate. Data collected in my laboratory by G. L. Bintz and L. B. Bintz (Personal communication, 1975) (Fig. 3, Table VIII and IX) emphasize this point as do data reported by Studier et al. (1970). Several years ago Carpenter (1968) determined the water loss of fish-eating bats to be 7 .9 mg gm-l hour-l . The l0% weight loss per 12 hour appears to describe the situation for at least two species, the little brown and the pallid bat. These data can be predicted on a somewhat theoretical basis from consideration of the caloric and oxygen requirements, caloric values of body tissues, and water content ofbody tissues (see following tabulation). Over a 12-hour period, assume the 1O-gmbat

506

MARVTN L. RTEDESEL

Caloric requirements

O, gm-t hour-t (Henshaw, 1968) oxygen results in 5 kcal of energy 10-gm bat requires 350 cal hour-l = 4200 cal per 12 hour Caioric and water content of tissue l-gm body carbohydrate or protein contains 4.5 kcal l-gm body fat contains 9.5 kcal 5gm liver or muscle tissue contains 4-gm water per l-gm nutrient (glycogen or protein) 5-gm body fat tissue contains l-gm water and 4-gm nutrient
10-gm bat utilizes 7 ml

I liter

obtained 4200 cal by utilizing 0.1-gn carbohydrate, 0.4-gm fat and 0.02-gm protein. If the respiratory water loss is equal to metabolic water from catabolism of nutrients, then the computations presented above and in Table VIII account for the l-gm weight loss by a 10-gm bat over the l2-hour period. Thus, just considering the caloric requirement and body tissue components of the animals, we can predict the weight loss of the animals. It may be pertinent to note that urination and defecation can result in rapid weight loss (greater lhanl0%per 12 hours) during the first few hours of a food- and water-depdvation period. The really challenging question which remains is how bats in a wide variety of habitats manage to limit the body tissue and water loss to the l0% per 12 hours.

H H J c .9
o

o/o Weighi Loss

Temperoture (oC)
Woter Vopor Pressure (mm Hg)

s c
o o
Sbler (nm Hs)

o -

30;
20
t0

(J o
l

-t8

o
3.
E

-t6

to

20

3Ol 40
N.M
r

50

60

70

80

Animols in Roswell, Animols in Lob

l'-

Hours

Fig. 3. Weight loss and ambient data following capture of pallid bats, n=13 (G. L. Bintz and L. B. Bintz, personal communication, 1975).

4.

BLOOD PHYSIOLOGY 507

TABLE

VIII. CALCULATED CALORIES AND FREE WATER AVAILABLE FROM ANIMAL TISSUE CATABOLISM
Caloric

Weight loss due to

nutrient catabolism (gm)


0.10 glycogen 0.41 fat 0.02 protein
0.5 3

ol nutrient
400
3690
80 41'70

value (cal)

Weight loss due to free water in tissue (gm) 0.40 0.08 0.08
0.5 6

TABLE

IX.

PER CENT WATER CONTENT OF BAT TISSUE4


Bats

without

food and water Io 30% weight Controls


liver Tadarida brasiliensis
n
SE

loss

P Value

liver

81.02 88 1.78 '79.97


n
SE

69.49

74.85 22 0.06 74.61 56 1-29

64.60

0.01

0.02

1.r
6',7

1.19 67.28 0.01

Antrozous pallidus

.8'l

66

0.96

r.2r

0.24

4G.L.Bintz and L.B. Bintz, personal communication, 1975.

The evaporative water loss (EWL) for bats described by Carpenter (1969) and Studier et al. (1970) is very close to the 10% per 12 hours. The metabolic water available from catabolism of laI may be lost by the respiratory system because catabolism of fat requires a greater oxygen intake than does carbohydrate or protein. Multiple factors, including (1) type of food being metabolized; (2) air velocity and water vapor pressure; (3) bat surface area available for evaporation; (4) isolation or clustering of animals; and (5) other behavioral, physical and physiological factors, determine water loss by bats. However, there must be some compensating mechanisms which keep weight loss close Io l0% of body weight during the first 12 hours. Note in Fig.3 thatbatshada25% weightloss 80 hours after capture. The rate of weight loss had declined to nearly 5%per 12

