Field water balance performance in prairie dogs (Cynomys leucurus and C. ludovicianus)

FIELD WATER BALANCE PERFORMANCE IN PRAIRIE DOGS (CYNOMYS LEUCURUS AND

c. LUDOvICIANUS)

EUGENE B. BAKKO Biology Department, St. Olaf College, Northfield, MN 55057, U.S.A.

(Receioed 30 April 1976)

Abstract-l. Field samples of urine, blood plasma, and kidneys were collected seasonally from white- tailed prairie dogs (Cpnomys leucurus) and black-tailed prairie dogs (C. ludouicianus).

2. Maximum field urine osmolalities for black-tailed prairie dogs were significantly below maximum urine osmolalities for that species under laboratory water deprivation. However, white-tailed prairie dogs produced field urine concentrations that did not differ from maximum urine osmolality collected under laboratory water deprivation except during June.

3. Black-tailed prairie dogs demonstrated greater urine concentrating ability than white-tailed prairie dogs as evidenced by kidney relative medullary thickness and by urine concentration under water deprivation. Survival time under water deprivation was higher for black-tailed prairie dogs. Potassium, sodium, urea, and ammonia concentration in urine are discussed. Blood plasma osmolality and plasma potassium, sodium, and urea concentrations are discussed.

4. It is argued that white-tailed prairie dogs, although living in a more xeric habitat than black-tailed prairie dogs, are not as well adapted to withstand water stress and probably rely on seasonal torpor. Black-tailed prairie dogs, while occupying a more mesic habitat, are better adapted to water stress and therefore are able to remain active throughout the year. This, in turn, enables continuous social contact in this species and subsequent high social organization,

INTRODL’CTION

Extensive laboratory work has been reported on water balance of wild mammals (summary in B. Sch- midt-Nielsen, 1964; K. Schmidt-Nielsen, 1964; Chew, 1965). However, few studies have been conducted to reflect water relations of wild mammals in the field under natural conditions (Mullen, 1971; MacMillen, 1972; Schmid, 1972; Baudinette, 1974; Bradford, 1974; Bakko. 1975). The purpose of this study has been to collect data from wild populations of black- tailed prairie dogs (Cynomys ludonicianus) and white- tailed prairie dogs (Cynomys leucurus) during different seasons of the year in an effort to learn how these animals react physiologically with respect to water balance. In addition, laboratory experiments under varying conditions were designed to gain further in- sight to the physiological limits of these animals.

Although both species of prairie dogs studied here occur in the grassland biome, white-tailed prairie dogs are more inter-montane in their distribution (Hall and Kelson, 1959). These inter-montane prairies are more subject to rain shadow effects from the Rocky Mountains and consequently receive less annual precipitation than do the more eastern grass- lands occupied by black-tailed prairie dogs. Gener- ally, the ability of members of a species to conserve water is inversely related to water availability in their natural habitat, Based on the habitat difference of these two species with respect to precipitation it might be predicted that white-tailed prairie dogs are physiologically better adapted to conserve water. However, one other factor complicates this situation. Several papers have reported that white-tailed prairie dogs probably hibernate because this species has not

been observed above ground in winter (Stockard, 1930; Tileston & Lechleitner, 1966; Bakko & Brown, 1967). It has also been generally concluded that black- tailed prairie dogs do not hibernate because this species has been observed above ground during all seasons (King, 1955; Koford, 1958; Smith, 1958). Because hypothermia may be an adaptation to stressful conditions imposed by lack of water (Fisher & Manery, 1967; Schmid, 1972), the question arises as to whether the white-tailed prairie dog is better adapted for water conservation because it inhabits a more arid environment than the black-tailed prairie dog, or, is the black-tailed prairie dog, in fact, better adapted for conserving water, even though it lives in a more mesic environment because it cannot escape environmental rigors by means of hibernation. The foregoing ques- tions provided a basis for studying these species.

MATERIALS AND METHODS

Prairie dogs were collected during June and July, 1969; March, June and August, 1970; September and November, 1971; and October of 1973. Collection of most black-tailed prairie dogs for field data occurred in Bowman County, ND. The October, 1973, sample for this species was collected in Wheatland County, MT. All white-tailed prairie dogs were collected in Albany County, WY. No white- tailed prairie dogs were collected during November. To avoid the possibility of eliciting behavioral and subsequent physiological responses that could be skewed by handling live animals (Bakko, 1976). prairie dogs collected for field data were shot with a .22 caliber rifle rather than collected by live trapping. Most animals collected in the above man- ner were killed instantly.

