BOSTON PUBLIC LIBRARY
3 9999 06317 721 4
COTTONTAIL REPRODUCTION
RELATED TO DIELDRIN
EXPOSURE
///
Bos.
nient?
Pm° 1 1 1974
DEPOSITORY
UNITED STATES DEPARTMENT OF THE INTERIOR
BUREAU OF SPORT FISHERIES AND WILDLIFE
Special Scientific Report-Wildlife No. 177
UNITED STATES DEPARTMENT OF THE INTERIOR
Bureau of Sport Fisheries and Wildlife
COTTONTAIL REPRODUCTION RELATED TO
DIELDRIN EXPOSURE
By
Richard A„ Malecki, Stephen H„ Allen, and John 0. Elliston
U.S. Bureau of Sport Fisheries and Wildlife
Missouri Cooperative Wildlife Research Unit
Columbia, Missouri
Kenneth C„ Sadler
Missouri Department of Conservation
Columbia, Missouri
W„ Reid Goforth and Thomas S. Baskett
U„S„ Bureau of Sport Fisheries and Wildlife
Missouri Cooperative Wildlife Research Unit
Columbia, Missouri
Bureau of Sport Fisheries and Wildlife
Special Scientific Report—Wildlife No. 177
Washington, D„C„ • 1974
Present addresses: Allen, North Dakota State Game and Fish
Department, Bismarck; Elliston, Morgan Veterinary Clinic, Coos Bay,
Oregon; Goforth, Northern Prairie Wildlife Research Center, James-
town, North Dakota.
CONTENTS
ABSTRACT iii
INTRODUCTION 1
MATERIALS AND METHODS 2
RESULTS 4
Onset and Synchrony of Breeding 4
Ovulation 5
Prenatal Mortality 6
Embryonic Litter Size 8
Testes 8
Lactation 9
Adult Mortality 10
Chemical Residue Determinations 11
Stress 15
CONCLUSIONS AND DISCUSSION 17
ACKNOWLEDGMENTS 18
REFERENCES 20
APPENDIX I 22
APPENDIX II 24
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1 1
ABSTRACT
Wild-trapped young-of-the-year cottontails (Sylvilagus
floridanus) , confined in 1-acre pens, were exposed to annual
ground applications of 0.5 and 2.0 pounds/acre of granular
dieldrin. Reproductive data from rabbits in treated pens were
compared with control groups during six breeding seasons,
1966-1971.
Breeding male rabbits in the pens showed no sign of
reproductive abnormality. Testis weights were comparable at all
dosage levels (P>0.05) and spermatozoa were evident in
microscopic examinations of the seminiferous tubules.
No measurable differences in onset and synchrony of breeding
were found among females in treated and control groups.
Conception dates for the penned rabbits corresponded closely
with those of wild, unpenned cottontails collected nearby.
Based on second pregnancies, ovulation rates,
preimplantation losses, resorption of embryos, and embryonic
litter size were not significantly affected (P>0.05) by the
treatments .
Residue levels in brain, liver, and muscle tissues of
rabbits from the two treatment levels were significantly higher
than those of control animals. A comparison of brain residue
levels within the two treatment groups also indicated that
accumulation of the pesticides was related to the amount applied.
Lethal accumulations of dieldrin were found in brains of three
cottontails. We recovered fewest breeding animals from pens with
highest treatment levels, but differences in recovery rates were
not significant (P>0.05). No adequate measures of postnatal
mortality were obtained.
Paired adrenal weight :body weight and spleen weight :body
weight ratios, plus histological information about cortical
lipid distribution in the adrenal glands showed no conclusive
evidence of stress among penned animals, whether treated or not.
Dieldrin persisted in soil from 1 year to the next,
following the annual applications, which fell within the limits
of recommended agricultural rates. Dieldrin residue levels in
cottontail tissues (brain, liver, muscle) reflected application
rates and soil residue levels .
in
INTRODUCTION
Mechanisms by which organochlorine insecticides affect
organisms are not completely understood. Toxic responses of wild
animals, involving the peripheral and central nervous systems,
are often observed following administration of lethal doses or
heavy field applications. Subtle effects of non-lethal doses are
far less distinguishable, but may be very important. Alterations
of hormone and enzyme metabolism are possible consequences
(Peakall, 1967; Hart et al., 1971). The influence of such
changes on population dynamics of the species involved is not
clear. Information about the effects of organochlorines on the
reproductive performance of wild animals exposed to these
insecticides is needed.
The purpose of this investigation was to test the effects of
dieldrin (1,2,3,4 ,10 ,10-hexachloro-6 ,7-epoxy-l , 4, 4a, 5, 6, 7,8, 8a-
octahydro 1 :4 ,5 :8-dimethanonapthalene) on the reproductive
processes of the cottontail (Sylvilagus f loridanus) . The
cottontail was selected due to: (1) its prevalence on farmland
where pest control practices make it a readily exposed nontarget
species, and (2) the abundance of reproductive data on this
species under both wild and semiwild conditions, facilitating
evaluation of treatment effects.
MATERIALS AND METHODS
Twelve 1-acre pens were constructed at the University of
Missouri's Ashland Wildlife Area in Boone County, Missouri. Pen
walls made of 1-inch mesh poultry wire were 5 feet high with an
additional 6 inches of wire buried in the ground. An electric
wire was installed around the top of the fence and padded steel
traps were placed on posts in and around the pens to minimize
losses to predators . Cedar brush piles were provided to
supplement natural cover.
Commercial rabbit pellets were offered ad libitum in covered
feeders. Food plots 20 x 150 feet were planted to milo in each
enclosure .
Soil samples were obtained annually from all pens beginning
in November 1965 (before initial application of dieldrin) and
ending in April 1971. Twenty- five samples (minimum of 25 grams
each) were randomly collected from approximately the top 3 inches
of soil in each pen during 1965-69. These were then combined to
give one aggregate sample for each pen.
Prior to 1965, none of the 12 pens had been treated with
pesticides, and all were relatively free of them. Four pens
served as controls and received no treatment. From 1965 to 1971,
annual treatments of 5% granular dieldrin were applied to the
remaining pens during December and January, after the pens were
stocked with cottontails. Four received 0.5 pound/acre of
active dieldrin and the other four, 2.0 pounds/acre.
