Reproductive biology of the wild red brocket deer (Mazama americana) female in the Peruvian Amazon

Abstract

Knowledge of the reproductive biology is critical for the development of management strategies of the species both in captivity and in the wild, and to address conservation concerns regarding the sustainable use of a species. The present report characterizes some aspects of the reproductive biology of the wild red brocket deer inhabiting the North-eastern Peruvian Amazon region, based on the anatomical and histological examination of the female reproductive organs of 89 wild adult females in different reproductive states. The red brocket deer female presented ovarian follicular waves involving the synchronous growth of a cohort of an average 25 follicles but only one follicle generally survived and continued development, reaching maturity at 4mm. Mean ovulation rate was 1.14 and litter size was 1 fetus. Females presented a low rate of reproductive wastage of 14.3% of embryos. Among the 89 adult females studied, 41 (46.1%) were pregnant and 48 (53.9%) were non-pregnant females. In the Northeastern Peruvian Amazon, conceptions occurred year-round in the red brocket deer but there were peaks in the rate of conception. Estimated yearly reproductive production was 0.76-0.82 young per adult female. Most pregnant females in advanced stage of pregnancy had at least one active CL, suggesting the persistence of CL throughout gestation.

Full text

Animal
Reproduction
Science
128 (2011) 123–
128
Contents
lists
available
at
SciVerse
ScienceDirect
Animal
Reproduction
Science
journal
homepage:
www.elsevier.com/locate/anireprosci
Reproductive
biology
of
the
wild
red
brocket
deer
(Mazama
americana)
female
in
the
Peruvian
Amazon
P.
Mayora,∗,
R.E.
Bodmerb,
M.
López-Béjara,
C.
López-Planaa
aDepartment
of
Animal
Health
and
Anatomy,
Faculty
of
Veterinary,
Universitat
Autònoma
de
Barcelona,
Bellaterra,
E-08193
Barcelona,
Spain
bDurrell
Institute
of
Conservation
and
Ecology,
University
of
Kent,
Canterbury,
Kent
CT2
7NS,
UK
a
r
t
i
c
l
e
i
n
f
o
Article
history:
Received
15
April
2011
Received
in
revised
form
15
September
2011
Accepted
18
September
2011
Available online 25 September 2011
Keywords:
Red
brocket
deer
Mazama
Americana
Reproduction
Female
reproductive
organs
a
b
s
t
r
a
c
t
Knowledge
of
the
reproductive
biology
is
critical
for
the
development
of
management
strategies
of
the
species
both
in
captivity
and
in
the
wild,
and
to
address
conservation
concerns
regarding
the
sustainable
use
of
a
species.
The
present
report
characterizes
some
aspects
of
the
reproductive
biology
of
the
wild
red
brocket
deer
inhabiting
the
North-
eastern
Peruvian
Amazon
region,
based
on
the
anatomical
and
histological
examination
of
the
female
reproductive
organs
of
89
wild
adult
females
in
different
reproductive
states.
The
red
brocket
deer
female
presented
ovarian
follicular
waves
involving
the
synchronous
growth
of
a
cohort
of
an
average
25
follicles
but
only
one
follicle
generally
survived
and
con-
tinued
development,
reaching
maturity
at
4
mm.
Mean
ovulation
rate
was
1.14
and
litter
size
was
1
fetus.
Females
presented
a
low
rate
of
reproductive
wastage
of
14.3%
of
embryos.
Among
the
89
adult
females
studied,
41
(46.1%)
were
pregnant
and
48
(53.9%)
were
non-
pregnant
females.
In
the
Northeastern
Peruvian
Amazon,
conceptions
occurred
year-round
in
the
red
brocket
deer
but
there
were
peaks
in
the
rate
of
conception.
Estimated
yearly
reproductive
production
was
0.76–0.82
young
per
adult
female.
Most
pregnant
females
in
advanced
stage
of
pregnancy
had
at
least
one
active
CL,
suggesting
the
persistence
of
CL
throughout
gestation.
© 2011 Elsevier B.V. All rights reserved.
1.
Introduction
In
the
Amazon
region,
wildlife
subsistence
hunting
has
been
a
traditional
source
of
food,
animal
skins,
and
other
essential
items
for
local
people
(FitzGibbon,
1998).