Urine samples were taken by bladder puncture with a syringe. Blood was collected by heart puncture with a lightly heparinized syringe. Blood was centrifuged immedi-

(‘.il.P. 56.3A M 443

444 EUC;t,NE B. BAKKO

ately with a specially machined centrifuge head mounted on a car heater fan motor using a 12-V car battery as a power source. Plasma was decanted and preserved in air tight polyethylene centrifuge tubes (0.4ml, A. H. Thomas Co.. Philadelphia, PA) as were urine samples. These samples were placed immediately on ice until they could bc frozen (within 7-3 hr) for later laboratory analy- ses.

Body weight was measured to the nearest 0.1 g. Kidneys were excised and preserved in AFA (IO”;, formaldehyde. IO’!,, glacial acetic acid, 30”;, alcohol, 50”; distilled water) for later examination.

All animals live trapped for experimental laboratory study were collected with open wire traps manufactured by the National Live-trap Company. Prairie dogs were housed in 2.4 x 2.4m floor cages with Purina Rat Chow, sunflower seed. and water available itd lihitlctn. Stainless Steel cages (30 x 25 x 16.5 cm. Acme Research Products. Cincinnati) were used to obtain daily quantitative measurc- ments of food and water consumption and of urine and feces production. Body weight was measured daily. The cages provided for separation of urine and feces. Urine was collected under mineral oil to prevent evaporation. Spillage of drinking water by the animals was collected separately under oil and not allowed to cont~millate urine samples. Pulverized, air-dried Purina Rat Chow was the food source in experiments. Urine samples to be analyzed for constituents were collected just after urination and then frozen in air tight (polyethylene) vials for later determina- tions. All metabolic cage experiments were conducted at 20 2°C (30-70 r.h.). Two experimental procedures were conducted on laboratory animals in metabolic cages: (1) with food and water citi ~j~?jf1{/~7, (2) with food cjri ~jbj~~~~~~ only.

Urine (I:9 dilution) and blood plasma (undiluted) were analyzed for total osmoconcentration by the freezing-point depression method on an Osmette osmometer (Model 2007, Precision Systems, Sudbury, MA). Urea and ammonia concentrations were determined by the Conway boric acid_HCl microdiffusion technique as modified by Obrink (1955). Sodium and potassium levels of urine and blood plasma were measured on a flame photometer (Model 143, Instrumentation Laboratory. Inc.).

Relative medullary thickness (RMT) of kidneys was determined according to Sperber (1944) by the following formula: RMT = IO(r)(T x H x L)m0-“2. This required measurements of I. gross dimensions of the kidney, thickness (T). height (H), and length (L); and 2. the radial exten- sion (r) of the medulla. The medulla radius was exposed by making a mid-sagittal cut through the kidney with a razor blade such that the maximum area of the medulla from the cortical-medullary boundary to the tip of the renal papilla was visible. Several measurements from the renal papilla tip to various locations on the cortical- medullary boundary were averaged to obtain the r value in Sperber’s formula. Meastirements were made to the nearest 0.1 mm with dial calipers. Representative kidneys of each species were prepared histologically and examined microscopically to verify the cortical-medullary boundary. Relative medullary thickness was averaged for each pair of kidneys to obtain one value for each animal.

Statistical procedures involved the use of Student’s f test to evaluate differences between means. Al1 differcnccs discussed in this paper were si~ni~~nt at the P i 0.05 level unless stated otherwise. Confidence intervals for each mean were calculated as x + I 0.07 ,S.E. Variances of compared means were tested for similarity by an F-test at P I 0.025. If variances were different. a weighted r value was com- puted by the method of Cochran & Cox (1964) to conduct the test.

L’YiW REX’LTS

The environment around Laramie. WY, where all

white-tailed prairie dogs were collected. is more arid than that around Bowman. ND. where most black- tailed prairie dogs were collected (Table I). The big- gest difference in precipitation between the two areas occurs in May and June, when Bowman receives an average of 6.7 cm more rainfall than Laramie for the two month period. During other seasons, precipitation differences between the two arcas is not nearly as ~ippreci~~ble altho.ugh Bowman usually receives slightly more. A ~~reclpltation pattern similar to that of Bowman. ND also occurs in Wheatland County. MT, where the October. 1972, collection of black- tailed prairie dogs was made (U.S. Dept. of Comm., Env. Sci. Serv. Admin., Montana Climatological Data, vol. 76. no. 13). Precipitation at Harlowton. MT (Wheatland Co.) was slightly above normal for 7 months prior to and dur?! the October. 1973. collection for black-tailed prame dogs.