Applications were made by a tractor-mounted broadcast seeder.
Application levels were within ranges recommended (before
inception of the experiments) for white- fringed beetle control in
cottonfields or for control of several species of insects in
ungrazed turf areas (United States Department of Agriculture,
1965) . Our application levels were well below the 3.0
pounds/acre used by Federal and State agencies in an intensive
campaign against Japanese beetles near Sheldon, Illinois, in
1954-55 (see Scott et al., 1959).
Test animals were live trapped within a 20-mile radius of
the research site. Ear-tagged cottontails were stocked annually
in a ratio of 1 male:2 females (except 1971) in each of the 12
pens. In 1966 through 1968, each pen received 2 males and 4
females; in 1969, 4 males and 8 females; and in 1971, 5 males and
12 females. Only young-of-the-year were used to assure some
uniformity in reproductive performance (Conaway et al., 1963).
Animals trapped in the wild prior to December, and weighing less
than 900 grams, were considered to be juveniles of that year.
This criterion has been substantiated under comparable conditions
by lens weight comparisons (Sadler, unpublished data) .
Rabbits were left in the treated and control pens until the
females were approximately 18 days pregnant with the second
litter. At this time all penned rabbits were collected,
sacrificed, and weighed. Reproductive organs, spleens, and
adrenals were removed and fixed in either 10% formalin or a
solution of alcohol, formalin, and acetic acid (AFA) . Samples
of brain, liver, and muscle were immediately frozen for dieldrin
analysis .
In 1970, rabbits introduced into the pens the previous fall
were allowed to breed for a full season, then removed from the
pens. Young-of-the-year progeny of these rabbits were then kept
in the pens until the following spring breeding season. The
purpose of this procedure was to evaluate the effects of dieldrin
on first season reproduction of rabbits born to exposed parents
in the pens .
In the spring of 1968, heavy predation occurred in the pens
and no meaningful reproductive data are available for that year.
However, data on dieldrin residues and spleen and adrenal
condition from that year are included in this presentation.
Chemical analyses were made by WARF Institute, Inc.,-/ using
electron capture gas chromatography. Methodology is described in
Appendix I.
Captive females were trapped each spring to determine
breeding condition, using Haugen's (1942) procedure involving
palpation of the abdominal walls between the thumb, index, and
middle fingers to locate uterine swellings at the sites of embryo
implantation. These swellings were classified by approximate
size: peanut (age of embryo=10 days) ; acorn (age=15 days) ; or
walnut (age=20 days) . The time of the year and the fact that
abdominal hair had not been pulled to line a previous nest served
as indicators that the female was pregnant with her first litter
of the year. Wild, free-ranging cottontails were periodically
collected in the vicinity of the pens, palpated, then autopsied
to corroborate breeding condition assessments made by abdominal
palpation of penned rabbits.
We assumed that penned and wild rabbits were in similar
stages of pregnancy, as was true in other central Missouri
studies (Conaway and Wight, 1962) . The limited collections
outside our pens reinforced this assumption.
-f Companies referred to in this publication do not imply
endorsement of the service by the Government.
When females were approximately 18 days pregnant with their
second litter, corpora lutea resulting from the second pregnancy
were easily visible and the first-litter young had been weaned.
Also, the critical stage of resorption was past, permitting a
more accurate determination of litter size (Brambell and Mills,
1948) .
Ovaries from all females were sectioned at 10 microns and
mounted as interrupted serials (every tenth section mounted) .
Sections were stained with a modified Schorr stain and examined
microscopically. Particular attention was given to the
following: 1) primary follicles in the ovarian cortex and
sinusoids in the corpora lutea (di Fiore, 1961) ; 2) necrosis and
degeneration of germinal epithelium (Albert, 1962) ; 3) cell size
and nucleus size; and 4) character of the ovarian connective
tissue. The ovulation rate was then determined by counting the
number of corpora lutea in the sectioned ovaries.
A wedge was removed from each testis, and slides were
prepared using the same staining and mounting procedures as
described for the ovaries. Sections were examined for the
following indications of pathological conditions: 1)
degeneration and disappearance of spermatogenic cells; 2)
dividing Sertoli cells; 3) giant multi-nucleated developing sperm
cells; and 4) abnormally large numbers of fibroblasts in
interstitial areas (Maximow and Bloom, 1957) .
During autopsies, embryo age was obtained by visually
estimating the size of the uterine swellings. From this
information, the time of second litter conception was determined.
Females having no visible embryos, but showing other signs of an
earlier pregnancy (i.e. having little or no fat, possessing
well-developed mammary glands which exuded milk when sliced, or
having abdominal hair pulled) were considered as being in
preimplantation postpartum pregnancy. This judgment was based on
the findings of Wight and Conaway (1962) who noted that almost
all female cottontails breed postpartum after first pregnancies.
Approximate dates for the onset of breeding were established by
backdating 28 days (average gestation) from second litter
conception dates.
RESULTS
Onset and Synchrony of Breeding
In each year, the majority of females from the control pens
and those of both treatment levels could be divided into two main
groups with respect to time of onset of breeding. For the entire
study, dates of onset of breeding were as follows: March 1 and
March 8-9, 1966; March 2 and March 10, 1967; March 16 and March 23,
1969; March 1 and March 12, 1971. In each instance breeding
periodicity was substantiated by comparable data from wild
cottontails in the region.
Although cottontails are generally synchronous breeders, a
few individuals conceived between the breeding dates established
for most years, as shown by ages of embryos collected on a single
day (Appendix II, Table A) . Such findings are not unusual,
however, since unfavorable weather occurring at this time of the
year has been shown to upset this synchrony (Marsden and Conaway,
1963; Sadler and Conaway, 1971) .
Ovulation
Each year, the ovulation rate of female cottontails was
numerically higher for rabbits at the 2.0 pounds/acre treatment
level than for those at the other levels (Table 1) . These
differences, however, were not significant (analysis of variance;
0.5 <P <0.10) . There were no statistically significant
differences in ovulation rates by year within the same treatment
levels .
