J. Zool., Lond. (1998) 244, 63±70 # 1998 The Zoological Society of London Printed in the United Kingdom
The reproductive cycle and determination of sexual maturity in
male brown long-eared bats, Plecotus auritus (Chiroptera:
Vespertilionidae)
A. C. Entwistle1, P. A. Racey and J. R. Speakman
Department of Zoology, Aberdeen University, Aberdeen, U.K.
(Accepted 13 March 1997)
Abstract
Observations of the external morphology of wild-caught and captive male brown long-eared bats (Plecotus
auritus) revealed a marked seasonal pattern of spermatogenesis, similar to that established by histological
examination of other temperate-zone vespertilionids, with a peak in testes size in August and a lag between
testicular growth and epididymal distension. This was followed by complete cessation of spermatogenesis
and shrinkage of the testes to prepubertal size. The period of peak spermatogenesis coincided with a
reduction in the incidence of torpor and also a decline in body mass. This suggests that torpor and
spermatogenesis may be incompatible in this species. Outside the season of testicular growth and
epididymal distension, sexual maturity could not be con®dently determined in P. auritus by the pigmentation of the tunica vaginalis surrounding the epididymis, a characteristic which has become established in
other species. Instead, the size and shape of the caudae epididymides appeared to be a better criterion for
de®ning sexual maturity in this species. Most males underwent testicular growth and epididymal distension,
and were assumed to have reached sexual maturity, at an age of 15 months. However, some individuals
(29%), particularly those in good condition (relatively heavy individuals), showed a degree of testicular and
epididymal development in their ®rst autumn, i.e. at 3 months of age, indicating that the onset of puberty
may be dependent on body condition. Poor body condition was associated with delayed spermatogenesis in
adult males.
Key words: Chiroptera, spermatogenesis, torpor
INTRODUCTION
In mammalian species which hibernate, periods of hibernation and the time of reproductive activity are usually
temporally separated (Wimsatt, 1969). In males of such
species, the annual reproductive cycle is usually arrested
prior to winter, so that spermatogenesis does not coincide with hibernation (Wimsatt, 1969). The inverse
relationships between torpor and spermatogenesis have
been explored in rodents and insectivores, and two
separate explanations have been developed (e.g. Fowler
& Racey, 1987; Darrow et al., 1988; Lee et al., 1990).
First, torpor appears to suppress spermatogenesis, probably because of generally low metabolic rates and low
body temperatures. The costs of testicular growth and
maintenance are small relative to basal metabolic rate in
euthermic animals, but may be large relative to hibernal
resting metabolic rate (Kenagy & Trombulak, 1986). In
All correspondence to present address: Dr A. Entwistle, Fauna &
Flora International, Great Eastern House, Tenison Road, Cambridge
CB1 2DT, U.K.
most cases, therefore, spermatogenesis will not proceed
until the animal has woken from hibernation (e.g.
Barnes, Kretzmann, Licht & Zucker, 1986; Barnes,
Licht & Zucker, 1987). Second, testosterone, concentrations of which are highly elevated during spermatogenesis (Bronson, 1989), appears to inhibit torpor in
rodents. Hibernation did not proceed until testes had
regressed and testosterone levels were reduced in
autumn in hamsters (Vitale et al., 1985; Darrow et al.,
1988; Ouarour, Kirsch & PeÂvet, 1991), and implantation
of physiological amounts of testosterone led to immediate reversal of torpor in most individuals (e.g.
hamsters: Vitale et al., 1985; Darrow et al., 1988;
Ouarour et al., 1991; ground squirrels: Lee et al., 1990).
In microchiropteran bats, the annual reproductive
cycle of males is unusual, showing marked asynchrony
between spermatogenesis and maximal accessory gland
activity, stored epididymal spermatozoa, libido, and
copulation (e.g. Nyctalus noctula Racey, 1974b). In
addition, the activity of the accessory glands and
libido are maintained through the winter hibernation
period and into the following spring (Gustafson, 1979).
64
A. C. Entwistle, P. A. Racey and J. R. Speakman
Spermatogenesis is initiated in late spring, or early
summer, and is restricted to the summer months. At the
end of summer, spermatozoa are released from the
testes and pass into the epididymides, and the testes
regress. The spermatozoa are stored in the caudae
epididymides throughout winter. Copulations occur ®rst
in autumn and thereafter spermatozoa may be stored
both within the female and by the male (Racey, 1979).