Seasonal trends in urine osmolality demonstrated that urine was least concentrated in June for white- tailed prairie dogs and in July for black-tailed prairie dogs (Fig. 1). However, the June sample for whitc- tailed prairie dogs was signjfi~dntl~ lower than the August and September samples only for that species. The July sample for black-tailed prairie dogs was significantly lower than all other months except November for that spccics. Urine osmolality in black- tailed prairie dogs was significantly lower than for white-tailed prairie dogs only during Juiy and October. Both species showed an increase in urine: osmolality in Aqgust and September. This increase was most dramatic for black-tailed prairie dogs. L!rine osmolalitj dccreascd during October and November for both species. however the drop was significant from September only in black-tailed prairie dogs. Urine osmolality of black-tailed prairie dogs under laboratory d~hydratioll stress was greater than any of the field collections. However. only the JLIX

urine sample from white-tailed prairie dogs was lower than the urine collected from that species under dehydration stress.

Seasonal trends in urine potassium concentration for white-tailed prairie dogs coincided closely to the pattern of total urine concentration (Fig. 2). However, the differences between samples were more pronounced. For instance. June urine potassium was significantly lower than any other period of collection. August and September potassium concentrations were significantly above any other sample for white- tailed prairie dogs. Urine potassium ct~ncentr~~tions in black-trailed prairie do_gs also correlated closely with total urine concentration trends for that species except during March. Potassium concentration for that month was not different from the June or JLII~ potassium concentrations for black-tailed prairie dogs. July urine potassium was significantly lower than for June in black-tailed prairie dogs. Urine potassium concentration from dehydrated animals was as low or lower than most field samples. There was no difference in urine potassium between hydrated and dehydrated black-tailed prairie dogs while dehydrated white-tailed prairie dogs had lower urine potassium than hydrated animals.

Urine urea ~oxi~~lltr~~ti~~n in black-tailed prairie dogs corrcfated with total urine co~~~entrati~~~ for March. June. and July but remained relatively low

Field water baiance performance in prairie dogs

Tabie 1. Annual and monthly precipitation (cm) for Bowman. ND, and Laramie, WY, for the period 1931-1952 and for the years 1969, 1970, and 1971. Data for

1973 is listed for Laramie. WY. only

Bowman, ND Laramie. WY 1931- 1931-

Month 1952” 1969b 1970h 1971b 1952” 1 969h 1970h 197lb 1973b

J I.2 1.2 0.6 1.6 1.0 I.1 0.2 0.8 1.1 F 0.9 0.6 0.2 0.6 0.9 2.9 0.5 3.5 0.4 M 2.1 0.7 0.4 0.9 1.9 0.5 3.6 2.2 3.8 A 3.6 3.5 4.7 5.8 3.8 1.7 0.8 2.4 5.7 M 5.6 3.3 12.4 3.8 3.8 1.8 0.7 5.3 2.1 J 8.6 15.2 9.x 14.0 3.7 7.7 5.0 0.7 5.8 J 4.9 11.0 1.9 1.3 4.3 1.9 1.3 2.3 4.9 A 4.3 1.1 7.6 0.4 3.0 1.1 1.4 5.2 2.0 S 3.0 0.6 3.4 1.6 2.1 3.2 3.9 2.7 5.6 0 2.4 1.5 1.6 6.5 1.x 5.2 3.x 0.2 0.2 N 1.0 0.1 3.2 0.9 1.1 1.1 2.8 0.7 3.2 D 0.8 1.5 1.0 0.4 1.1 0.4 0.7 0.2 2.0

Total 38.6 40.9 49.3 43.6 28.6 28.5 24.8 25.9 36.7

’ U.S. Dept. of Comm. Weather Bureau. Climatic summary of the U.S.. 1931. 1952, for North Dakota and Wyoming.

b U.S. Dept. of Comm. Environmental Science Services Administration. North Dak- ota and Wyoming Climatological Data, Vols. 78-80: no. 13.

445

from August through November when urine concentration increased sharply (Fig. 3). During March, June, and July, urea averaged 57.9’>; of total urine concentration compared to 34.17; during August through November in black-tailed prairie dogs. Urea concentration in white-tailed prairie dogs followed similar trend but not as pronounced. The average urea concentration in this species up through July was 45.2’:; of total urine concentration compared to 32.3”:: during August through October. Urine urea from dehydrated black-tailed prairie dogs was significantly greater in concentration than any field sample. Urea concentration from dehydrated white-tailed prairie dogs was not greater than the March sample but greater than the other field samples for that species.

IBlack-toiled proire dogs 0 White-toiled prawe dogs

Fig. 1. Field and laboratory urine osmolalities for black- tailed and white-tailed prairie dogs. Vertical lines represent ranges; horizontal lines represent means (X); rectangles enclose the x k t 0.97$.E. Numbers in parentheses represent the number of animals. For laboratory data. the left sample for each species represents dehydrated animals and the right sample represents hydrated animals. Numbers outside parentheses represent the number of

2. Field urine potassium concentrations of b~dck-tailed and white-tailed prairie dogs compared to laboratory urine potassium and to field urine osmolalities._Open circles connected by a dotted line represent mean (X) urine osmalahty for white-tailed prairie dogs_Closcd circles connected by a solid line represent mean (X) urine osmolality for black- tailed prairie dogs. Vertical lines represent ranges; horizontal lines represent means (X); rectangles enclose the xit 0,‘,75S.E. Numbers in parentheses represent the number of animals. For laboratory data, the left sample for each species represents dehydrated animals and the right sample represents hydrated animals. Numbers outside parentheses represent the number of measurements

measurements from the animals involved. from the animals involved.