Table 1. Mean ovulation rates per female cottontail for second
litters .
No treatment Dieldrin treatment level
(control^ 0.5 lb/acre 2.0 lbs/acre
Year x Sx x Sx x Sx
1966 5.64 + 0.372 5.86 + 0.466 6.80 + 0.551
1967 6.50 + 0.872 6.13 + 0.436 7.00 + 0.712
1969 6.67 + 0.318 7.21 + 0.330 7.94 + 0.308
1971 5.83 + 0.229 5.68 + 0.221 5.90 + 0.283
It is possible that the number of ova recorded is biased
upwards. This could occur if luteinized follicles existed which
could not be differentiated from true corpora lutea (Conaway and
Wight, 1962) .
A few instances of polyovulation were observed in both
control and treated females. For example, rabbit no. 1545
(control, 1966) had seven embryos (six viable, one resorbing) ,
but only six corpora lutea (see Appendix II, Table A) .
Polyovulation was not a significant source of error in
determination of ovulation rates because it was infrequent; this
conclusion was also reached by Wight and Conaway (1962) .
In 1967, two of five females from the 2.0 pounds/acre
dieldrin treatment showed no corpora lutea or albicantia in the
ovaries for either the first or second litters of the year. This
is unusual for cottontails once most females are pregnant with
their second litters, as shown by Conaway and Wight (1962) .
However, no comparable observations were made in 1966 or any of
the years after 1967.
Histological examination of the ovaries from control rabbits
and dieldrin-treated rabbits failed to reveal any abnormalities
or even any notable differences according to treatment.
Prenatal Mortality
Preimplantation Losses. — A comparison of the number of
corpora lutea with the total number of embryos present (alive or
resorbing) late in gestation provides an index to the proportion
of released ova that failed to implant in the uteri. Appropriate
data are summarized in Table 2 and presented for individual
females in Appendix II, Table A.
In females from the control pens, preimplantation losses of
ova ranged from 0-8.1%. These figures are consistent with
findings of Conaway and Wight (1962) , who stated that in most
cottontail populations, approximately 2-8% of the ovulated ova
are lost before implantation.
Table 2. Preimplantation losses for the second litter of the
year in treated females and controls.
Dieldrin treatment level
No treatment 0.5 2.0
(control) lb/acre lbs/acre
1966
Total number of corpora lutea observed 62 41 34
Number of released ova not
implanting in uteri 1 0 6
Preimplantation loss (percentage) 1.6 0.0 17.6
1967
Total number of corpora lutea observed 13 49 21
Number of released ova not
implanting in uteri 0 3 2
Preimplantation loss (percentage) 0.0 6.1 9.5
1969
Total number of corpora lutea observed 37 49 111
Number of released ova not
implanting in uteri 3 10 19
Preimplantation loss (percentage) 8.1 20.4 17.1
1971
Total number of corpora lutea observed 146 165 112
Number of released ova not
implanting in uteri 9 27 6
Preimplantation loss (percentage) 6.1 16.3 5.3
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In our dieldrin-treated pens (both levels) preimplantation
losses of ova were generally higher than in control pens, and
ranged upward to 20.4% (Table 2). However, there was great
variability, and differences between controls and treated pens
were not significant (P>0.05; chi-square test).
Litter Resorption. — Data from females with partially
resorbed litters are shown in Appendix II, Table A. Table 3
presents a summary of those data.
For partially resorbed litters, a chi-square test showed no
significant differences (P>0.05) in embryo resorption between
rabbits in either of the two dieldrin treatments and the controls
Similarly, the number of females with partially resorbed litters
was not related to the treatment level.
In 1966, two instances of total litter resorption were
noted; both occurred in control females. One female resorbed a
litter of five and the other a litter of undetermined size.
Three additional cases of total litter resorption were
observed in subsequent years . All involved females were from the
pens treated with 0.5 pound/acre of dieldrin; litter sizes were
four and six (1967) and four (1971) .
Embryonic Litter Size
Complete data on numbers of embryos per female are shown in
Appendix II, Table A and summarized in Table 4.
Table 4. Mean embryonic litter sizes for female cottontails in
control and treated pens, 1966-71 (viable embryos only) .
No treatment Dieldrin treatment level
_ (control^ 0.5 lb/acre 2.0 lbs/acre
Year x Sx x Sx x Sx
1966 5.20 + 0.425 5.57 + 0.508 5.40 + 0.601
1967 6.00 + 0.950 5.17 + 0.548 6.33 + 0.776
1969 5.67 + 0.548 5.14 + 0.508 6.57 + 0.359
1971 5.32 + 0.269 4.89 ± 0.254 5.47 ± 0.308
Analysis of variance showed that litter size was not
significantly different (P>0.05) between controls and treated
groups or among years within treatments.
Testes
Testes were removed, fixed in AFA solution and stored for 2
months. After epididymis and connective tissue were removed,
one testis (fixed) from each animal was weighed. Testis weights
are presented in Appendix II, Table A, and are summarized in
Table 5.
Table 5. Mean testis weights in grams for breeding males
(1966-71) .
No treatment
(control)
Dieldrin trea
tment level
0.5 lb/acre
2.0 lbs/acre
Year
x Sx
x Sx
x Sx
1966
9.44 + 0.691
8.63 + 0.691
9.06 + 0.640
1967
10.69 + 1.197
8.25 + 0.000
8.91 + 0.977
1969
9.34 + 0.452
9.59 + 0.535
9.63 + 0.691
1971
9.42 + 0.535
10.20 + 0.510
9.79 + 0.510
""
Analysis of variance comparing testis weights between
treatment levels and between years revealed no significant
differences (P>0.05).
No signs of testis degeneration were evident through
histological examination, and spermatozoa were found in the
seminiferous tubules of all males.
Lactation
We assumed that increased proportions of nonlactating
females in treated pens would reflect increased juvenile
mortality related to dieldrin treatment levels, or possibly some
delay in conceptions. Detailed lactation data are presented in
Appendix II, Table A, and summarized in Table 6.
Table 6. Recovery rates and lactation data for females collected
between 1966 and 1971.