Hunt-
ing,
however,
may
lead
to
a
situation
in
which
mammalian
species
in
forested
habitats
become
locally
or
even
widely
extinct
(Redford,
1993).
The
red
brocket
deer
(Mazama
americana)
is
one
of
the
most
frequently
hunted
species
in
the
Amazon
region,
representing
an
important
source
of
meat
for
local
human
populations
(Puertas
and
Bodmer,
2004).
∗Corresponding
author.
Tel.:
+34
3
581
2482;
fax:
+34
3
581
2006.
E-mail
address:
mayorpedro@hotmail.com
(P.
Mayor).
The
red
brocket
deer
is
a
medium-sized
artiodactyl,
weighing
between
20
and
30
kg
at
maturity
(Emmons,
1997).
The
species
has
a
wide
distribution,
ranging
from
southern
Mexico
to
Amazonia
and
the
Chaco,
and
through
eastern
Paraguay
to
northern
Argentina
(Redford
and
Eisenberg,
1992).
In
the
Amazon
region,
the
female
red
brocket
deer
is
considered
to
be
non-seasonal
polyestric,
apparently
breeding
year-round
(Hurtado-Gonzales
and
Bodmer,
2006),
but
exhibits
clear
peaks
of
conceptions
and
births
(Branan
and
Marchinton,
1987;
Bisbal,
1994).
This
species
has
a
mean
gestation
length
of
210
days
(Muller
and
Duarte,
1992)
and
litter
size
is
usually
one,
but
occa-
sionally
twins
may
occur
(Redford
and
Eisenberg,
1992;
Hurtado-Gonzales
and
Bodmer,
2006).
Reproductive
information
is
critical
for
the
develop-
ment
of
management
strategies
of
species
both
in
captivity
and
in
the
wild,
and
to
address
conservation
concerns
0378-4320/$
–
see
front
matter ©
2011 Elsevier B.V. All rights reserved.
doi:10.1016/j.anireprosci.2011.09.009

124 P.
Mayor
et
al.
/
Animal
Reproduction
Science
128 (2011) 123–
128
regarding
the
sustainable
use
of
any
species
(Bodmer
and
Robinson,
2004).
Therefore,
it
is
necessary
to
further
inves-
tigate
the
biological
performance
to
be
able
to
estimate
the
vulnerability
of
species
to
support
different
hunting
pres-
sures
in
the
Amazon.
Species
differences
in
reproductive
form
and
function
limit
the
practical
applicability
for
off-
spring
production.
One
of
the
limiting
factors
is
the
lack
of
basic
knowledge
about
thousands
of
unstudied
species
(Pukazhenthi
and
Wildt,
2004).
To
the
best
of
our
knowl-
edge,
the
reproductive
biology
of
the
red
brocket
deer
is
still
largely
unknown.
The
present
report
characterizes
some
aspects
of
the
reproductive
biology
of
the
red
brocket
deer
in
the
North-eastern
Peruvian
Amazon.
2.
Materials
and
methods
2.1.
Study
area
This
study
was
conducted
in
the
Tamshiyacu–Tahuayo
Communal
Reserve
and
on
the
Yavarí-Mirí
river,
in
the
Northeastern
Peruvian
Amazon.
The
reserve
spans
322,500
ha
of
continuous
forest,
predominantly
non-
flooded
terra
firme
forest,
with
a
harvest
of
between
1.1
and
2.7
mammals
km−2year−1.
The
climate
in
the
region
is
typ-
ically
equatorial
with
an
annual
temperature
of
22–36 ◦C,
a
relative
humidity
range
from
80%
to
100%,
and
a
rain-
fall
range
from
1500
to
3000
mm.
Seasons
are
defined
as
dry
(January–February
and
July–September)
and
wet
(March–June
and
October–December).
2.2.
Animal
collection
From
2003
to
2008,
hunters
living
in
the
study
area
collected
reproductive
organs
from
89
adult
red
brocket
deer
females,
as
part
of
an
ongoing
participatory
conserva-
tion
program
that
involves
local
hunters
in
implementing
a
community-based
wildlife
management
program.
This
methodology
assured
the
absence
of
any
cruelty
towards
the
experimental
animals.
2.3.