Ammonia concentration in urine from field samples (Fig. 4) was similar for both species. but differed in seasonal trend from urine osmolality (Fig. 1). There was a sharp drop in urine ammonia during August through November for both species (Fig, 4) with the exception of the October black-tailed prairie dog sample which had greater variation. Urine ammonia relative to total urine concentration dropped by ap- proximately a factor of four in each species when comparing the periods March through July with

446 EUGENE B. BAKKO

2500 l I Ela,ck-toiled pmirie dogs * D White-talled prairie dogs

I,, ,,,. ,I M A M : J A S 0 N 1 Lob

months

Fig. 3. Field urine urea concentrations of black-tailed and white-tailed prairie dogs compared to laboratory urine urea and to field urine osmolalities. Open circles connected by a dotted line represent mean (x) urine osmolality for white-tailed prairie dogs. C_losed circles connected by a solid line represent mean (X) urine osmolality for black- tailed prairie dogs. Verticallines represent ranges; horizontal l&es represent means (X); rectangles enclose the interval X f r,,,,$.E. Numbers in parentheses represent the number of animals. For laboratory data. the left sample for each species represents dehydrated animals and the right sample represents hydrated animals. Numbers outside parentheses represent the number of measurements

from the animals involved.

August through November. It decreased from 3.25% to 0.81% in black-tailed prairie dogs and from 1.22% to 0.34u/, in white-tailed prairie dogs for those respective periods. Urine ammonia from dehydrated black- tailed prairie dogs was not greater than several of the field samples but white-tailed prairie dog urine ammonia from dehydrated animals was significantly‘ greater than any field sample.

There were no intraspecific differences in urine sodium concentration between months for either species (Table 2). However, there were five unusually high values for balck-tailed prairie dogs during Sep- tember which distorts the overall mean if added to it. Aside from the September data for black-tailed prairie dogs, urine sodium was significantly greater in white-tailed prairie dogs collected in the field

throughout the year. Urine sodium from hydrated laboratory animals of both species was much higher than from field samples. This was undoubtedly due to the high NaCl content of the Purina Chow sup- plied to lab animals.

Plasma

Although the mean plasma osmolality in field collected black-tailed prairie dogs was higher than for white-tailed prairie dogs, this difference was not significant (Table 3). There was also no difference between the two species when comparing plasma potassium. However, sodium concentration in plasma of white- tailed prairie dogs was lower than in black-tailed

4 Black-toiled prairie dogs Cl White-toiled prlwie dogs

MAMJJASCN months

Fig. 4. Field and laboratory urine ammonia concentrations of black-tailed and white-tailed prairie dogs. Verti- cal lines represent ranges; horizontal lines represent means (x); rectangles enclose the interval X & to,975S.E. Numbers in parentheses represent the number of animals. For laboratory data, the left sample for each species represents dehydrated animals and the right sample represents hydrated animals. Numbers outside parentheses represent the

number of measurements from the animals involved.

Table 2. Field and laboratory urine sodium concentrations (m-equiv/L) from black-tailed and white-tailed prairie dogs. Numbers in parentheses represent number of animals from which samples were taken in the laboratory

Period Black-tailed prairie dogs White-tailed prairie dogs

x + t” 975SE N range X + r,,q,,S.E. N range

March June July August September October November Field

(Overall) Lab w/H,0 Lab wio H20

7.8 + 5.5 8.7 * 5.7 4.5 f 1.0 8.3 * 4.1

84.8 & 82.3 8.6 k 4.4 8.8 + 4.8

8.0” f 1.6

161.0 f 29.4 169.2 i 24.8

8 4.2-24.0 ii 3.8-33.4 8 36-7.5 7 4.0-17.0

13 5.0-478.0 14 2.0-22.1 12 2.3-26.0 68 2.0-33.4

30(4) 30.1-284.0 8615) 7.3-485.0

14.6 k 8.9 12.1 f 3.4 9.5 i: 4.0

17.7 j, 8.0 18.9 * 14.0 7.7 rt 3.8

13.2 f 2.7

147.3 i: 24.4 70.3 i: 70.4

12 6.0-58.0 12 6.3-26.4 12 s.c-26.1 10 7.2-38.3 8 648.2 9 3.2-20.0

63

57(4) 57(5)

3.2-5X.0

I l&364.0 I 12335.0

* Overall field value, exclusive of five unusually high September values.