No treatment
(control)
Dieldrin treatment
level
0.5
lb/acre
2.0
lbs/acre
1966
Number of females: Recovered
Lactating
Percentage lactating
12
6
50.0
7
4
57.1
5
2
40.0
1967
Number of females: Recovered
Lactating
Percentage lactating
2
2
100.0
8
7
87.5
4
3
75.0
1969
Number of females: Recovered
Lactating
Percentage lactating
16
13
81.3
14
10
71.4
16
14
87.5
1971
Number of females: Recovered
Lactating
Percentage lactating
29
19
65.5
30
21
70.0
19
11
57.9
No significant differences were found between the percentage
of lactating females in the control pens and those of the two
treatment levels (chi-square test: P >0.05).
Inspection of lactation data and all reproductive parameters
previously considered shows no consistent differences in
reproductive performance between wild-trapped rabbits stocked
annually in the pens, 1966-69, and the rabbits breeding in 1971,
born of captive parents (Tables 1-6) .
Adult Mortality
Mortality estimates of breeding adults in the treated pens
and control pens were obtained for 1966, 1969, and 1971 by a
comparison of the numbers originally stocked with those recovered
at the time of collection (Table 7) . Because of heavy losses to
predation, similar data were not available for 1967 and 1968; in
1970, cottontails were left in the pens as breeders.
Table 7. Adult cottontails recovered in spring from pens stocked
the previous fall.
Dieldrin treatment
level
No treatment 0.5 2.0
(control) lb/acre lbs/acre
1966 F M F M F M
Number of rabbits: Stocked 16 8 16 8 16 8
Recovered 12 6 8 6 5 7
Percentage recovered 75.0 58.3 50.0
1969
Number of rabbits: Stocked 32 16 32 16 32 16
Recovered 19 14 20 10 17 6
Percentage recovered 68.8 62.5 47.9
1971
Number of rabbits: Stocked 48 20 48 20 48 20
Recovered 29 10 31 11 19 11
Percentage recovered 57.4 61.8 44.1
Although fewer rabbits were recovered from the treated pens
than from controls, the difference was not statistically
significant (chi-square test, P> 0.05).
No systematic attempt was made to determine the fate of
individual rabbits in the pens prior to collection. However, in
the dieldrin-treated pens, some mortality was observed which
appeared to be related to the pesticide. Rabbits found dead in
these pens often showed no external injuries, were very
emaciated, and in some instances, contained frothy intestinal
contents. Rabbit mortality was most noticeable soon after
application of dieldrin to the soil.
10
Raptorial birds preyed on some rabbits in most pens, but we
could not determine whether raptors preferentially fed on rabbits
in pens treated with dieldrin.
Chemical Residue Determinations
Dieldrin in Cottontail Tissues . — Residue data for 1966
through 1971 are presented in Appendix II, Table B, and
summarized in Table 8. In 1966 and 1968, residue determinations
were made separately on tissue samples from individual animals.
In the other years, tissue samples from various numbers of
individuals were pooled; numbers of samples comprising the pools
are shown in Table 8 .
In 1966, three separate sets of dieldrin residue analyses
were made. One set consisted of analyses of tissue samples from
individual adult rabbits; this set is alluded to above, and
tallied in Appendix II, Table B. A second set was made on pooled
tissues collected from different combinations of adult animals
recovered at each of the three treatment levels as a guide for
subsequent pooling procedure. The third set consisted of
analyses performed on pooled tissues from the progeny (first
litter of the year) of these adults. The latter two sets were
not considered in the statistical analyses of the data, but are
placed on record in Appendix II, Tables C and D.
Large variances in the data and small sample size
necessitated using the Mann-Whitney U test for statistical
testing. This nonparametric test provides the same function as
the "t" test, but does not require such restrictive assumptions.
Comparisons of dieldrin tissue residue data are made by combining
the sample results from any two groups and ranking these while
still maintaining their individual identity. Differences in the
sums of these ranks are then responsible for the different
significance levels.
In testing the null hypothesis that observations from two
populations are identical, differences between controls and
treated groups are expressed at the following significance
levels :
** - implies a significant difference at the 10% level
* - implies significance at the 25% level and is used
whenever the sample size is so small that 10%
significance cannot be achieved by use of the
tables (from Siegel, 1956) .
In 1967, too few males were collected for the data to be
analyzed statistically (see column n, Table 8) .