Reproductive
state
of
females
The
reproductive
organs
were
maintained
in
buffered
4%
formaldehyde
solution
(v/v),
and
were
stored
at
the
Museo
de
Zoologia
de
la
Universidad
Nacional
de
la
Ama-
zonía
Peruana
(UNAP)
until
analyzed.
Samples
of
the
ovaries,
uterine
tubes,
uterus
and
vagina
were
dehydrated,
embedded
in
paraffin
wax,
cut
into
3-␮m
sections,
stained
with
haematoxylin
and
eosin,
and
PAS-haematoxylin,
and
examined
under
a
light
microscope.The
reproductive
organs
were
examined
for
the
evidence
of
embryos
or
fetuses.
Females
with
at
least
one
embryo
or
fetus
were
considered
to
be
pregnant,
and
the
pregnancy
stage
was
defined
as
embryonic
or
fetal
(International
Committee
on
Veterinary
Embryological
Nomenclature,
1994).
According
to
the
embryo
or
fetal
length,
pregnant
females
were
clas-
sified
as
in
early
(0–15
cm),
mid
(15–30
cm)
and
advanced
(30–45
cm)
stages
of
pregnancy.
Non-pregnant
adult
ani-
mals
with
ovaries
containing
active
corpora
lutea
(CL)
were
described
as
being
in
the
luteal
phase
of
the
estrous
cycle,
while
females
with
ovaries
bearing
large
antral
follicles
and
lacking
CL
were
considered
to
be
in
the
follicular
phase
of
the
estrous
cycle.
In
the
absence
of
either
large
antral
folli-
cles
or
CL,
the
ovaries
were
considered
inactive.
Due
to
the
anatomical
and
histological
similarities
between
females
in
the
luteal
phase
and
pregnant
females
in
the
first
two
weeks
of
pregnancy,
10%
of
females
diagnosed
as
non-
pregnant
females
in
the
luteal
phase
may
actually
have
been
pregnant
(Mayor
et
al.,
2010).
2.4.
Reproductive
performance
Monthly
conceptions
were
determined
by
back-dating
embryos
or
fetuses
from
the
estimated
age
on
the
date
when
each
red
brocket
deer
females
was
collected.
Gesta-
tion
length
used
to
back-date
fetuses
was
210
days
(Muller
and
Duarte,
1992).
Since
there
is
no
characterization
of
fetal
development
in
the
red
brocket
deer,
the
determination
of
embryo/fetal
age
was
based
primarily
on
the
sheep
fetal
description
given
by
Noden
and
de
Lahunta
(1985).
Litter
size
and
fetal
sex
of
each
pregnancy
were
recorded.
Reproduction
performance
of
the
wild
red
brocket
deer
was
estimated
as
follows
(Mayor
et
al.,
2010):
Ovu-
lation
rate
=
Number
of
CL/ovulating
female,
Fertilization
rate
=
total
embryos
or
fetuses/number
of
CL
in
pregnant
females,
Reproductive
wastage
=
number
of
CL
−
number
of
embryos
or
fetuses
in
pregnant
females,
Pregnancy
rate
=
number
of
pregnant
females/total
adult
females,
Pregnancy-days
per
year
=
365
days/year
×
pregnancy
rate,
Number
of
births
per
female
per
year
=
yearly
pregnancy-
days/gestation
length,
Farrowing
interval
=
gestation
length/pregnancy
rate,
Parturition–conception
inter-
val
=
farrowing
interval
−
gestation
length,
Yearly
reproductive
production
=
number
of
births
per
female
per
year
×
litter
size,
Gross
productivity
=
number
of
embryos
or
fetuses/number
of
adult
females,
and
Gross
fecundity
=
number
of
female
fetuses/number
of
adult
females.
2.5.
Macroscopic
and
microscopic
analyses
Based
on
the
macroscopic
and
microscopic
study
of
reproductive
organs
of
51
red
brocket
deer
females,
we
studied
the
functional
anatomy
of
the
species.
Ovarian
sizes
(r1,
r2and
r3)
were
calculated
and
the
volume
estimated
by
means
of
the
formula
for
the
vol-
ume
of
ovoid
bodies:
V
=
4/3(r1r2r3).