On arousal from hibernation, the accessory glands
involute, the caudae epididymides shrink, and the cycle
of spermatogenesis recommences.
Many species of temperate-zone microchiropteran
bats occasionally become torpid during the summer
(e.g. Pearson, Koford & Pearson, 1952; Saint-Girons,
Brosset & Saint-Girons, 1969), as a mechanism to
balance energy expenditure when food supply is inadequate (Kurta, 1986). In many species, males remain
solitary during the summer and, without the thermal
bene®ts of clustering (Herreid, 1967; Kurta, 1986), may
thus experience low ambient temperatures. Males do
not have the same constraints against torpor as act on
reproducing females (i.e. delayed birth date: Racey,
1982), and consequently it has been suggested that they
would be expected to use daily torpor to minimize
energy expenditure (Fenton, 1970; Barclay, 1991; Hamilton & Barclay, 1994). However, in one species,
Myotis lucifugus, captive males kept under simulated
roost conditions maintained slightly higher body temperatures than lactating females (Kurta & Kunz, 1988),
thus contradicting expectations from ®eld studies.
Population studies require sexual maturity to be
determined in the ®eld, so that inferences about group
composition may be drawn. Because of the pronounced
seasonal regression of testes in many species of bat, it is
not always obvious which males of adult size have
previously undergone spermatogenesis and are thus
sexually mature. Racey (1974a) developed a method of
assessing sexual maturity in pipistrelle bats (Pipistrellus
pipistrellus) through external examination of the caudae
epididymides. He showed that when spermatozoa had
descended into the caudae epididymides the surrounding tunica vaginalis, which appears jet black in
juvenile animals owing to the high density of darkly
pigmented melanocytes, became stretched. The melanocytes became dispersed, revealing epididymal tubules
swollen with spermatozoa, which appeared white
through the skin of the interfemoral membrane. Even
when spermatozoa had been voided from the caudae
epididymides, the dispersed coloration remained, giving
a ¯ecked appearance, in contrast to the black pigmentation present before the onset of the ®rst spermatogenesis. Surgical investigations (removal of the testis and
epididymis through a slit in the skin) demonstrated this
criterion of sexual maturity to be accurate in 78% of
cases. Although this method has since been used to
determine sexual maturity in male Plecotus auritus (e.g.
Speakman & Racey, 1986; Boyd & Stebbings, 1989), its
reliability in this species has not been veri®ed.
The present study uses data from wild and captive
bats to investigate the timing and pattern of the repro-
ductive cycle in male Plecotus auritus, in relation to the
extent to which diurnal torpor is used during the
summer by males, and thus is compatible with spermatogenesis. It also investigates the applicability of
Racey's (1974a) criterion for assessing sexual maturity
in male P. auritus, and the age at which sexual maturity
is attained in males of this species.
METHODS
Bats were caught by hand or stationary handnet in 30
summer roosts, in north-east Scotland, during the
summers of 1991±1993. Bats were sexed, the forearm
was measured with Vernier callipers, and the bats were
weighed on a portable top-loading balance. Bats were
ringed with 3.0 mm aluminium rings (Mammal Society,
London). For every male caught, the diameter of the
testes was measured with Vernier callipers, and a sketch
was made showing the size and shape of the caudae
epididymides, and pattern of coloration of the surrounding tunica vaginalis, as seen through the transparent interfemoral membrane when held up to the light.
Bats were classi®ed as `torpid' or `euthermic', from their
temperature in the hand on capture and their response to
disturbance during capture, a technique validated under
laboratory conditions by comparison with measurements of body temperature (Entwistle, 1994).
Individuals with unfused phalangeal epiphyses were
classi®ed as juveniles (Racey, 1974a); individuals with
fused epiphyses but still in their year of birth (i.e. 2±3
months of age) were termed `young of the year' and
such bats were recognized from the grey colour of their
pelage. Bats in the summer after their birth (i.e. 9±15
months of age) were termed `yearlings'.