Field water balance performance in prairie dogs 447

Table 3. Field and laboratory plasma concentrations in black-tailed and white-tailed prairie dogs (x + c,,,~,~S.E.). Numbers in parentheses represent the number of animals

from which the samples were taken

Species and condition

Total osmolality (mOsm/L)

Na’ (M-equiv/L)

K+ (m-equiv/L)

Black-tailed prairie dogs

Field

Lab w H,O

Lab w/o H,O

White-tailed prairie dogs

Field

Lab w H,O

Lab w/o H,O

301.2 k 3.5 N = 56

r = 214329 306.9 i 7.1

N=8 r = 2977319 343.2 k 15.0 N = 13(2)

r = 318412

296.0 + 4.5 N = 34

r = 265-310 308.0 k 8.1

N=6 r = 295-315 335.0 * 6.8 N = lO(2)

r = 318-347

137.6 rt 3.4 N = 62

r = 96187 151.2 k 7.8

N= 10 r = 134-169 156.2 + 7.7 N = 13(2)

r = 132-180

122.1 k 6.7 N = 40

r = 69-184 152.3 k 10.2

N=8 r = 125-163 169.2 k 4.6 N = 10(2)

r = 159-178

9.1 * 0.7 N = 62

r = 5518.2 3.2 i 0.3 N = 10

r = 263.9 3.5 & 0.3

N = 13(2) r = 2.64.6

8.5 k 0.8 N = 40

r = 5.3-17.3 3.3 k 0.6

N=8 r = 2.44.6 3.7 i_ 0.3 N = 10(2) r = 3.&4.2

prairie dogs. There was no significant difference among months in plasma osmolality, plasma sodium, or plasma potassium.

Both species reacted similarly to laboratory conditions in that there were no differences between the species for any of the plasma measurements made when the animals were provided with water ad lihi- turn. The only difference detected in comparisons of dehydrated animals was higher plasma sodium in white-tailed prairie dogs. Total plasma concentration and plasma sodium was higher in dehydrated animals than in field animals for both species. However, plasma potassium was higher in field animals than in either hydrated or dehydrated animals for both species.

Although differences among months in total plasma osmolality, plasma sodium, or plasma potassium were not observed for either species, differences were observed in plasma urea from month to month (Fig. 5). Plasma urea in black-tailed prairie dogs followed the trend of urine osmolality (Fig. 1) with lowest concentration occurring in July (Fig. 5). Plasma urea was significantly higher in field collected black-tailed prairie dogs during October and November than in dehydrated laboratory animals of this species. Plasma urea in white-tailed prairie dogs during July, August, and October was significantly greater than in dehydrated animals and was also significantly greater than the March sample for that species. Plasma samples were not collected from white-tailed prairie dogs in June.

Kidneys

Because a difference in ability to produce a concentrated urine was observed between the two species of prairie dogs (Fig. 1). examination of kidney structure was made to see if a morphological correlation

existed. An extensive morphological study by Sperber (1944) demonstrated that mammals of xeric habitats tend to have kidneys with a longer renal papilla than species from more hydric habitats. Since that study, others have shown that the length of the renal papilla is generally related to habitat and the ability of the animal to concentrate urine (Vimtrup & Schmidt- Nielsen, 1952; Schmidt-Nielsen & O’Dell, 1961; Mac- Millen & Lee, 1969; Schmid, 1972). Relative medull-

I Black-tailed prairie dogs (‘I’ 0 White-tailed prairie dogs

I. ” ” ” .’ M A M J J A S 0 N 1 Lob

months

Fig. 5. Field and laboratory plasma urea concentrations in black-tailed and white-tailed prairie dogs. Vertical lines represent ranges; horizontafiines represent means (X); rectangles enclose the interval X k c~,~,$.E. Numbers in parentheses represent the number of animals. For laboratory data, the left sample for each species represents dehydrated animals and the right sample represents hydrated animals. Numbers outside parentheses represent the number of

measurements from the animals involved.

448 EUGLN~ B. BAKKO

ary thickness (RMT) of prairie dog kidneys was determined according to Sperber’s calculations to see if morphological differences exist. Black-tailed prairie dogs exhibited a RMT of 6.32 k 0.16 (N = 54) which was significantly greater than the RMT of 5.85 + 0.13 (N = 40) for white-tailed prairie dogs.

Because of the small variation in plasma concentration within each species and between species. monthly urine/plasma (U/P) ratios followed identical seasonal patterns as urine osmolality for each respective species (Fig. 1) and therefore are not illustrated here. Months of maximum and minimum U/P ratios for each species are compared along with laboratory values in Table 4. There was no difference in U/P ratios between species in September when the highest values were observed. However. black-tailed prairie dogs had considerably lower U/P ratios in July than white-tailed prairie dogs did in June. the lowest months for each species, respectively. Maximum field U/P ratios for white-tailed prairie dogs was above that for dehydrated animals but this difference was not significant. Urine,Plasma values for dehydrated black-tailed prairie dogs was greater than the maximum field sample (September) for that species but this difference was not significant.