508

MARVTN L. RTEDESEL

hours after 40 hours of capture and withdrawal of food and water. In contrast carpenter (1969) reported EWL in Leptonycteris sanborni as high as 3% of body weight per hour during flight of these inhabitants of desert areas. This high rate of water loss during flight is in keeping with the theory that insectiv<_rres may limit all of their flight and eating to two 30-minute periods per 24 hours. The extent of dehydration tolerated and the effects of dehydration differ among bats. The percentage of water content of free-tail bat liver tissue decreased following the 30% weight loss (Table IX). The pallid bat apparently has a mechanism which permits 30% weight loss without dehydration of liver tissue. carpenter (1969) noted that when comparing EWL, in the big brown and free-tailed bats, the free-tailed bats lost less water at higher ambient temperatures than did the big brown bat. He accounted for the difference by noting that the free-tailed bats had higher body temperatures; thus Eptesicus fuscus had, greater evaporative losses which kept body temperatures lower. It is of interest that several investigators have described a relationship between EWL of bats and body weight (Herreid and schmidt-Melsen, 1966;Licht

weight even though environmental conditions, water intake, and water reserves vary. Many of these physiological mechanisms have not been described to date but we do have clues. The large size of bat lung relative to body size suggests bats limit EWL by permitting large depths of ventilation and 1ow frequency of lung ventilation. Shallow breathing and panting increase EWL. In summary, the water baiance of bats must be taken into account when collecting and interpreting hematological and blood chemistry data. Thus it is important to recognize that (1) the amount of water available for evaporation may change by selective catabolism of fat tissue with low water content and catabolism of liver or muscle with high water content;(2) water reserves in bats may be kept nearly constant under adverse conditions by the water-conseruing activity of the kidneys; (3) variation in body temperature is undoubtedly an important asset in water conservation. currently, variation in body temperature, insensible water loss, and renal activity appeff to be important in maintaining body water balance in active bats in warm and dry environments. Reports of active bats living without drinking water emphasize the unique biological tool bats possess in the area of mammalian water-conserying systems (carpenter, 1969; vogel, 1969). yariation in body temperature. ranging from 37'c to near freezing. may be the major mechanism accounting for the tolerance for iimited water intake. If bodv

and r-eitner, 1967). Actually the EWL and body weight relationship is not strictly empirical because the variables listed above are also related to body weight. The important point of this discussion is that bats have physiological mechanisms and behavioral characteristics which keep EWL related to body

4.

BLOOD PHYSIOLOGY 509

temperature is very near the ambient temperature, then the vapor pressure gradient between the bat and environment can be relatively small. Thus lowering of body temperature to near ambient can make a major contribution toward conservation of body water. It should be noted that body temperatures near ambient are common in tropical bats as well as in those from temperate regions (McNab, 1969). Thus lowered body temperature can make a major contribution toward body water conservation in tropical as well as in temperate bats. Insensible water loss apparently is very high during flight, therefore behavioral adaptations which limit time and duration of flight are important. Most of the small bats need to restrict flight to brief periods when water and food supplies
are limited.

There is at least one bat which has been reported to live without drinking
water. Rhinopoma hardwickei d,oes not need free water because (1) their renalconcentrating capacity is high, (2) blood urea values are high, and (3) there is a

low insensible evaporative water loss from the skin (Vogel, 1969). As noted earlier, vampire bats also may not require drinking water (McFarland and
Wimsatt, 1969). The renal capacity to concentrate urine is not always dependent upon long loops of Henle (Horst, 1969). The vampire bat (Desmodus rotundus muinus) kidney has cells which can concentrate urine without the long loops of
Henle.

V.

Lipids, Carbohydrates, and Proteins The specialized diets and the process of hibernation have stimulated interest

in the blood

chemistry

of

bats. The periodicity

of

feeding and bursts of

metabolic activity of many bats result in ingestion, mobilization, and storage of relatively large amounts of energy within brief periods of time. The 24-hour oxygen consumption of Myotis velifer at temperatures of 5o, 10o, 20o,30o, and 35oC has recently been measured (Riedesel and Williams, 1976). The 10- to 13-gm animais were isolated and confined to cylindrical metabolic chambers with 6.5-cm diameters and heights of 9.5 cm. Under these laboratory conditions individual bats could maintain for 6 to 12 hours a resting metabolic rate which was from 40% to 400% above minimal oxygen consumption (Table X). In addition, the bats had periodic bursts in metabolic rate. Most of the bursts in metabolic rate occurred primarily at the time the lights were turned off. One bat at 5oC had a 228-fold inprease in metabolic rate. Hock (1951) had reported as much as a 130-fold increase in metabolic rate for small insectivorous bats. The large changes in metabolic rate suggest bats not only have a wide range in metabolic rates but the major metabolites and blood chemistry
are also subject to change.