In a previous study, relative body condition was
calculated as individual body mass divided by forearm
length. However, since bats with larger forearms tend to
be proportionally heavier, this type of estimate may be
biased towards larger individuals. Instead, the relative
body condition of males was estimated as the residual
difference of individual body mass from that expected
from the overall relationship between body mass and
forearm (calculated across all adult bats; mass = 0.243
n = 1926,
(forearm)71.76;
F = 131.39,
r2 = 0.08,
P50.001).
A total of 14 males were brought into captivity from
summer colonies under licence from Scottish Natural
Heritage. They were housed in a ¯ight room (approximately 5 m63 m62 m) which was covered in netting but
otherwise subject to ambient temperature and a natural
light±dark cycle. A roost box provided shelter, and food
(mealworms, Tenebrio molitor) and water were available
ad lib. Females were kept in the same enclosure over the
autumn and winter, thus allowing mating opportunities.
At intervals of 2 weeks throughout the year all the males
were caught and the testes and caudae epididymides
were photographed at a magni®cation of 68.
The patterns of change in both testes and caudae
epididymides in wild bats were followed through a series
Reproductive cycle in male Plecotus auritus
Male reproductive cycle
Testicular growth was ®rst observed in early July and
continued to a peak in mid-August (Fig. 1a). During
September and October the testes regressed. At the
beginning of August, the caudae epididymides began to
distend. By mid-September, the caudae epididymides
appeared bulbous and their coloration was often
patchy. Thus any bat caught with enlarged testes and/or
distended caudae epididymides in autumn could be
considered to have undergone spermatogenesis that
year.
The form of the cauda epididymidis after autumn
could be ascertained only from captive animals, since no
wintering bats were located in the wild during the
present study. Caudae epididymides gradually shrank
over winter, reaching a minimum size in March/April.
There was no evidence of any spermatogenic activity
(i.e. testicular development) in winter or early spring.
5
1.0
55
4
Size (mm)
52
3
0.6
50
2
0.4
26
69
1
Proportion of males
0.8
36
0.2
11
0
6
11
8
1/5
1/6
0
1/7
1/8
1/9
1/10
(b)
1.0
Proportion of males euthermic
RESULTS
(a)
66
0.8
46 68
12 42 43
0.6
8
0.4
60
0.2
99
7
0
1/5
1/6
1/7
1/8
1/9
1/10
(c) 8.5
7
8.0
96
84
Mass (g)
of recaptures. Records from a previous ringing study,
carried out at the same roosts between 1978 and 1989,
were consulted. During this period, classi®cation of
sexual maturity in males had been made according to
the criteria of Racey (1974a). In the present study,
seasonal changes in testicular size and distension of the
cauda epididymidis of sexually mature adult males were
followed, as an indication of the progress of spermatogenesis, from ®eld records, in addition to photographs
from captive animals.
Investigations of the use of the cauda epididymidis to
distinguish sexual maturity, in male P. auritus, relied
upon ®rst identifying the state of the caudae epididymides found in juveniles and young of the year, which
could not previously have undergone spermatogenesis.
The form of such caudae epididymides could then be
compared to those of individuals known from ringing
records to have previously undergone spermatogenesis.
65
7.5
54
37
75
55
7.0
11 48
Torpor
4
6.5
The occurrence of torpor in males, in the wild, was
calculated from the proportion of males that were
caught torpid, either within a cluster or roosting alone,
in summer roosts. The incidence of torpor changed over
the summer (occurrence of torpor in each fortnight
between June and mid-September, w2 = 87.80, n = 344,
d.f. = 6, P50.001). The proportion of males using
torpor was lowest during the months of July and
August, and highest in May and September (data from
1991±1993; occurrence of torpor in the period between
mid-July and mid-August, compared with the rest of the
summer, w2 = 112.04, n = 451, d.f. = 1, P50.001; Fig.
1b). The decline in the incidence of torpor coincided
with the main peak in testes size and epididymal distension, although the relationship between testes size and
6
6.0
1/5
1/6
1/7
1/8
Date
1/9
1/10
Fig. 1. (a) The average testes size (*) and the proportion of
males showing distended caudae epididymides (*) in each
fortnight of the summer (data from 1991±1993). Error bars
indicate standard errors, and value labels show the sample
size. (b) The proportion of males caught which were euthermic
in each fortnight of the summer (data from 1991±1993). Error
bars indicate standard errors. Value labels represent sample
size. (c) The average body mass of males in each fortnight of
the summer (data from 1991±1993). Error bars indicate standard errors. Value labels represent sample size.