When deprived of water, white-tailed prairie dogs lost weight more rapidly and survived for a shorter period of time than did black-tailed prairie dogs (Fig. 6). Both species were able to tolerate weight losses of over 50% initial body weight. The two white-tailed prairie dogs survived to 43% and 41”,, initial body weight and the two black-tailed prairie dogs survived to 39:; and 1971; initial body weight. The largest black-tailed prairie dog started the water deprivation at a body weight (2208 g) which was larger than most field body weights. However, the other black-tailed prairie dog and both white-tailed prairie dogs started the experiment at weights similar to those of field animals. Adult body weights of black-tailed prairie dogs collected in this study averaged 1144.8g and adult white-tailed prairie dogs averaged 962.2 g. No body fat was apparent on animals of cithcr species at time of death after water deprivation.

with regard to precipitation. The low urine osmolality of black-tailed prairie dogs in July was probably a result of the increased rainfall and subsequent higher water content of the vegetation at that time. Urine osmolality for white-tailed prairie dogs, on the other hand, was slightly lower in June but not significantly below urine osmoiality in March. July, or October for that species. This corresponded to the slight increase in precipitation at Laramie during the early summer. The increased urine concentration during August and September for black-tailed prairie dogs and during July. August, and September for white- tailed prairie dogs was probably due in part to decreased precipitation and subsequent lower preformed water availability in their food at that time. Another predominant factor contributing to this may have been increased ambient temperatures. This would not only increase transpiration in vegetation but also increase the water evaporation/oxygen consumption ratio in the prairie dogs (Raab & Schmidt-Nielsen. 1972). Likewise. the decline in urine osmolality observed during October and November in both species may have been due in part to the above normal precipitation in both areas during or just preceding those collection periods. However, much of the vegetation starts to become dormant by October and November thereby restricting incorporation of water into above ground stems and leaves. Thus, reduced ambient temperatures in the fall rather than increased precipitation, may have contributed to decreased

-Black-tolled pralrle dogs ----White-toiled proirle dogs

I-Inltml body wt F-Final body wt

F=426g

DISCUSSION

Seasonal urine osmolality in the two species of Fig. 6. Response of body weight to water deprivation in prairie dogs reflected their respective environments black-tailed and white-tailed prairie dogs.

Table 4. Field and laboratory urine/plasma ratios in black-tailed and white-tailed prairie dogs. Numbers in parentheses represent the number of animals from which the samples were taken

Condition Black-tailed prairie dogs White-tailed prairie dogs

X*t 0.~75S.E. N range x+t o 975S.E. N range

Field (maximum month)

Field (minimum month)

Lab w/o H,O

8.76 + 0.63 (September)

2.92 i 0.62

(July)

9.09 k 0.62

9 7.76.-10.67

7 I .92--4. I2

11(2) 7.58~10.51

x.05 + 1.02 (September)

6.22 + 0.59* (June)

6.80 2 1.26

8 6.6610.76

12 4. I S-7.34

1 O(2) 3.45-X.74

* U/P values not paired. Mean plasma concentration for all field animals was used to compute June U/P.

Field water balance performance k prairie dogs 449

urine concentration at that time. Also, above ground activity in the fall is reduced compared to summer in both species (Tileston & Lechleitner, 1966) thereby resulting in more time spent in the burrow where humidity is high (Schmidt-Nielsen & Schmidt- Nielsen. 1950).

No fret: surface water was observed in areas of either species and probably seldom if ever occurs. Therefore, in addition to oxidative water. virtually all other water available to both species probably was preformed water in their natural foods. King (1955) reported that while black-tailed prairie dogs readily accepted grain in traps. they would ignore water dishes or even fill them with dirt. However, he did report pregnant and Iactating females eating snow and suggested that they may be dependent on it. Urine osmolality in March was lower than in Sep- tember for both species, but the difference was significant only for black-tailed prairie dogs. Because snow was present in March at both areas. it may have accounted for the lower urine osmolaiity at that time.

Urine osmolality of dehydrated black-tailed prairie dogs in the laboratory was greater than that of any field sample indicating that under natural conditions, this species was not maximally stressed for water conservation. However, urine concentrations for white- tailed prairie dogs for all periods of collection except June were not different from maximum urine concentration in dehydrated animals. Thus. white-tailed prairie dogs were apparently stressed close to maximum for water balance under natural conditions for much of the time. Also, because urine from dehydrated black-tailed prairie dogs was greater in concentration than urine from dehydrated white-taiIed prairie dogs indicates that black-tailed prairie dogs are better adapted to water stress. This was substantiated by kidney structure and U/P ratios. Black- tailed prairie dog kidneys had a greater relative medullary thickness and dehydrated black-tailed prairie dogs had a greater U/P than dehydrated white-t~liled prairie dogs.