11
Table 8. Dieldrin determinations (ppm wet weight) for adult
cottontails in experimental and control pens (1966-71)
No treatment
Dieldrin treatment level
(control)
0.5 lb/acre
2.0
lbs/acre
k
Sample
X
Sx
nt
x Sx
nt
x
Sx
nt
1966+
Females
Brain
0.036
+
0.028
2
0.219 + 0.093
4
**0.420
+
0.078
4
Liver
0.083
+
0.007
2
**4.125 + 1.138
4
**7 .825
+
1.616
4
Muscle
0.01
—
2
**0.054 + 0.018
Males
3
**0.088
+
0.023
4
Brain
0.01
-
2
*0.183 + 0.034
4
*0.390
+
0.104
3
Liver
0.061
+
0.002
2
*5.300 + 1.520
4
*6.350
+
1.333
4
Muscle
0.01
-
2
*0.036 ± 0.003
3
*0.149
+
0.084
4
1967 +
Females
Brain
0.01
-
3(1)
*0.049 + 0.008
9(5)
*0.186
+
0.044
5(3)
Liver
0.049
+
0.0
3(1)
*0.997 + 0.142
6(3)
*5.017
+
1.749
5(3)
Muscle
0.01
—
3(1)
0.013 + 0.004
Males
8(4)
0.052
+
0.030
4(2)
Brain
0.01
-
3(1)
0.069 + 0.0
KD
0.113
+
0.042
3(2)
Liver
0.11
+
0.0
2(1)
No data
0
3.500
+
0.639
3(2)
Muscle
0.01
-
3(1)
0.01
KD
0.022
+
0.003
3(2)
1968 +
Females
Brain
0.01
-
5
**0.262 + 0.101
5
**0.661
+
0.251
7
Liver
0.052
+
0.013
5
**3.026 + 0.841
5
**4.330
+
1.455
7
Muscle
0.011
+
0.002
5
**0.043 + 0.015
Males
5
**0.149
+
0.094
7
Brain
0.01
-
4
**0.110 + 0.0
2
*0.36
+
0.0
1
Liver
0.071
+
0.011
4
**2.725 + 0.885
2
*6.69
+
0.0
1
Muscle
0.01
-
4
**0.112 + 0.019
2
*0.062
+
0.0
1
1969++
Females
Brain
0.005
-
19(8)
**0.094 + 0.012
20(9)
**0.339
+
0.042
17(7)
Liver
0.348
+
0.135
19(8)
**2.619 + 0.433
20(9)
**5.903
+
0.634
17(7)
Muscle
0.005
—
19(8)
**0.027 + 0.004
Males
20(9)
**0.050
+
0.009
17(7)
Brain
0.006
+
0.002
14(6)
*0.148 + 0.024
10(5)
*0.523
+
0.112
6(3)
Liver
0.180
+
0.035
14(6)
*5.100 + 0.634
10(5)
*7.750
+
2 .653
6(3)
Muscle
0.005
-
14(6)
*0.028 + 0.006
10(5)
*0.187
+
0.047
6(3)
1971 ++
Females
Brain
0.005
-
30(7)
**0.104 + 0.010
31(7)
**0.328
+
0.057
19(5)
Liver
0.033
+
0.003
30(7)
**1.474 + 0.153
31(7)
**3.448
+
0.564
19(5)
Muscle
0.005
—
30(7)
**0.020 + 0.003
Males
30(7)
**0.064
+
0.012
19(5)
Brain
0.005
-
9(3)
**0.120 + 0.018
11(3)
**0.375
+
0.068
11(2)
Liver
0.067
+
0.013
9(3)
**3.307 + 0.565
11(3)
**6.185
+
1.172
11(2)
Muscle
0.005
-
9(3)
*0.045 + 0.008
11(3)
0.057
+
0.012
11(2)
+ Sensitivity = 0.01
++ Sensitivity = 0.005
** Significantly diffe
* Significantly diffe
t Individuals; number
ppm (Sx values
ppm one-half
rent from contro
rent from contro
of pooled sampl
involving trace amounts based on
the sensitivity values)
Is (P<0.10; Mann-Whitney U test)
Is (P<0.25; Mann-Whitney U test)
es in parentheses.
12
Residue levels in brain, liver, and muscle tissues of
rabbits from the two dieldrin-treatments were significantly
higher than those of control animals (see Table 8) . A comparison
of brain residue levels by treatment groups also indicated that
accumulation of the pesticide was related to the amount applied
in the pens .
Stickel et al. (1969:197) have shown that the brain is a
useful tissue in appraising the probability of death from
dieldrin poisoning. They cautioned that "...1 p. p.m. in the
brain cannot be regarded lightly, for when brain residues are
that high, body residues are many times as great." Some dieldrin
levels in rabbit brains reported for this study thus strongly
suggest a potential lethal condition for these animals. Three
rabbits found dead in the pens during 1966 had brain residue
levels of 26, 31, and 31 ppm of dieldrin.
Dieldrin in the Soil .--Chemical analyses showed general
agreement between annual application rates of dieldrin and
residue levels in soils, with a minor exception in the samples
collected in November 1969 (Table 9 and Appendix II, Table E) .
Dieldrin persisted in the soil from one annual treatment to
the next. After 1966, residue levels in soils of treated p§m
exceeded amounts applied annually, based on computations
described by Korschgen (1970:189-190). Residue levels in soil
before the fifth treatment provided additional evidence of
persistence (Table 9) .
Variability in the data over the 6-year period precluded
firm conclusions about rates of accumulation of dieldrin in the
soil. This variability may be attributable to: 1) precipitation
causing the mechanical movement of dieldrin into low areas; 2)
nonuniform application of the pesticide because of vegetation;
3) time of year samples were collected; and 4) inconsistency in
the soil collection technique (the 1970 and 1971 collections
were taken at somewhat shallower depths than the intended 3
inches) .
Dieldrin in Plants .--Three plant species in the pens were
collected in June 1970 and analyzed for dieldrin (Table 10) by
the Bureau of Sport Fisheries and Wildlife Fish-Pesticide
Research Laboratory, Columbia, Missouri (see Appendix I for
methodology) . Plants analyzed were among the preferred natural
food sources in the pens (orchard grass, Dactylis glomerata;
broomsedge, Andropogon virginicus; and panic grass, Panicum sp.) .
In the treated pens, all plant samples tested had
measurable amounts of dieldrin. Thus, plant food was one of the
sources of dieldrin accumulation in the rabbits.
13
Table 9. Dieldrin residues in soil in experimental and control
pens .
ppm dieldrin
Rate of dieldrin
recovered
Sx
Range
application
(wet wt.)t
November 1965
Control
0.5 lb/acre
2.0 lbs/acre
+
(before treatment)
0.01
0.01
0.01
May 1966 (after first treatment)
Control 0.01
0.5 lb/acre 0.383
2.0 lbs/acre *0.765
0.112
0.211
0.15 - 0.56
0.25 - 1.22
1967 - No analysis made between second and third treatments
May 1968++ (after third treatment)
Control 0.015
0.5 lb/acre *3.050
2.0 lbs/acre *6.268
0.003
- -
.02
0.668
2.22 -
4.62
1.640
4.50 -
10.10
++
June 1969
Control
0.5 lb/acre
2.0 lbs/acre
(after fourth treatment)
0.005
November 1969
Control
0.5 lb/acre
2.0 lbs/acre
July 1970++ I
Control
0.5 lb/acre
2.0 lbs/acre
April 1971++
Control
0.5 lb/acre
2.0 lbs/acre
++
*2.720
0.878
0.72 -
5.00
*3.750
1.171
2.19 -
7.19
(before fifth treatment)
0,296
0.282
- -
1.14
*2.913
2.247
0.12 -
9.61
*2.408
0.410
1.72 -
3.53
er fifth treatment)
0.005
0.001
— -
0.007
*2.593
0.459
1.78 -
3.91
*8.230
1.471
5.31 -
10.0
(after sixth treatment)
0.005
*2.915
*10.333
0.448
2.845
1.89 - 3.91
5.39 - 17.7
+ Sensitivity = 0.01 ppm.