66
A. C. Entwistle, P. A. Racey and J. R. Speakman
the proportion of bats that were euthermic was not
signi®cant (Spearman's rank correlation rs = 0.467,
n = 10, n.s.), primarily because the bats were warm
during the period that the testes were growing but were
still small.
Body mass
Changes in body mass in males over the summer are
shown in Fig. 1c. A signi®cant decreasing trend in body
mass was recorded between mid-July and September
(data summed 1991±1993: mass = 9.8670.0111 (date),
F = 34.29, r2 = 0.07, n = 433, P50.001), followed by an
increase. Relative body condition (the residual to the
overall relationship between body mass and forearm),
and the degree to which the caudae epididymides were
distended, were compared in September of the years
1991 and 1992. In 1992, adult bats in which the caudae
epididymides were swollen had signi®cantly higher relative body conditions than those in which the testes were
large but no epididymal distension had yet occurred
(Table 1). No such difference was apparent in 1991,
when the sample size was much smaller.
Determination of sexual maturity in males
From the records of bats caught and recaptured
between 1978 and 1989, males were anomalously recorded as changing from a mature to an immature state
between subsequent catches in 26% of recaptures
(n = 74). This proportion was not signi®cantly different
from that expected if classi®cations had been made at
random (w2 = 0.162, n = 74, d.f. = 1, n.s.).
In both juveniles (n = 29) and young of the year
(n = 41), the cauda epididymidis was seen as a tiny
discrete nodule at the base of the fur line (Fig. 2; see
facing p. 64), although it was sometimes not visible at
all. The cauda epididymidis was usually of a dense black
colour; however, completely white, unpigmented,
caudae epididymides were also found in four young
individuals, and one bat with one black and one white
cauda epididymidis was caught (Table 2). Once an
individual showed signs of testicular growth, followed
by growth of the cauda epididymidis, the caudae could
no longer be discriminated from those of other bats
known to have undergone spermatogenesis previously.
Bats caught in autumn with large testes and swollen,
mottled black and white caudae epididymides had
clearly undergone spermatogenesis. Recapture records
allowed the changing form of the caudae epididymides
of such bats to be followed in subsequent years. The
following spring, after the spermatozoa had been
voided, the caudae epididymides were generally dorsoventrally ¯attened. However, many caudae epididymides did not retain the blotchy patterns of pigmentation associated with distension, and instead were of a
uniform black colour (Fig. 3). The larger size of these
caudae epididymides, however, made them obviously
different from those of sexually immature bats (which
Table 1. Comparison of the relative body conditions of bats,
caught in September, that showed distension of the caudae
epididymides and those that did not (Student's t-test)
Year
Mean not
distended
n
Mean
distended
n
t
P
1991
1992
70.438
70.780
6
9
70.375
70.377
5
28
0.23
2.66
n.s.
50.02
Table 2. The number of juveniles and young of the year found
with different forms of caudae epididymides
Form of caudae epididymides
Juvenile
Young
of year
Nodular, almost invisible under fur line
Tiny black nodule
Tiny nodule, tip black
Tiny white nodule
Tiny nodules, one black/one white
Black with limited distension
Patchy colour with some distension
10
16
2
1
0
0
0
0
28
2
3
1
6
1
Table 3. The colour of the cauda epididymidis of bats known
to have bred previously (i.e. caught with large testes and
distended epididymides in at least one autumn). This does not
include multiple recaptures of single bats
Black
Dispersed
June/July
August
Overall
12
14
8
9
20
23
possessed small nodular caudae epididymides, see Fig.
2). Of those males which had previously undergone
spermatogenesis and were recaptured during summer,
47% had caudae epididymides which remained black
(Table 3). The proportion of bats with black caudae
epididymides did not vary between the early part of the
summer (June and July) and late summer (August)
(w2 = 0.003, n = 43, d.f. = 1, n.s.; Table 3).