Ovarian
follicles
were
classified
using
the
optical
plane
through
which
the
oocyte
nucleolus
was
visible,
according
to
a
modified
clas-
sification
of
Mayor
et
al.
(2006).
Morphometric
features
of
primordial,
primary,
small
pre-antral,
large
pre-antral,
small
antral
and
large
antral
follicles
were
recorded.
The
classification
of
luteal
tissue
was
used
to
classify
corpora
lutea
(Mayor
et
al.,
2006).
Ovarian
corpora
lutea
were
considered
active
after
a
pregnancy
was
established
or
as
indicated
by
luteal
cell
morphology.
Depending
on
the
diameter,
viability
of
luteal
cells
and
the
presence
or
absence
of
an
oocyte,
corpora
lutea
were
classified
as:
true
corpora
lutea,
differentiated
as
cyclic
or
pregnancy
CL,
and
atretic
CL.
Measurements
of
ovarian
structures
were
taken
using
a
micrometric
ocular.
Diameters
were
measured
as
the

P.
Mayor
et
al.
/
Animal
Reproduction
Science
128 (2011) 123–
128 125
mean
length
of
the
2
maximum
perpendicular
axes.
Luteal
volumes
were
calculated
using
the
formula:
V
=
4/3(D/2)3.
Luteal
volume
per
female
was
calculated
as
the
sum
of
volumes
from
active
luteal
structures.
Recorded
ovarian
variables
were
number
and
type
of
antral
follicles,
number
and
type
of
CL,
luteal
volume,
and
size
of
luteal
cells.
2.6.
Statistical
analysis
To
test
the
hypothesis
of
seasonal
reproduction,
we
used
the
number
of
parturitions
per
season
and
tested
this
using
a
chi-square
test.
The
vulnerability
to
hunting
of
females
at
different
stages
of
pregnancy
and
of
adults
of
each
sex
was
also
analyzed
using
a
chi-square
test.
Statistical
analyses
were
performed
using
GraphPad
Instat
(version
3.01
for
Windows
95,
GraphPad
Software
Inc.,
San
Diego,
CA,
USA:
www.graphpad.com).
Differences
with
a
probability
value
of
0.05
or
less
were
considered
significant.
All
values
are
expressed
as
the
mean
±
standard
deviation
(SD).
3.
Results
3.1.
Reproductive
performance
Among
the
89
adult
females
studied,
41
(46.1%)
were
pregnant
and
48
(53.9%)
were
non-pregnant
females.
Table
1
shows
the
estimated
reproductive
performance
of
the
red
brocket
deer
in
the
study
area.
Non-pregnant
females
included
17
(35.4%)
females
in
the
follicular
phase
and
31
(64.6%)
females
in
the
luteal
phase.
Considering
that
the
10%
of
females
diagnosed
as
non-pregnant
females
in
the
luteal
phase
may
actually
have
been
pregnant,
3
females
in
the
luteal
phase
could
be
considered
as
preg-
nant
females
in
the
earliest
pregnancy
stage.
Therefore,
the
pregnancy
rate
could
be
as
high
as
49.4%
(44
pregnant
females).
Fig.
1
shows
the
monthly
pregnancy
rate
and
the
yearly
distribution
of
conceptions
of
the
red
brocket
deer
in
the
study
area.
Pregnancies
were
observed
in
all
months
of
the
year,
except
in
July
and
August,
and
peaks
of
conceptions
were
observed
in
May,
September
and
December.
Nonethe-
less,
conception
rates
did
not
differ
between
the
wet
and
the
dry
season
(69.4%
and
33%,
respectively;
P
=
0.10).
Table
1
Reproductive
performance
of
wild
red
brocket
deer
(n
=
89)
in
the
North-
eastern
Peruvian
Amazon
from
2003
to
2008.
Reproductive
parameters
Value
Number
of
females
89
Number
of
non-pregnant
females 48–45
Number
of
pregnant
females 41–44
Number
of
fetuses 48
Pregnancy
rate
(%)
46.1–49.4
Pregnant
days/year
(days)
168–180
Non-pregnant
days/year
(days)
197–185
Parturitions/year/female 0.76–0.82
Farrowing
interval
(days) 477–445
Parturition–conception
interval
(days)
257–225
Litter
size
(youngs/parturition)
1.00
Fetal
sexual
ratio
(F/M) 20:17
Yearly
reproductive
production
(youngs/year/pregnant
female)
0.76–0.82
Gross
productivity
(youngs/year/adult
female)
0.46–0.49
Gross
fecundity
(female
youngs/year/female)
0.25–0.27
Mean
ovulation
rate
was
1.14
±
0.38
CL/female
(ranging
from
1
to
2
CL/female,
in
the
85.4%
and
15.6%
of
females,
respectively).
