PREGNANCY AND OVULATION DETECTION IN BISON (BISON BISON) ASSESSED BY MEANS OF URINARY AND FECAL STEROIDS Author(s): Jay F. Kirkpatrick, K. Bancroft, and V. Kincy Source: Journal of Wildlife Diseases, 28(4):590-597. Published By: Wildlife Disease Association DOI: http://dx.doi.org/10.7589/0090-3558-28.4.590 URL: http://www.bioone.org/doi/full/10.7589/0090-3558-28.4.590

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Journal

PREGNANCY

AND

ASSESSED

OVULATION

BY MEANS

DETECTION

OF URINARY

of

Wildlife

IN BISON

AND

FECAL

Sexually

lation by diagnosis

mature

means of urinary was determined

bison (Bison bison) steroid metabolites among 18 bison cows,

28(4), Disease

1992, pp. 590-597 Association 1992

(BISON

BISON)

STEROIDS

Jay F. Kirkpatrick,’ K. Bancroft,2 and V. Kincy2 1 Deaconess Research Institute, 1500 Poly, Billings, Montana, 59102, USA 2Department of Biological Sciences, Eastern Montana College, Billings, Montana

ABSTRACT:

Diseases, © Wildlife

59101,

cows were tested and fecal steroids.

USA

for both pregnancy The accuracy of

and ovupregnancy

in approximately the third month of gestation, by means of urinary pregnanedio!-3#{244}-glucuronide (PdG), urinary estrone conjugates (E,C), and fecal total estrogens (TE). Urinary PdG was 100% accurate, urinary E1C was 89% accurate, and fecal TE was 100% accurate in predicting pregnancy. Fecal progesterone (P4) and TE, as well as urinary EC and PdG concentrations all increased from conception (August) through January, but significant differences were not apparent until November. During the rutting season ovulation was detected by increases in either urinary PdG or fecal P4 concentrations. Both pregnancy and ovulation were detected in uncaptured bison with reasonable accuracy by means of urinary and fecal steroids or their metabolites. Key words: Bison, Bison bison, ovulation, pregnancy, reproduction, steroids, urine, feces.

INTRODUCTION

detection total and

Until recently the study of reproductive physiology in large free-roaming wildlife has required immobilization on capture of animals to measure blood. During the of pregnancy and ovarian function have been based

endocrine past decade, non-invasive in captive exotic on measurement

nary 1983; from

steroid Lasley, certain

metabolites 1985). Urine free-roaming

used

in

study

the

levels diagnosis study

of

et al., 1991a). Very little

in of

species of uri-

means olites, by

Kirk-

and

cycles

Kirkpatrick,

ican bison Kirkpatrick While

in 1991)

feral and

horses North

means

study stand

(Lasley Amer-

regulation

(Bison bison) (Kincy et al., 1990; et a!., 1991b). these techniques are successful,

success pressures.

collection of urine, even in snow, can be time-consuming. Use of feces for similar studies has such advantages as easily observable elimination by the animal and relatively strategy

means

of

of fecal

et a!., 1990b) (Kirkpatrick about

the

repro-

fecal steroid could be

urinary

PdG hypotheses of fecal urinary

and

metabdetected feca!

pro-

tested estrogens estrogen

were and and

progesterone metabolites differed significantly between pregnant and non-pregnant animals, and (b) ovulation could be detected by identification of a luteal phase pattern of excretion of fecal progesterone and urinary progesterone metabolites. Our

gesterone metabolites (iPdG). Collection of serial urine samples has permitted the characterization of conceptive and nonconceptive

by

of free-roaming bison. this study were to decould be detected by

of urinary and and if ovulation

gesterone (P4). The (a) concentrations progesterone and

patrick et a!. (1988, 1990, a, b) diagnosed pregnancy in uncaptured feral horses (Equus caballus) by measuring urinary estrone conjugates (E1C) or non-specific pro-

horses

is known

ductive physiology The objectives of termine if pregnancy

(Loskutoff et a!., can be collected wildlife and

reproduction.

in feral

estrogens (Kirkpatrick fecal steroid conjugates

was based on the mechanisms and that

the

the desire to of reproductive

changes

accompany

MATERIALS

underself-

in reproductive environmental

AND METHODS

Animals in this study were part of a herd of approximately 80 bison inhabiting a 200 ha range in northern Wyoming (44#{176}44’N, 109#{176}2’W). The vegetation included predominantly mixed-grass prairie and has been described by Knight et a!.

easy location of the excrement. This has led to successful pregnancy 590

KIRKPATRICK

(1987).