++ Sensitivity = 0.005 ppm.
t 1968 samples were dried before analyses, resulting in
disproportionately high residue values.
* Significantly different from controls (P<0.10) - "t" test
(Sx values involving trace amounts based on one-half the
sensitivity values.)
14
0.127
0.250
0.028
0.075
0.024
0.139
0.012
0.093
Table 10. Dieldrin content of some selected plant species (ppm) .
No treatment
June 1970 (controls) 0.5 lb/acre 2.0 lbs/acre
Orchard grass (Dactylis) 0.0
(blades)
Orchard grass (Dactylis) 0.004
(seed heads)
Broomsedge (Andropogon) 0.0
(seed heads)
Panic grass (Panicum) 0.009
(blades and stalks)
Stress
Adrenal glands were fixed in 10% formalin at the time of
removal from the rabbits. Gland capsules were then stripped of
extraneous connective tissue and weighed .
One adrenal from each rabbit was sectioned at 20 microns
with a freezing microtome, collected in water, and stained with
oil-red-0 lipid specific stain according to the method described
by Fickess (1963) . Following microscopic examination of the
sections, adrenals were classified according to content and
distribution of cortical lipid material as described by Fickess
(1963) . This classification system has six types of lipid
distribution in adrenals, which can be related to stress. In our
study, no differences in lipid distribution were noted in adrenals
from control rabbits compared with those of the dieldrin-treated
pens .
Mean paired adrenal weight (mg) :body weight (g) ratios and
mean spleen weight (mg) :body weight (g) ratios were also used to
determine if any major physiologic responses were apparent as a
result of the dieldrin treatments. We assume that if the
pesticide had acted as a constant source of stress, some
deviation in these ratios would be observed . This response
would be in accord with the rationale of Selye's General
Adaptation Syndrome (Selye, 1946) , in which thymo- lymphatic
atrophy and adrenal cortical hypertrophy are recognized as two of
the first responses observed in animals under stress.
Both adrenal and spleen weight :body weight ratios differed
by sex, year, and treatment, but differences showed no
consistent patterns (Tables 11 and 12) . Thus, these ratios
provide no indication of differential physiological stress as a
result of treatment.
15
Table 11. Mean adrenal weioht (mg) :body weight (g) ratios of
adult cottontails treated with dieldrin and of controls
(1966-71) .
No treatment
(control)
Dieldrin treatment
level
0.5
lb/acre
2.0 lbs/acre
X
Sx
n
X
Sx
n
X
Sx
n
1966
Females
0.20
0.015
12
0.18
0.021
6
0.16
0.023
5
Males
0.18
0.025
4
0.20
0.021
6
0.22
0.019
7
1967
Females
0.13
0.029
3
0.14
0.018
8
0.15
0.021
6
Males
0.20
0.029
3
0.17
-
1
0.16
0.029
3
1968
Females
0.35
0.025
4
0.22
0.025
4
0.24
0.234
5
Males
0.37
0.025
4
0.30
0.036
2
0.37
-
1
1969
Females
0.15
0.013
15
0.15
0.012
17
0.16
0.013
16
Males
0.21
0.015
12
0.18
0.016
10
0.20
0.021
6
1971
Females
0.11
0.012
18
0.12
0.012
19
0.13
0.019
7
Males
0.18
0.016
10
0.16
0.019
7
0.17
0.036
2
Table 12. Mean spleen weight (mg) :body weight (g) ratios of
adult cottontails treated with dieldrin and of controls
(1966-71) .
1 ' " '
No treatment
(control)
x Sx n
Dieldrin
treatment
level
0.5
X
lb/acre
Sx
n
2.0 It
X
is/acre
Sx
n
1966
Females
Males
0.29
0.54
0.160
0.277
12
4
0.28
0.41
0.209
0.209
7
7
0.32
0.26
0.248
0.209
5
7
1967
Females
Males
0.83
1.46
0.320
0.320
3
3
0.47
1.28
0.196
8
1
0.90
0.75
0.248
0.320
5
3
1968
Females
Males
1.11
1.23
0.277
0.277
4
4
0.70
1.29
0.320
0.392
3
2
0.79
1.21
0.248
5
1
1969
Females
Males
1.09
1.38
0.134
0.154
17
13
1.15
1.02
0.124
0.175
20
10
1.18
0.56
0.134
0.226
17
6
1971
Females
Males
0.55
0.75
0.109
0.161
26
10
0.32
0.40
0.105
0.185
28
9
0.45
0.44
0.127
0.167
19
11
16
It should be noted that density of cottontails may affect
adrenal and spleen weight :body weight ratios (Conaway and Wight,
1962) . In our experiments, the stocking rates were equal in all
pens each year. Recovery rates for rabbits at the end of the
breeding seasons were generally higher in the control than in the
experimental pens, but these differences were not statistically
significant (see Table 7).
From the available data, we doubt that density affected the
measures of stress that we used; however, we cannot completely
rule out this possibility.
CONCLUSIONS AND DISCUSSION
The following principal points emerged from this study:
(1) Dieldrin behavior in soil — Dieldrin levels in
soil samples taken a few months after application
generally reflected the application levels. Dieldrin
persisted from 1 year to the next in the soils of the
pens treated annually. However, variable residue
readings, attributable at least in part to experimental
procedure, permitted no assessment of long-term accumuation
of dieldrin in the treated pens. Annual carryover in
the soil of organochlorine pesticides, including aldrin
and dieldrin, has been demonstrated in other studies
(reviewed by Korschgen, 1970) . Persistence over
periods of a few years has also been demonstrated
previously, as has been the perplexing variability in
soil residue levels long after application of dieldrin
(see Caro and Taylor, 1971) .
(2) Dieldrin residues in cottontail tissues —
Residue levels in brain, liver, and muscle tissues of
rabbits from pens subjected to dieldrin treatment were
significantly higher than those of control animals.