510

MARVTN L. RIEDESEL

TABLE

X.

MEAN RESTING AND MINIMAL OXYGEN coNSUMPTION AND Q,o VALUES. MYOTIS VELIFERA'D

Tair

Resting
(ml gtl hour-1
1.5 5

cc)
35

Oxygen (Q,")
2.tt
2.86 1.40 0.00

(mi g-1 hour*l


1.35

Minimal )
0.65 0.19 0.16 0.07

Oxygen

(Q,")
2.08 3.89

30 20 10
5

1.00 0.35 0.25 0.25

t.02
2.29

dlRiedesel and Williams, 1976). bEight to twelve animals studied.

A. Lipids
Seasonal changes in whole body content have been described (Weber and Findley, 1970; Krulin and Sealander,1972).In these studies and references cited by the authors there is ample evidence of an annual cycle of body lipid content among Eptesicus fuscus, Myotis grisescens, M. lucifugus, M. thysanodes, M. nigricans, Tadarida brasiliensis, and Nycticeius humeralis. Many of these bats have low body lipid content in spring and early summer but have a 5- to 7-fold increase in body lipid in late summer. In the gray bat, Myotis grisescens, Iipids account for 56% of the weight in October. The rapid weight gains common in these bats suggest a great capacity for fat deposition and mobilization. K. N. Geluso (personal communication, 1975) has been making observations on young Tadardia brasiliensis, and noted that 10 animals with an average weight of 9.0 gm lost 1.6 gm during 6 to 11 days in captivity at 29"C with water but no food available. These bats were flown or disturbed for 10 to 30 minutes each day and

body fat was their only source of energy. Studies of blood lipids confirm
seasonal mobilization of lipids.

Highest serum lipid values of Myotis grisescens occurred in late summer and fall (September, October and November) with the lowest values in the spring (March, April and May) (Dodgen and Blood, 1956). On the basis of urine, blood, and RQ data, Dodgen and Biood (1956) concluded that a combination of lipids and protein represents the major energy source during hibernation. Breakdown of muscle tissue with a J 5% water content may very well be an important source of water during hibernation. Although iipids yield a lot of metabolic water (Brntz et a1.,1971), body lipid as a sole source ofenergy is apt to result in

4. BLOODPHYSIOLOGY

511

negative water balance because: (1) Fatty acid oxidation requires more oxygen per caloric yield than does monosaccharide or amino acid oxidation. High

oxygen intake increases respiratory EWL (Bintz, 1969;Bintz et al., 197 1'). (2) The amount of free water in fat tissue is small, 15% or less. The light weight and high caloric value of lipids represent a strong argument for fat as the major energy source during migration. The increases in plasma-free fatty acids coupled with the decrease in liver triglycerides and free fatty acids reported by Esher e/ al. (1973) support the hypothesis that iipids are an important source of energy during and shortly after arousal from hibernation. Serum values of total cholesterol and phospholipids have been reported to increase in concentration from frugivores and omnivores to the vampires, but was highest in an insectivore (A. A. Arata, A. Wahner, and K. Triparthy, personal communication, 1969). The values shown in Table XI were kindly supplied by Dr. Arata.

B. Carbohydrates
Blood glucose values in two specie s of X[yotis (M. grisescens and M. lucifugus) have been described to be related to body temperature and duration of hibernation (Dodgen and B1ood, 1956). The blood glucose of 16 hibernating bats ranged from 7 to 15 mg%, whereas most of the values for active animals were between 100 and 150 mg%,with some values as high as 200 mg%. The low total glycogen content, 0.lVo to 0.2% of body weight (Dodgen and B1ood, 1956), suggests that gluconeogenesis is an important process in bat physiology.