Cows

ranged

in age

from

3 to 17 yr.

Six

sexually mature bulls were present among the herd at all times. Water was available from natural sources ad libi’tum and feed was natural grass. Individuals were identified by numbered ear tags. Experiment 1: During November 1988, bison were observed from a distance of 50 to 100 m; urine samples were collected from 18 cows. Urine was aspirated from pools on the ground or extracted from freshly soaked earth as described by Kirkpatrick et a!. (1988). Samples were kept on ice during the day of collection and stoned at -7 C without preservatives until tested 2 to 3 mo later. Fecal samples were stored in plastic bags at -7 C until tested. Urine samples were diluted 1:2 with distilled water (dH2O); 20 l of the diluted sample were analyzed for pregnanediol-3#{246}-glucuronide (PdG) and E,C. The enzyme immunoassays for PdG and E1C have been described previously (Kirkpatrick et al., 1990a; Munro et al., 1991) and the PdG assay has been validated in bison (Kincy et al., 1990; Kirkpatrick et al., 1991b). To account for differences in urine concentrations, urine samples were diluted from 1:50 to 1:100 with dH2O and analyzed for creatinine (Cr) concentrations by the microcolorimetnic method of Taussky (1954). Pregnanediol-3-#{244}-glucuronide and EC values were calibrated to Cr values and reported as ng/mg Cr. Wet fecal samples were weighed and 0.5 g samples were extracted in ethyl acetate/hexane (3:2, V/V) and analyzed for total estrogens by radioimmunoassay (Kirkpatrick et al., 1990b). The cross-reactivity of the anti-estrogen antibody with 17#{244}-estradiol was 11% (Kirkpatrick et al., 1990b). Approximately 5,000 counts per minute (cpm) of 3H-17 estradiol was added to each fecal sample before extraction in order to estimate recovery of estrogens. Total estrogens were reported as ng/g wet feces. In January 1989, the bison were confined in chutes and tested for pregnancy by rectal palpation; calves were counted during April, May and June. Based on the dates of partunition, 12 of the conceptions had occurred between 15 July and 10 August 1988.

Experiment 2: Fecal samples were collected from six bison cows in September, November 1989 and January, 1990. Weighed samples were extracted with dH2O, the residue dried and weighed, 0.25 g was rehydrated and extracted with diethyl ether, and redissolved in 95% ethanol by the methods of Desaulniers et al. (1989). Approximately 10,000 cpm of ‘I-progesterone was added to each fecal sample before extraction in order to estimate recovery of P4. Twenty

ET AL-PREGNANCY

,l of the dHp,O

AND OVULATION

extract

were

IN BISON

analyzed

for PdG

and EC. The ethanol extracts were 1:100 to 1:1,000 in dH2O and 20 il were for total estrogens by radioimmunoassay

patrick et al., 1990b), immunoassay (Munro

and and

591

for P4 by Stabenfeldt,

diluted

assayed (Kirk-

enzyme

1984). given as ng/g dry feces. Mean for September 1989, November 1989, and January 1990 were tested for significant differences with Student’s t-test (Freedman et al., 1978). Pregnancy was confirmed by rectal palpation in January 1990, and calf counts

All values concentrations

are

were made in April, May and June, 1990. Dates of partunition indicated that five of the six conceptions occurred between 25 July and 15 August.