All
pregnant
females
had
one
embryo
or
fetus,
with
a
fetal
sex
ratio
of
54.0%
females
and
46.0%
males,
which
did
not
differ
from
a
1:1
sex
ratio
(P
=
0.65).
Red
brocket
deer
females
presented
a
fertilization
rate
of
81.9%,
and
a
mean
ovum
mortality
of
0.14
±
0.39
(14.3%)
oocytes
or
embryos
per
pregnancy.
There
were
no
signif-
icant
differences
in
hunted
pregnant
females
according
to
the
pregnancy
stage
(P
=
0.28)
or
adult
sex
(P
=
0.42).
3.2.
Functional
anatomy
Mean
ovarian
volume
was
not
significantly
different
in
morphometric
measures
with
varying
reproductive
stages
of
females
(non-pregnant
females
in
the
follicular
phase,
0.24
±
0.12
cm3;
non-pregnant
females
in
the
luteal
phase,
0.35
±
0.15
cm3;
pregnant
females,
0.38
±
0.37
cm3).
There
were
not
differences
in
ovarian
morphometric
measures
according
the
side
of
the
ovary.
In
the
ovary,
growing
folli-
cles
or
CL
were
not
externally
discernible.
Fig.
2
shows
the
follicular
distribution
of
antral
folli-
cles
per
female
according
to
the
reproductive
state
of
the
female.
Ovarian
follicles
were
observed
in
both
pregnant
Fig.
1.
Monthly
pregnancy
rate
and
yearly
distribution
of
conceptions
(by
percentage)
of
wild
red
brocket
deer
(n
=
45)
in
the
Northeastern
Peruvian
Amazon
from
2003
to
2008.
Number
of
pregnant
females
per
month
is
shown
in
brackets.

126 P.
Mayor
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/
Animal
Reproduction
Science
128 (2011) 123–
128
0
5
10
15
20
25
>3.0 mm2.5-3.0 mm2.0-2.5 mm1.5-2.0 mm1.0-1.5 mm0.5-1.0 mm0.0-0.5 mm
Folicular females
Luteal females Pregnant females
a,b,c Values appearing in rows with different superscripts are significantly different
(P<0.05).
Diameter of antral follicles (mm)
Number of
antral
follicles
a
b
b
a bc a a b
Fig.
2.
Average
distribution
of
antral
follicles
according
to
the
follicle
diameter
and
the
reproductive
state
of
the
red
brocket
deer
female
(n
=
51).
Table
2
Follicular
characterization
according
to
the
reproductive
state
of
the
female
brocket
deer
(n
=
51).
Reproductive
status
n
Number
of
antral
follicles
per
female
Number
of
large
antral
follicles
>2
mm
Average
largest
antral-follicle
diameter
(mm)
Largest
antral
follicle
diameter
(mm)
Non-pregnant
females
in
follicular
phase
241
24.7
±
13.7a
1.40
±
0.55a
3.05
±
0.57a
3.90
Non-pregnant
females
in
luteal
phase
157
13.9
±
6.6b
0.73
±
0.79ab
2.21
±
0.81b
3.07
Pregnant
females 565 18.2 ±
12.3c
0.47
±
0.68c
1.89
±
0.72c
3.47
Values
appearing
in
rows
with
different
letters
(a,b,c)
are
significantly
different
(P
<
0.05).
and
non-pregnant
red
brocket
deer
females.
The
small-
est
and
the
largest
antral
follicles
observed
presented
a
diameter
of
0.21
and
3.90
mm,
respectively.
Females
in
the
follicular
phase
had
a
larger
number
and
diameter
of
antral
follicles
than
both
non-pregnant
females
in
the
luteal
phase
and
pregnant
females
(P
<
0.0001;
Table
2).