Tissue residue levels reflected residue levels in the
soils of the treated pens.
(3) Mortality of adults — At the end of each year's
experiment, lower percentages of stocked cottontails
were recovered from the pens treated with dieldrin than
from the control pens. These differences were not
statistically significant (P > 0.05), but they may have
been real: three animals found dead in treated pens had
lethal brain residue levels, and a few others found
dead showed some symptoms of dieldrin poisoning.
(4) Reproductive performance — No major differences
were apparent in the reproductive performance of either
female or male cottontails according to treatment.
17
(However, the data for females pertained only to second
pregnancies; it is possible that effects would have been
detected in subsequent litters following longer exposure.)
These findings are concordant with other studies of the
effects of dieldrin on mammals. For example, Murphy
and Korschgen (1970) studied effects on reproduction in
white-tailed deer (Odocoileus virginianus) fed 0, 5, and
25 ppm dieldrin. They found no consistent differences
in conception rates and in mortality in utero among
treatment groups. Fertility of male progeny was not
affected. However, they showed a greater postpartum
mortality of fawns from dieldrin-treated does. In the
present study, there were no consistent differences in
reproductive performance between wild-trapped rabbits
stocked annually in the pens, 1966-69, and the rabbits
breeding in 1971, born of captive parents.
Several studies besides that of Murphy and Korschgen (1970)
have shown increased postnatal mortality of mammals born to
females treated with organochlorines . For example, Morris (1968)
studied the effects of feeding endrin (0-7 ppm) on survival and
reproduction in the deer mouse (Peromyscus maniculatus) .
Frequency of litter production and mean litter size were similar
for each group before and during experimental feeding. Increased
postnatal mortality before weaning was observed among the treated
animals. He concluded that the postnatal period may be the
crucial one for survival of young mammals subjected to
pesticides .
Harr et al. (1970) reported reproductive data for 220
female Wistar rats fed a semipurified ration to which dieldrin
was added. The maximal dietary exposure level of dieldrin
consistent with reproductive values of normal rats was 0.24 ppm
(0.014 ug/g of body weight per day) . Exposure levels in excess
of 0.24 ppm resulted in a lowered percentage of females that
conceived, an increased concentration of dieldrin in the stomach
milk curd of pups as compared with the ration fed the dam, and
death of nursing pups.
In the present study, there was no adequate measure of
postnatal mortality. Thus, a possibility remains that dieldrin
application suppressed productivity of the cottontails, even
though reproductive rates themselves, at least during second
pregnancies, were apparently not affected.
ACKNOWLEDGMENTS
The authors acknowledge the valuable advice and assistance
of Clinton H. Conaway, Director, Caribbean Primate Research
Center, Puerto Rico, whose effort was considerable in the early
phases of this study. We appreciate the efforts of Frank Sapp
18
and Charles Shaiffer, managers of the research area on which the
study was conducted. We are grateful to the graduate students
who gave their time .
We are indebted to Nicholas R. Holler, Jerry R. Longcore,
and James R. Palmer, Bureau of Sport Fisheries and Wildlife,
Washington, D. C, for editorial assistance and criticism. E.
H. Dustman, Lucille F. Stickel, and William H. Stickel,
Patuxent Wildlife Research Center, U. S. Bureau of Sport
Fisheries and Wildlife, provided valued advice throughout the
study. Sandra Clark deserves special thanks for manuscript work.
This paper is a contribution from the Missouri Cooperative
Wildlife Research Unit: U. S. Bureau of Sport Fisheries and
Wildlife, Missouri Department of Conservation, Wildlife
Management Institute, and University of Missouri-Columbia
cooperating. Support was provided to Richard Malecki through an
Edward K. Love Fellowship and to John Elliston through a Paul K.
Wehmiller Fellowship. All research was supported by research
contract number USDI 17-14-0008-703 with the U. S. Bureau of
Sport Fisheries and Wildlife, Patuxent Wildlife Research Center,
Laurel, Maryland.
19
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domestic fowl. Auk, vol. 79, p. 104-107.
Brambell, F. W. R., and I. H. Mills. 1948. Studies on sterility
and prenatal mortality in wild rabbits. Journal of
Experimental Biology, vol. 25, p. 241-269.
Caro, J. H., and A. W. Taylor. 1971. Pathways of loss of
dieldrin from soils under field conditions. Journal of
Agricultural and Food Chemistry, vol. 19, p. 379-384.
Conaway, C. H., and H. M. Wight. 1962. Onset of reproductive
season and first pregnancy of the season in cottontails.
Journal of Wildlife Management, vol. 26, p. 278-290.
, , and K. C. Sadler. 1963. Annual
production by a cottontail population. Journal of Wildlife
Management, vol. 27, p. 171-175.
di Fiore, M. S. H. 1961. An atlas of human histology. Lea
and Febiger, Philadelphia. 224 p.
Fickess, D. R. 1963. Seasonal sudanophilic variation in the
cottontail (Sylvilagus floridanus) adrenal cortex. Ph.D.
Thesis, University of Missouri, Columbia. 106 p.
Harr, J. R., R. R. Claeys, J. F. Bone, and T. W. McCoveie . 1970.
Dieldrin toxicosis: rat reproduction. American Journal of
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Hart, M. M., R. H. Adamson, and S. Fabro . 1971. Prematurity
and intrauterine growth retardation induced by DDT in the
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Haugen, A. O. 1942. Life history studies of the cottontail
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Korschgen, L. J. 1970. Soil- food-chain-pesticide wildlife
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Wildlife Management, vol. 34, p. 186-199.
Marsden, H. M., and C. H. Conaway. 1963. Behavior and the
reproductive cycle in the cottontail. Journal of Wildlife
Management, vol. 27, p. 161-170.
Maximow, A. A., and W. Bloom. 1957. A textbook of histology.
W. B. Saunders Company, Philadelphia. 628 p.
20
Morris, R. D. 1968. Effects of endrin feeding on survival and
reproduction in the deer mouse (Peromyscus maniculatus) .