Experiment 3: Urine and fecal samples were collected approximately every 2 to 4 days during the rutting season from five sexually mature cow bison between 31 July and 31 August 1989. Urine samples were collected, stored, and analyzed for PdG as described in experiment 1. On some days both urine and fecal samples were collected from the same cow but on other days only

one

samples yl ether as

type

were and

described

of

sample

was

collected.

weighed and extracted the residue redissolved by

Desaulnier

et

Fecal

with diethin ethanol (1989). The

al.

ethanol extracts were diluted 1:100 in dH2O and 20 zl were analyzed for P4 (Munro and Stabenfeldt, 1984). The patterns of urinary PdG and fecal P4 excretion were recorded for each bison cow and compared by regression analysis; the correlation coefficient for the two hormones was determined (Freedman et al., 1978). RESULTS

Experiment 3H-17f3 (±6.45)%. nant

1:

Mean

estnadiol Fourteen

during

January

by rectal palpation, calves during 1989. gen analysis was pregnancy, with lowest value in

(±SE)

recovery

from feces of 18 cows 1989 and The

was were

as determined all 14 delivered total fecal estro-

the most accurate 1.09 ng/g feces pregnant cows

ng/g being the highest value pregnant cow (Table 1). Using feces

as the

total accurate cy,

minimum

fecal estrogen as a diagnostic

of 62.18 preg-

value analysis test for

for

test for being the and 0.20 in

a 1.0

nonng/g

pregnanwas 100% pregnancy.

Urinary PdG analysis was equally accurate. The lowest urinary PdG value for pregnant cows was 54.7 ng/mg Cr while 9.9 ng/mg Cr was the highest value for a

592

JOURNAL

TABLE

1.

OF WILDLIFE

Urinary

concentrations

Bison

DISEASES,

VOL. 28, NO. 4, OCTOBER

(PdG),

pregnanediol-3#{244}-glucuronide

for

reproductive

pregnant

bison

at

group

Pregnant

(n

three

urinary

gestation,

PdG (ng/mg Cr)

estrone and

conjugates

nonpregnant

EC (ng/mg

(EC),

and

54.7

Mean SE

113.30 18.57

Total

(n

9.4

to 302.9

to 83.5

1.09

26.74 5.65

4)

=

3.6 6.82

5.62

0.16

SE

1.55

2.03

0.02

cow.

between

urinary

PdG

The

total was

to 9.9

2.7

correlation

fecal

r

0.70

=

coef-

estrogens (P

and 0.001).


10.0 ng/mg Cr minimum PdG value for pregnancy,

as the uri-

nary PdG analysis was 100% accurate in predicting pregnancy. The urinary E1C analysis was less accurate in predicting pregnancy. for pregnant the

(P

The lowest cows was

highest

pregnant correlation estrogens =

E1C

nary

urinary E1C value 9.4 ng/mg Cr and

concentration

0.049).

Using E,C

E1C

10

value

analysis

ng/mg for

was

all rose between approximately

September 0.001) Both

E1C

and

concentrations tion period the estrous Asdell, bonasus)

had cycle

Urinary

November,

PdG

but

did Janrose

and

European bison and Raczynski,

fecal collecwith taurus) (Bison 1967).

from feces P4 concen-

ranged to 3,000

beng/g

feces and reached a peak of 5,000 to 10,000 ng/g midway through the luteal phase (Fig. 2). These values were similar to those in domestic cows (Desaulniers et al. 1989). Basal urinary PdG ing ovulation ranged mg Cr and reached

concentrations precedbetween 5 to 100 ng/ a peak of 350 to 1,000

during

phase (Fig. 2). The between urinary the five bison cows

the

August

rut

ranged

a low of r = 0.310 to a high of r however, in all five cases the luteal

pattern

of P4 secretion

hormones.

Four

was

of the

evident

five

=

for both

bison

demon-

strated classic estrous behavior which was coincidental with both PdG and P4 nadins immediately preceding luteal phase elevation. Four of the five bison had a second estnous dates

of

cycle during parturition

those second conception.