Antral
follicles
>
2
mm
were
present
in
all
(100%)
females
in
the
follicular
phase,
and
were
also
observed
in
46.7%
of
preg-
nant
females
plus
non-pregnant
females
in
the
luteal
phase.
All
females
in
the
luteal
phase
had
at
least
one
true
CL.
Six
(19.4%)
pregnant
females
lacked
a
CL
and
were
in
mid
(2)
and
late
(4)
stages
of
pregnancy.
Pregnant
females
with
at
least
one
CL
and
females
in
the
luteal
phase
presented
on
average
the
same
number
of
true
CL
(Table
3),
and
there
was
no
difference
between
the
left
and
right
ovary.
The
largest
true
CL
was
7.10
mm
in
diameter
and
the
smallest
was
2.23
mm.
Table
3
shows
the
number,
diame-
ter
and
volume
of
CL,
and
luteal
volume
in
the
red
brocket
deer
females.
There
was
no
difference
in
luteal
variables
between
pregnant
and
non-pregnant
females
in
the
luteal
phase.
The
CL
was
characterized
by
the
presence
of
two
dis-
tinguishable
cell
types:
large
and
small
luteal
cells.
Large
luteal
cells
were
oval
or
polygonal
cells
(32.5
±
8.4
␮m
in
diameter)
with
an
abundant,
eosinophilic
and
vacuolated
cytoplasm
and
spherical
nuclei.
Small
luteal
cells
were
Table
3
Number,
mean
diameter
(mm),
volume
(mm3)
of
CL,
and
mean
luteal
volume
(mm3)
observed
in
ovaries
of
pregnant
and
non-pregnant
female
brocket
deer
(n
=
42).
N
Number
of
CL
Diameter
of
CL
(mm)
Largest
diameter
(mm)
Volume
of
CL
(mm3)
Luteal
volume
(mm3)
Non-pregnant
females
in
luteal
phase
11
1.22
±
0.4
4.61
±
1.57
7.10
11.50
±
4.08
13.91
±
3.75
Pregnant
females
31
0.97
±
0.57
5.17
±
1.46
6.50
13.76
±
2.63
10.93
±
6.39

P.
Mayor
et
al.
/
Animal
Reproduction
Science
128 (2011) 123–
128 127
oval
in
shape
with
a
round
nucleus
and
mean
diameter
of
9.9
±
2.4
␮m.
Both
large
and
small
luteal
cells
did
not
present
differences
according
to
the
type
of
CL.
4.
Discussion
The
aim
of
the
present
study
was
to
provide
knowl-
edge
on
the
reproductive
biology
of
the
red
brocket
deer
inhabiting
the
Amazon
region,
based
on
the
anatomical
and
histological
description
of
female
reproductive
organs
in
different
reproductive
states.
As
reported
by
Bisbal
(1994)
and
Hurtado-Gonzales
and
Bodmer
(2006),
in
the
Northeastern
Peruvian
Amazon,
con-
ceptions
occurred
year-round
in
the
red
brocket
deer
but
there
were
peaks
in
the
rate
of
conception.
In
this
study,
of
the
calendar
months
in
which
these
peaks
in
conception
occurred
did
not
coincide
with
those
recorded
by
Hurtado-
Gonzales
and
Bodmer
(2006)
in
the
same
study
area.
In
the
Amazon
region,
the
lack
of
large
seasonal
variation
in
the
availability
of
resources
in
the
tropical
environment
could
result
in
a
sufficient
food
supply
for
deers
to
sustain
a
pregnancy
regardless
of
the
month
of
the
year
(Gottdenker
and
Bodmer,
1998).
Since
variation
in
food
availability
is
the
main
factor
responsible
for
the
seasonal
reproduc-
tive
pattern
(Goodman,
1999),
the
red
brocket
deer
could
be
considered
an
opportunist
seasonal
breeder
capable
of
breeding
year-around
when
sufficient
food
is
available.
This
reproductive
strategy
is
particularly
common
in
the
tropics
(Goodman,
1999),
and
could
explain
the
different
peaks
in
conception
reported
by
Hurtado-Gonzales
and
Bodmer
(2006)
and
the
present
study.