In addition to the immature males described above,
nine mature males were caught with completely white,
unpigmented, caudae epididymides (7% of the 134 bats
examined 1991±1993), and, also, eight mature males had
one black and one white cauda epididymidis (6% of
bats; total = 134).
Between 1991 and 1993, when the criterion of maturity was based upon the size of the cauda epididymidis, as opposed to colour, there were only two cases
in which bats which had previously undergone spermatogenesis were misidenti®ed as sexually immature (1.5%
of recaptures; n = 134). This contrasts with misclassi®cations of 26% (n = 74) over the years 1978±1989, when
colour was used as a criterion.
Timing of sexual maturity in males
From the males ringed as young of the year, 25 individuals were recaptured on at least one other occasion.
Reproductive cycle in male Plecotus auritus
Seven bats ringed as young of the year were recaptured
later in the autumn, and of these ®ve (71%) showed no
testicular development or subsequent swelling of the
caudae epididymides. The remaining two showed a
limited degree of testicular development, and very little
sign of any swelling of the caudae epididymides, which
lagged behind that of the adult males. Of seven bats
recaptured early in the year following their birth, only
two showed any degree of gonadal development from
the sexually immature state. However, by the autumn of
their second (yearling) year, three of the same individuals were caught and all showed some degree of
development, as did a further six individuals which had
not been caught since the previous year. Thereafter, the
caudae epididymides of these males were indistinguishable from those of older males. Of the individuals
recaptured in subsequent years (a total of seven recaptures between two and eight years after birth), only one
three-year-old showed no evidence of previous expansion of the caudae epididymides. It thus appeared that
the majority of males became sexually mature in their
second autumn, although some showed limited testicular development in their year of birth, and some may
take longer to develop.
In 1992, bats which showed some degree of testicular
growth and epididymal development in the autumn of
their natal year had signi®cantly higher relative body
condition than individuals where no development was
recorded (Table 4). This difference was not found in
1991 when a smaller sample size was available.
DISCUSSION
Male reproductive cycle
Changes in the appearance of testes and caudae epididymides, assessed through external examination, were
consistent with summer spermatogenesis, as described in
other hibernating vespertilionid species (e.g. Pearson et
al., 1952; Kunz, 1973; Racey & Tam, 1974). Changes in
testicular size indicated that spermatogenesis was completed, and spermatozoa were released from the testis,
around the end of August in Plecotus autirus, with a lag
between the seasonal recrudescence of testes and caudae
epididymides. Testes remained quiescent throughout
hibernation, and the caudae epididymides gradually
shrank over that time. At least some of the shrinkage in
size of the caudae epididymides may be attributable to
loss of spermatozoa during inseminations, since females
were housed in the same ¯ight cage. Spermatozoa stored
in caudae epididymides for long periods remain fertile
(Racey, 1973), and records exist for several species of
copulations of hibernating bats during periods of
arousal throughout hibernation (Pearson et al., 1952;
Thomas, Fenton & Barclay, 1979; Phillips & Inwards,
1985) and occasionally into spring (Barbour & Davis,
1969). A prolonged mating season, through winter and
spring, has been described previously for P. auritus
(Strelkov, 1962; Stebbings, 1966). Although sperma-
67
Table 4. Comparison of the body condition of bats that
showed distension of the caudae epididymides in the autumn
of their natal year, and those that did not (Student's t-test)
Year
Mean not
distended
n
Mean
distended
n
t
1991
1992
70.597
70.707
3
17
70.356
70.073
3
2
0.78 n.s.
4.67 50.001
P
tozoa stored by females, from autumn matings, may still
be fertile (Racey, 1979), spermatozoa storage over
winter by males may facilitate matings with females that
have lost spermatozoa during periodic arousals
(Oxberry, 1979), or with females that had not previously
been inseminated.
The current data suggested that inter-individual
differences in the timing of spermatogenesis were related
to body condition. The importance of body condition
during gonadal development in P. auritus had previously been considered by Speakman & Racey (1986),
who proposed that a `target body condition' had to be
achieved before spermatogenesis could proceed, in bats
considered to be sexually immature. In seasonally
breeding bats, a high degree of association has been
shown between testicular recrudescence and seasonal
increases in body weight (correlated in tropical bats
with the onset of the rains and the consequent elevated
food availability: McWilliam, 1988a, b). Thus, good
body condition may be a prerequisite for the commencement of spermatogenesis (Frisch, 1980).