Septem-

during the 32-day a pattern consistent of the cow (Bos

1964) an the (Krasinski

ovulation 2,000

from 0.922;

between November and fecal P4 and total estrogens

3:

preceding approximately

monitored

4.5 mo postconE1C and PdG did (P < 0.05) be-

Experiment

trations tween

the

and

to 0.2

Mean (±SE) recovery of 19-P4 was 61.8 (±5.3)%. Basal Fecal

uri-

as

and PdG concentrations

(P 35 days postconception) detection of pregnancy in the Penisso-

(B)

through

urinary

of

January

Collection

pregnanediol-3#{246}-glucuronide

approximately

180 days

of pregnancy.

dactyla and particularly the Equidae (Kassam and Lasley, 1981; Kasman et al., 1985, 1986, 1988; Czekala et al., 1990), but these early

steroid detection

Bovidae. metabolize

metabolites are of pregnancy

This is probably plasma estrogens

of conjugated

point where predictors

of

useful among

because to other

compounds.

to 4 mo of pregnancy, trations have increased

not

for the

bovids forms

However, estrogen in bovids

by

estrone conjugates are pregnancy, despite

useful repre-

senting only a minor urinary metabolite. This is corroborated by the dramatic crease in fecal estrogens demonstrated Safer-Hermann

et a!.

(1987)

3

concento the

in cows,

inby red

594

JOURNAL OF WILDLIFE DISEASES, VOL. 28, NO. 4, OCTOBER 1992

6000

400

(i

-5000 300

E

E -4

0I

C

#{163}

#{163} 0

o

0.

0 .5

0.

a

0.

a

IL.

.,

0

200

a. 3

-

U

100

a

2000

30

Day

+10

20

Day

Coll.ctlon

of

a

U

a

of

0

30

CoIl.ctlon

7000

500-

c5

C,

6000

400-

E

.

5000 C

C

300 -4000

0 200’

0

a.

0

0

0.

:

3000

a U .

a U.

U.

2000

100’

,.

0

.

10

20

Day

of

10

40

30

Day

ColI.ctlon

20 of

CoIl.ctlon

1000

PdG(ngmgCr)

-=

FscalPo(ngi9)

4-

C)

E C C

0

0.

C .5 0.

S U S

U.

a C

Day

2.

FIGURE

excretion

Patterns

during

of

the luteal

urinary

phase

of

ColI.ctlon

pregnanediol-3#{244}-glucuronide

for five bison

cows.

(PdG)

Arrows

indicate

and

fecal

the days

progesterone

of observed

(Fecal

behavioral

Po)

estrus.

buffalo (Syncerus caffer nanus) and yak (Bos mutus). The primary fecal estrogen during pregnancy in cows, after 90 days postconception, is 17#{244}-estradiol (Most! et a!., 1984), and the elevation of estrogens is great enough that an estrogen radioimmunoassay with only an 11 % cross-reac-

sitive enough for pregnancy detection. The assay in this study, however, was used to measure total estrogens, and the presence of 17#{246}-estradiol in pregnant bison is only assumed. Use estrogen

of

tivity

nancy

detection

with

this

particular

metabolite

is sen-

urinary PdG, concentrations in bison

E1C, on fecal for accurate was

most

total preg-

reliable

KIRKPATRICK

after 90 days postconception. The of increase in fecal total estrogens nary E1C in plasma

in the total

gens seen (Desaulniers

in

The small imals in this the

full

bison is similar estrogens and

the pregnant et al., 1989). number study

range

to changes fecal estro-

domestic

cow

of non-pregnant prevented analysis

of

values

measured. Perhaps with of non-pregnant animals, mone curacy crease.

pattern and un-

values would of pregnancy

be

for

the

steroids

a larger the range

greater diagnosis

anof

number of hor-

and the might

acde-

Ovulation and formation of the corpus luteum could not be confirmed by rectal palpation or ultrasound in bison of this study. detected table

While by

presence of a fetus could be rectal palpation, the intrac-

nature

of the

animals

did

not

permit

ET AL-PREGNANCY

AND OVULA1]ON

traction. Conjugated are excreted primarily after being resorbed vascular bed; however,