Because the concentration of potassium in the urine of both species was associated closely with urine osmolality indicates that this was the major com- ponent to influence the variation in seasonal trends of urine osmolality for both species. The only exception to this was the March sample for black-tailed prairie dogs. which was no different from the July potassium concentration for that species. During that month, urea compensated for the low potassium concentration in black-tailed prairie dogs. There evidently was a relative dietary difference or at least a metabolic difference when considering potassium and protein utilization for black-tailed prairie dogs during March, compared to the rest of the periods, as evidenced by the decreased amount of potassium and increased amount of urea in the urine at that time.

Urine urea concentration was quite constant during all collecting periods for both species except the March sample for black-tailed prairie dogs. This means that during times of lowest urine osmolality. urea comprised a larger proportion of urine solute. Conversely, when urine osmolality was highest. urea comprised a small proportion of the urine solute. Las- siter et al. (1961) reported and Danielson et cd. (1970) confirmed that the collecting ducts in the mammalian

kidney were responsible for urea recirculation, which was greatest in animals on a low protein diet. Walser (1970) reported that ammonia nitrogen resulting from degradation may be used for protein synthesis. Nel- son et al. (1975) reported recycling of 14C-urea and D,O via the urinary bladder in black bears. Whether or not the relatively low urine urea concent~dtions during August through November for both species studied here represented urea recirculation and subsequent degradation to simpler nitrogen compounds for protein synthesis remains to be demonstrated. However, ammonia excretion in both species of prairie dogs did not disagree with the above idea. That is, if ammonia nitrogen was to be used for protein synthesis it would thus become a possible “asset” rather than a “liability” and probably would be excreted in lesser amounts. Ammonia was excreted in much smaller amounts in both species from August through November. When ammonia excretion is compared as percent of urine osmolality, the difference between the March-June-July vs the August through November samples is even more pronounced. Like- wise, plasma urea concentrations from field animals are compatible with this concept. If urea is to be recir- culated for possible degradation and subsequent protein synthesis, higher concentrations would be expected in the plasma also. This was best observed in b&k-tailed prairie dogs from August through November.

Dehydrated animals produced higher urine urea concentrations than did field animals except for the March sample from white-tailed prairie dogs, and this March sample was not significantly different from that of the dehydrated white-tailed prairie dogs. Urine potassium from dehydrated animals was lower than most field samples for both species. Potassium is usually in high concentrations in most vegetation (Ovington. 1962) and was evidently higher in natural foods than in the Purina Chow used in this study. Even if urine sodium concentration from dehydrated animals is added to potassium from the same animals, the combined electrolyte concentration does not equal urine potassium concentration for most field samples. Undoubtedly. lab diet was not similar to natural diet.

Urine sodium constituted a small part of urine osmolaiity and probably represented a small amount of animal material (mainly insects) in the diet (Kelso, 1939; King. 1955; Koford, 1958; Smith, 1958). Sodium is usually in very low concentration in vegetation (Ovington, 1962). Consequently, many hervi- vorous rodents consume some animal material as a source of sodium (Landry, 1970). Aside from the Sep- tember data for black-tailed prairie dogs. urine sodium was signi~cantly greater in white-tailed prairie dogs collected in the field throughout the year. There could have been several reasons for this, poss- ibly including a higher incidence of palatable insects in the white-tailed prairie dog habitat. Alternatively, perhaps insects helped to supply water to the more water stressed white-tailed prairie dogs. The five unusually high urine sodium values for black-tailed prairie dogs occurred in September when urine osmolality was greatest. This could have been a response in a few individuals to negative water balance with insects being consumed as a possible water source.

450 EUGENE B. BAKKO

Plasma concentrations of field animals were similar for both species except that plasma sodium concentration in white-tailed prairie dogs was low. Trauma may cause a sodium-potassium shift in the plasma which results in a decrease in sodium and an increase in potassium (Friedman & Friedman, 1963). The shooting of field animals in this study may explain why sodium was lower and potassium was higher in field animals than in hydrated laboratory animals. However, another factor that may have contributed to this was the relatively high sodium content of the laboratory food compared to natural vegetation. Con- versely, the higher potassium concentration in plasma of field animals compared to hydrated lab animals may have been due to the naturally high potassium in vegetation. The greater plasma sodium concentrations recorded in hydrated laboratory animals compared to field animals of both species did not increase total osmotic pressure of the plasma as much as might be expected. This may have been a result of an outward shift of plasma colloids due to increased vascular permeability (Horowitz & Borut, 1973). Dehydrated animals demonstrated higher total plasma and plasma sodium concentration as expected.