The
wild
red
brocket
deer
female
presented
a
pregnancy
rate
of
46.1–49.4%,
similar
to
the
50%
of
pregnancy
rate
reported
by
Hurtado-Gonzales
and
Bodmer
(2006).
Esti-
mated
yearly
reproductive
production
of
0.76–0.82
young
per
female
was
considerably
lower
than
that
of
peccaries
(1.98
and
1.42
piglets
per
pregnant
female
in
the
collared
and
the
white-lipped
peccary,
respectively;
Mayor
et
al.,
2009,
2010),
suggesting
higher
vulnerability
to
hunting
for
this
species
compared
to
that
of
peccaries.
Bodmer
et
al.
(1997)
demonstrated
that
subsistence
hunters
in
the
study
area
do
not
have
prey
preference.
This
factor,
along
with
the
reproductive
aseasonally
of
the
species
in
the
study
area,
and
the
fact
that
there
is
no
sig-
nificant
difference
in
the
vulnerability
to
hunting
of
the
red
brocket
deer
female
according
to
the
pregnancy
stage
or
adult
sex,
justifies
the
accuracy
of
the
estimated
reproduc-
tive
parameters
in
the
studied
red
brocket
deer
population.
Red
brocket
deer
females
in
the
follicular
phase
had
on
average
24.7
antral
follicles,
from
which
1.40
follicles
were
larger
than
2
mm
and
reaching
a
maximum
diameter
of
3.90
mm.
These
data
suggest
the
presence
of
follicu-
lar
waves
involving
the
synchronous
growth
of
a
cohort
of
follicles,
but
only
one
will
generally
survive
and
con-
tinue
development,
reaching
maturity
at
4
mm.
The
other
follicles
degenerate
through
a
process
known
as
atresia.
Selection
in
monovular
species,
such
as
the
red
brocket
deer,
indicates
that
usually
only
one
follicle
of
a
follicular
wave
reaches
dominant
status
(Ginther,
2000).
In
species
with
a
strong
control
over
the
number
of
ovulations,
at
the
time
of
selection,
the
largest
follicle
probably
secretes
a
compound
with
a
paracrine
inhibitory
action
in
both
ovaries,
resulting
in
an
inhibitory
effect
on
the
growth
of
the
other
follicles
of
the
cohort
(Driancourt
et
al.,
1993).
These
data
suggest
the
high
correspondence
between
the
number
of
selected
follicles
for
its
further
development
and
the
ovulation
rate.
Although
the
red
brocket
deer
seems
to
be
monovular,
we
observed
the
occasional
occurrence
of
multiovulations.
The
frequent
presence
of
large
antral
follicles
in
the
ovaries
of
pregnant
females
suggests
that,
as
in
the
cow
(Rexroad
and
Casida,
1975;
Guilbault
et
al.,
1986),
follicular
growth
continues
throughout
pregnancy
in
the
red
brocket
deer.
Nevertheless,
in
pregnant
females
the
largest
follicle
is
smaller
than
those
in
females
in
the
follicular
phase.
The
observed
mean
ovulation
rate
was
1.14
CL
and
litter
size
was
1
fetus.
Females
presented
a
low
rate
of
reproduc-
tive
wastage
of
14.3%
of
embryos.
This
efficiency
is
high
compared
to
the
40–60%
wastage
per
pregnancy
reported
for
the
cow,
and
similar
to
the
12%
observed
in
the
ewe
(Sreenan
and
Diskin,
1986;
Berg
et
al.,
2010).
In
most
mam-
mals,
the
reduction
of
the
litter
size,
compatible
with
the
spatial
requirements
of
the
placenta
and
embryo
in
the
uterus,
is
paralleled
by
a
reduction
in
ovulation
rate,
result-
ing
in
a
lesser
rate
of
ovum
mortality
(Weir
and
Rowlands,
1973).
In
the
Bovidae,
there
are
important
species
differences
related
to
the
ability
of
ovaries
and
placenta
in
the
main-
tenance
of
pregnancy.
Whereas
in
goats
(Sheldrick
et
al.,
1980),
sheep
and
cattle
(Casida
and
Warwick,
1945)
the
pregnancy
CL
persists
until
term;
in
muskoxen
(Ovibos
moschatus;
Rowell
et
al.,
1993a,b),
Grant’s
gazelle
(Gazella
granti;
Spinage,
1986)
and
Thompson’s
gazelle
(Gazella
thompsonii;
Hvidberg-Hansen,
1970),
the
CL
regresses
completely
during
early
gestation,
and
pregnancy
is
prob-
ably
maintained
by
the
placenta
alone.