C. Prctteins

Studies of blood proteins have been oriented to examining hemoglobin as a tool in taxonomy, examining the immunological capacity of bats, or evaluating protein as an energy soufce. There is a great void of information regarding the gas-transporting capacity of bat hemoglobin and the roles of serum proteins in bat nutrition and osmotic activity of plasma protein. The oxygen equilibrium curves of hemoglobin ftom Eptesicus fuscus, Myotis keenii, M. lucifugus, and Pipistrellus subflavus have been described to be similar

(Manwell and Kerst, 1966). The Bohr effect and other physiological properties resemble other mammalian hemoglobins. The minor physiological differences
among the hemogiobins may be because the bats examined were limited to
insectivorous microchiroptera.

Electrophoretic examination of bat hemoglobins has at least a limited taxonomic value as molossid bats can be distinguished from other families (Valdi-

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BLOOD PHYSIOLOGY 513

vieso et al., 1969). The greatest value of these examinations may be in phylogenetic analysis (Foreman, 1964;Manwell and Kerst, 1966;Mitchell, 1966; Tamsitt and Valdivies o, 1 9 69). In contrast to most other vertebrate species bat heart and skeletal muscle have been described to have identical lactate dehydrogenase (LDH) moiecules (Manwell and Kerst, 1966). After examining blood proteins, LDH isozymes, and lipases of tissues, these investigators concluded that vespertilionine bats are in the beginning of a period of extensive speciation and that they have not had time to accumulate conspicuous genetic differences. Antibody production is a fascinating aspect of protein metabolism.Immunological response of bats maintained at24"C is equivalent to the response at 37"C (Hatten et al., 1968). This suggests that either bats are capable of synthesizing proteins when body temperature is near 24"C or protein synthesis isvery rapid during brief periods when body temperature is elevated in a 24"C ambient environment. The point that interests me is that the production of antibodies in bats is very rapid and that they are short lived (Jaeger, 1963). Jaeger also noted a rapid rate of gamma globulin disappearance during hibernation. The complement activity rn Eptesicus fuscus, Myotis lucifugus, Tadarida brasiliensis, and Pteropus vampyrus was compared to guinea pig, chicken, and rabbit compiement by Hatten et al. (1973). Whereas the amount of complement present in bat blood was within the range expected for various species, the bat complements were unique in their response to changes in temperature and pH. The authors suggest that a thorough examination of bat complement would provide fundamental knowledge in the kinetics of complement. The development and characteristics of complement among the various bat species was unique and represents a potentiai tool for bat taxonomists. Short-term antibody responses characteristic of bats may be due to low antigen doses because such responses have been described in response to low antigen doses in many animals (Allison, 1972). There are several points which suggest that protein catabolism is an important energy source for bats. The small size of many bats results in a high energy requirement per unit mass, and the capacity for storage of energy in forms of glycogen and fat is limited. The data presented in Fig. 1 along with Studier and co-workers' data (Studier et al., 1970) collected in field and laboratory conditions emphasize the need for bats to feed regularly. It is interesting to digress and speculate that birds combine flight, low body energy reserves, and hyperthermia whereas bats combine flight, low body fat and hypothermia. Hypo-

thermia occurs

in

animals

that are inactive during warm daylight;

and

hyperthermia in animals inactive during cool dark hours. Catabolism of protein as an energy source for bats would conserve the small fat stores and provide tissue water for thermoregulation and obligatory urine formation. The high tolerance of bats for ammonium ions and high blood urea

514

MARvIN L. RTEDESEL

in other hibernators (Kristoffersson, 1963) may eventually lead to additional evidence for the role of protein catabolism as an energy source for mammalian hibernators, including bats. Dodgen and Blood (1956) describe
values

protein as a major metabolite following arousal from hibernation. The vampire bat must represent the mammal with the diet richest in protein, 85.5%, combined with lowest fat, I/o, and carbohydrate, 1.7% content. Following feeding, the blood urea concentration can increase from27'to 57 millimoles per liter (McFarland and Wimsatt, 1969). In summary, the water- and electrolyte-conserving mechanisms of bats must operate precisely but under a w.ide variety of circumstances as the small body size represents limited water and electrolyte reserves. Furthermore, descriptions of conserving mechanisms operating at several levels of organization-social, behavioral, circulatory and renal systems, cellular, molecular, and physical-can be expected. There is a vast amount of information needed to determine what changes occur within the bat when a change is made in activity or in the environment.

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