The ability of black-tailed prairie dogs to survive longer without water further substantiated their superior adaptation to negative water balance. Ani- mals of both species ended the experiment at similar body weights. The absence of body fat at time of death indicated that both species were able to survive on metabolic water until fat reserves were depleted. Hudson (1962) reported that mammals with a U/P ratio less than 10 were unable to maintain weight on a dry diet. Dehydrated black-tailed prairie dogs, with a U/P ratio close to 10 (9.09 + 0.62) were able to survive for 122 and 238 days for an animal of average weight and an obese animal, respectively. This represents the longest survival time reported to date for a rodent species not capable of maintaining body weight on a dry diet. Also, few species have been reported to tolerate over a 50% weight loss. Chew (1951) reported a 36-53x weight loss in Pero- WTJ'SCUS lrucopus. Schmidt-Nielsen rt ul. (1948) reported a 52.60/:, weight loss in Rattus rzorwyicus and Bredahl (1969) reported a 53% weight loss in Spermo- philus frankhii. Both species of prairie dogs in this study tolerated weight 16sses of over 50%. No rodent has been reported to tolerate a weight loss equal to that of the prairie dogs in this study.

It is interesting that black-tailed prairie dogs. although living in a more mesic environment, are better adapted to xeric conditions than are white-tailed prairie dogs. Black-tailed prairie dogs do not hibernate (King, 1955; Koford, 1958; Smith, 1958; Tileston & Lechleitner, 1966), whereas white-tailed prairie dogs probably do hibernate (Stockard, 1930; Tileston & Lechleitner, 1966; Bakko & Brown. 1967). These authors also reported that although white-tailed prairie dogs were observed above ground for eight months of the year (late February to October), individuals were active above ground for only 4-5 months. Adults appear above ground in late February or early March and return permanently to their burrows in mid-July or August. Reproduction occurs in March. Juveniles appear above ground in mid-June and

remain active through October. Therefore, adults and juvenile white-tailed prairie dogs are feeding together on the available vegetation for only about one month. This period coincides with the most productive period of plant growth as governed by precipitation for that area. Survival of juvenile white-tailed prairie dogs under the dry conditions of late summer and fall probably indicates that adults also could survive above ground at that time. However, there may not be enough succulent vegetation to maintain the entire population (both age classes) of each colony through the dry period whereas there is enough for the juveniles. If an extremely dry period should occur, the adults would have a better chance of surviving to the spring reproductive period because they put on body fat during the “green” period followed by a retreat to cool, moist. underground burrows. Thus, white-tailed prairie dogs have evidently adapted to xeric conditions by means of torpor (Fisher & Manery, 1967).

Furthermore, although white-tailed prairie dogs live in socially structured colonies (Tileston & Lech- leitner, 1966). they are not as highly organized as are black-tailed prairie dogs and density within the colony is greater for black-tailed prairie dogs (King, 1955; Koford, 1958; Smith, 1958: Tileston & Lech- leitner, 1966; Clark. 1969). The greater amount of precipitation that occurs in the habitat of the black-tailed prairie dog results in more vegetation for that species. This allows for a higher density of animals and, subse- quently, more social interaction. Because a major por- tion of this increased precipitation is received during May and June. the black-tailed prairie dog must face dehydration under natural conditions at other periods of the year comparable to that of the white-tailed prairie dog. This precipitation pattern is similar throughout the range of the black-tailed prairie dog. (U.S. Dept. of Comm. Weather Bureau, Climatic Summary of the U.S.. 1931~1952). It apparently has been more advantageous for the black-tailed prairie dog to increase renal efficiency. rather than rely on torpor, as a means of adapting to this combination of climatic factors. Maintenance of highly organized societies by black-tailed prairie dogs would be favored by a nearly continuous interaction of the entire colony. For white-tailed prairie dogs on the other hand, spending a substantial period of time underground each year in addition to living in less dense colonial populations has precluded the more social nature observed in black-tailed prairie dogs.

A~knowlr~ye,)~er~ra--I am indebted to Dr. William D. Schmid of the Department of Zoology. University of Min- nesota, for his invaluable advice and assistance and for his critical review of the manuscript. Special thanks are extended to Drs. E. C. Birney and P. J. Regal for their constructive criticism. and to D. Nelson, W. Saatala. T. Clifford, W. Chilian. and J. Enestvcdt for assistance. I am also very grateful to R. Cunningham. Theodore Roosevelt National Park. and to the many ranchers. especially T. Stevens and J. Wallis, who were extremely cooperative. This study was supported in part by NSF Traineeships GB6158 and GZl628.

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Field water balance performance in prairie dogs (Cynomys leucurus and C. ludovicianus)