IN BISON

steroid metabolites by way of the urine, from the gut into the a small proportion

of the conjugates remain trapped gut and are excreted in the feces and Kirkpatrick, 1991). These fecal conjugates the ether

remain extraction on

water used

based

niers this

et a!. (1989), who successfully method to the fecal analysis

recent

muskoxen P4 could

not

in the (Lasley steroid

soluble. Finally, for progesterone

was

cows and Tnitiated

the

595

work

of

Desaulapplied of P4 in

(Ovibus moschatus). be used for deter-

mination of P4 recovery because large amounts of plant pigments also are removed with the ether extraction, and the interference of the spectrophotometny is too great for liquid scintillation counting. Validation

of

urinary

and

fecal

steroid

the sensitive palpation techniques required for detection of corpora lutea. Ultrasound was not available. Despite the in-

analysis in large intractable ficult and cannot always procedures used with

ability these

(Lasley and Kirkpatrick, 1991). Validation of these methods rests on several assumptions. First, it has previously been dem-

to confirm direct methods,

ovulation by the pattern

either of of P4 se-

cretion was indicative of ovulation. There can be at least three causes for increases in P4, including ovulation, formation of a persistent

corpus

luteum,

on extra-ovarian

(adrenal) formation

P4. However, only ovulation and of the corpus luteum result in

bison

the P4 pattern seen in these bison. There was an evident 2 to 3 day lag in excretion of fecal P4 compared to the excretion of urinary PdG. Despite the coefficient between urinary P4 in some of the animals, pattern was clearly evident indicator

low correlation PdG and fecal the lutea! phase and a reliable

of ovulation.

Several were used

different for the

extraction recovery of

onstrated between

methods steroids or

Second, matography validate mary

the

between

(Kirkpatrick

et a!., validation of the

traction

measured.

organic

solvent

ex-

bison

This (1975),

primary cow also

and the PdG have been

physiological ovulation and precise nature

than

in

1990c). Fehen the

trogens and diagnosis of pregnancy in feral horses (Kirkpatrick et a!., 1990b). Extraction of E1C and PdG required water exrather

plasma

in

therefore, PdG and 2) imply

and

fecal

P4.

performance liquid chropreviously has been used to presence of PdG as the pri-

P4 metabolite

parallelism

1991b); urinary here (Fig.

between high

strated that the domestic

timate measure

the es-

et a!.,

patrick et a!., the work of

covery previous

based on of fecal

(Kirkpatrick

a correlation

ples ously

of free estrogens was successful extraction

that there is a strong correlation plasma P4 and urinary PdG

the correlations between fecal P4 demonstrated

their conjugated metabolites for the three experiments. The ethyl acetate/hexane extraction used in experiment 1 for the re-

animals is diffollow the same captive animals

(Kirk-

P4 metabolite in was PdG. Third,

serially standard demonstrated 1991b).

urine

is supported by who demon-

diluted curve Finally,

of these techniques accuracy in predicting events in question, pregnancy, rather of the metabolites

sampreviin bison the

ulis a the

namely than the being

596

JOURNAL OF WiLDLIFE DISEASES, VOL. 28, NO. 4, OCTOBER 1992

ACKNOWLEDGMENTS The

authors

gistical

gratefully

support

of the

Bar-X

study

was

acknowledge

provided

Ranch,

by Mrs.

in Powell,

funded

in part

by

tional Science Foundation 01 and DCB-8922800.

1964.

CZEKALA,

N.

Sigma

L.

This

Xi and

Na-

H.

ductive

Press,

Ithaca,

J.

KA5MAN,

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T.

1975.

Gas

pregnanediols

in

Veteninania

during

Statistics.

W.

W.

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Norton,

(Bos Ca-

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A.

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Pregnancy and ovulation detection in bison (Bison bison) assessed by means of urinary and fecal steroids.

Sexually mature bison (Bison bison) cows were tested for both pregnancy and ovulation by means of urinary steroid metabolites and fecal steroids. The ...
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