The
persistence
of
the
CL
in
the
late
pregnancy
stages
apparently
assures
the
maintenance
of
pregnancy
until
parturition
(Flood
et
al.,
2005).
On
the
other
hand,
in
species
presenting
a
complete
CL
regression
during
early
gestation,
the
high
placental
steroidogenesis
seems
to
inhibit
lactation.
Consequently,
the
conceptus
could
gain
a
nutritional
advantage
by
redi-
recting
resources
from
the
elder
sibling
to
the
fetus
in
uterus
(Mollett
et
al.,
1976).
In
the
red
brocket
deer,
most
pregnant
females
in
mid
(83%)
and
late
(64%)
pregnancy
stages
had
at
least
one
active
CL,
suggesting
the
persistence
of
CL
throughout
gestation.
Nonetheless,
a
small
proportion
of
pregnant
females
did
not
present
CL.
Although
preg-
nancy
CL
is
a
critical
source
of
progesterone
(Driancourt
et
al.,
1993),
in
some
pregnant
red
brocket
deer
females
in
advanced
stage
of
pregnancy
the
true
CL
regresses
com-
pletely
before
parturition,
probably
due
to
the
increasing
luteotropic
activity
of
the
placenta
and
its
ability
to
replace
the
CL
as
the
primary
source
of
progesterone
(Willard
et
al.,
1998).
The
basic
pattern
of
ovarian
events
in
the
red
brocket
deer
seems
to
be
as
follows.
The
red
brocket
deer
female
presents
ovarian
follicular
waves
involving
the
syn-
chronous
growth
of
a
cohort
of
an
average
25
follicles,
but
only
one
antral
follicle
is
selected
to
complete
its
growth,
reaching
a
pre-ovulatory
diameter
of
4
mm.
After
ovula-
tion,
the
matured
follicle
luteinizes
resulting
in
functional

128 P.
Mayor
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/
Animal
Reproduction
Science
128 (2011) 123–
128
CL.
In
case
of
oocyte
fertilization,
the
functional
CL
(now
pregnancy
CL)
grows
to
a
maximum
of
7
mm
in
diame-
ter.
In
most
pregnant
females,
the
CL
persists
throughout
pregnancy,
but
in
a
lesser
proportion
of
pregnant
females
regression
of
the
CL
in
advanced
stages
of
pregnancy
prob-
ably
occurs
due
to
the
increasing
luteotropic
activity
of
the
placenta.
Pregnant
females
have
waves
of
follicular
activ-
ity
until
late
pregnancy
stage,
but
dominant
follicles
do
not
attain
the
maximum
diameter
of
pre-ovulatory
follicles.
5.
Conclusions
The
present
study
provides
reproductive
information
related
to
the
reproductive
and
functional
ovarian
pattern
of
the
wild
red
brocket
deer
inhabiting
the
Northeast-
ern
Peruvian
Amazon.
The
present
reproductive
evaluation
provides
important
information
that
should
be
taken
into
account
in
management
plans,
and
the
results
of
this
study
are
being
directed
to
the
estimation
of
vulnerability
of
hunting
and
the
establishment
of
sustainable
harvest
rates
for
this
species.
Acknowledgements
We
sincerely
thank
all
the
people
from
the
Tamshiyacu-
Tahuayo
Communal
Reserve
(El
Chino,
San
Pedro,
7
de
Julio,
Diamante
and
Nueva
Esperanza)
who
actively
participated
in
data
collection,
which
shows
that
communal
participa-
tion
is
an
important
step
in
the
development
of
wildlife
management.
We
also
extend
our
thanks
to
P.
Puertas,
E.
Puertas,
M.
Antúnez
and
P.
Pérez
for
their
kind
assistance
during
the
fieldwork.
We
are
specially
thankful
for
the
institutional
support
provided
by
the
Universidad
Nacional
de
la
Amazonía
Peruana
and
the
Dirección
General
de
Flora
y
Fauna
(DGFF)
of
Perú.
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