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Murphy, D. A., and L. J. Korschgen. 1970. Reproduction, growth,
and tissue residues of deer fed dieldrin. Journal of
Wildlife Management, vol. 34, p. 887-903.
Peakall, D. B. 1967. Pesticide-induced enzyme breakdown of
steroids in birds. Nature, vol. 216, p. 505-506.
Sadler, K. C, and C. H. Conaway. 1971. Cold temperatures,
snow and ice as reproductive inhibitors in cottontail
rabbits. In Proceedings of the Snow and Ice in Relation to
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Press, Ames, p. 197-202.
Scott, T. G., Y. L. Willis, and J. A. Ellis. 1959. Some effects
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21
APPENDIX I
ANALYTICAL METHODOLOGY
Rabbit Tissue
Analyses for dieldrin were made at the WARF Institute, Inc.,
Madison, Wisconsin. All samples were stored frozen until time
for analysis.
Tissues analyzed included brain, muscle, liver, testes, and
fat. Samples from individual animals weighed approximately 5-10
grams, except for fat, which was 2-4 grams. Fat samples were
taken from the supra-scapular region of the body; muscle samples
were from the thigh. In some years, tissue samples from more
than one animal from the same pen were combined and homogenized
before analysis. Samples were then proportionately larger. The
numbers of individuals represented in each sample are shown in
the tables in Appendix II.
Samples were dried to constant weight in a 40 C oven for
72-96 hours, then ground with sodium sulfate and extracted with a
mixture of ethyl and petroleum ether (70 ml: 170 ml) for 8 hours
in a Soxhlet apparatus. The extract was cleaned and separated
into two fractions by elution through a florisil column with
mixtures of ethyl and petroleum ether (5:95 and 15:85). Analysis
was by electron capture gas chromatography on a Barber-Coleman
Pesticide Analyzer Model 5360. Instrument conditions were:
Column, 1.2 m x 4 mm glass, packed with 5% DC-200 on 80/100 mesh
Gas Chrom Q? injector temperature 230 C, column 200 C, and
detector 240 C; carrier gas, nitrogen; flow such that dieldrin
had a retention time of 4-5 minutes.
No corrections were made for recovery, which was 85% or
better. Lipids were determined on an aliquot of the extract
reduced to dryness on a steambath and placed in a 40 C oven for
204 hours.
Soil
Analyses for dieldrin were made at the WARF Institute, Inc.,
Madison, Wisconsin. Samples were stored frozen until analysis.
The soil sample (approximately 800 grams) was passed through
a mesh screen to remove stones and other foreign materials. A
20-gram portion was taken for analysis. The sample was extracted
in a 1-quart Waring Blender with 200 ml acetonitrile, filtered
through glass wool into a separatory funnel containing 600 ml of
tap water, partitioned from acetonitrile into petroleum ether,
dried with sodium sulfate, and passed through a florisil column
as described for rabbit tissue. Subsequent steps and instrument
conditions are also as described for rabbit tissue.
22
Soil moisture was determined for a separate 10-gram aliquot
by heating in a vacuum oven at 100 C for 5 hours, then reweighing
for moisture calculation.
Organic matter was measured in the same sample used for
moisture determination; the dry sample was heated in a muffle
furnace at 500 C for 4 hours, then reweighed for organic matter
calculation.
pH was determined for a separate 5-gram sample and read to
the nearest 0.1 pH unit on a Beckman Zeromatic II pH meter.
Plant Tissue
Analyses for dieldrin were made at the Bureau of Sport
Fisheries and Wildlife, Fish-Pesticide Research Laboratory,
Columbia, Missouri. Tissues analyzed included seed heads, blades,
or blades plus stalks. All samples were stored frozen until
time for analysis.
Two-gram samples were ground and dried with anhydrous sodium
sulfate; extracted in a 1 cm ID glass column, with reservoir, with
100 ml of 5% diethyl ether in hexane; cleaned by eluting with 75
ml of diethyl ether and petroleum ether (5:95) through a 1 cm ID
florisil column topped with sodium sulfate. Analysis was by
electron capture gas chromatography on a Packard 804. Instrument
conditions were: Column, 1.8 m x 2 mm, glass, packed with 0.3%
OV-7 on 80/100 mesh glass beads; temperature was 180 C; carrier
gas, nitrogen; flow 30 ml per min .
23
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60
Table E. Dieldrin residues (ppm) in the soil from 1965 through
1971. (Sx values involving trace amounts are based on
one-half the sensitivity values.)
Control
(no treatment)
0.5 lb/acre
Dieldrin treatment
2.0 lbs/acfi~
November 1965
<0.
,01
May.
1966+
<0.01
<0.
.01
<0.
,01
<0,
,01
x =
<0.
,01
May
1968 +
<0.01
0,
,019
0,
.018
0,
.012
x =
0,
.015 + i
June 1969+
<0,
.005
<0
.005
<0,
.005
<0,
.005
x =
<0
.005
November 1969
<0
.005
1
.14
0
.034
0
.006
x =
0
.296 +
July 1970++
0.007
0
.005
<0
.005
<0
.005
x =
0
.005 +
April !
L971++
<0
.005
<0
.005
<0
.005
<0
.005
<0.01
0.15
0.56
0.23
0.23
x = 0.383
2.22
2.39
4.62
2.97
+ 0.112
<0.01
0.25
0.97
1.22
0.62
x= 0.765 + 0.211
4.50
4.81
5.66
10.10
0.003
x = 3.050 + 0.668
0.72
2.50
2.66
5.00
x = 6.268 + 1.640
2.19
2.34
7.19
3.28
++
0.282
0.001
x = 2.720 + 0.878
9.61
1.34
0.12
0.58
x = 2.913 + 2.247
1.78
2.34
3.91
2.34
x = 2.593 + 0.459
x = 3.750 + 1.171
3.53
1.72
2.50
1.88
x = <0.005
3.91
1.89
3.36
2.50
x = 2.915 + 0.448
x = 2.408 + 0.410
5.31
9.38
10.0
x = 8.230 + 1.471
5.39
17.7
6.34
11.9
x =10.333 + 2.845
+ Sensitivity = 0.01 ppm.
++ Sensitivity = 0.005 ppm.
61
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