Use of torpor
In the present study, the peak in testes size and the
initial distension of the caudae epididymides coincided
with an almost complete suspension of the use of torpor
by the males, as suggested by Kurta & Kunz (1988).
Loss of body mass over this period may have indicated
that food intake was insuf®cient to balance the costs of
remaining euthermic, or of the actual process of spermatogenesis. During the same period, the body mass of
both reproductive and non-reproductive females increased (Entwistle, 1994). The pattern in the use of
torpor by males over the summer suggests that, although
females are more likely to remain euthermic throughout
this time (Hamilton & Barclay, 1994; Grinevitch,
Holroyd & Barclay, 1995), the advantages of euthermy
for males may change as spermatogenesis progresses.
An increased incidence of males in the summer roosts
also occurs during this period of the summer (Entwistle,
1994), and may indicate a change in microclimate selection, and in the bene®ts of clustering, associated with
the peak of spermatogenesis.
The relationship between peak spermatogenesis and
the reduction of the use of torpor was consistent with
both non-exclusive suggestions regarding the incompatibility of torpor and spermatogenesis. If euthermy is a
prerequisite for spermatogenesis, avoidance of torpor
68
A. C. Entwistle, P. A. Racey and J. R. Speakman
during the warmest part of the summer may ensure that
sexual recrudescence is completed prior to the autumn
mating season. Plasma testosterone in several vespertilionid and rhinolophid species reaches its highest
annual level at the end of spermatogenesis (Racey,
1974b; Gustafson & Shemesh, 1976; Bernard, 1986), as
in other seasonally breeding mammals and birds
(Bronson, 1989). Thus the cessation in the use of torpor
at this time may re¯ect a reduced ability to enter torpor
when circulating testosterone levels are high. If testosterone inhibits torpor in bats, the consequences for
maintained secondary reproductive function throughout
hibernation need to be considered. Titres of plasma
testosterone taken from three microchiropteran species
during hibernation were considerably reduced, relative
to those taken during spermatogenesis (Nyctalus noctula
Racey, 1974b; Myotis lucifugus Gustafson & Shemesh,
1976; Gustafson, 1979; Rhinolophus capensis Bernard,
1986). It thus appears that, once developed, the accessory glands of reproduction are maintained by much
lower levels of testosterone than during recrudescence.
Hibernation may not be inhibited by moderate levels of
testosterone (as found in some individual ground squirrels: Lee et al., 1990), or bats may be less sensitive than
rodents to the action of testosterone. Levels of testosterone may be elevated during periodic arousals from
hibernation and act to maintain secondary reproductive
processes, before declining again on re-entry to torpor
(as shown in ground squirrels: Barnes et al., 1988). The
interrelationships of testosterone and hibernation in
bats require elucidation, perhaps through investigating
the effects of exogenous testosterone on hibernating
males. In addition, some bats do not display the same
temporal dissociation between hibernation and spermatogenesis; for example Rhinopoma kinneari (Rhinopomatidea) appears only to undergo spermatogenesis
during seasonal torpor (Anand Kumar, 1965). This may
suggest that the reactions of bats to testosterone may
differ from those reported in rodents.
Determination of sexual maturity in males
The use of the dispersal of melanocytes in the tunica
vaginalis surrounding the cauda epididymidis, as a
criterion of sexual maturity (Racey, 1974a), was developed speci®cally in relation to male Pipistrellus pipistrellus and has proved a useful ®eld diagnosis for that
species. However, its applicability to other vespertilionid
species has not been assessed (Racey, 1988). The present
study demonstrated that the ¯ecked black and white
appearance of distended caudae epididymides found in
autumn in P. auritus was not always retained after loss
of spermatozoa. Instead, the caudae epididymides often
regained a uniform black colour. In addition, completely
white caudae epididymides occurred in a small number
of bats, apparently present from birth, and presumably
the result of the complete absence of melanocytes from
the tunica vaginalis. Such inconsistencies, relative to the
pattern described for Pipistrellus pipistrellus, would
explain the anomalous changes from mature to immature classi®cations of bats caught between 1978 and
1989 and classi®ed by Racey's (1974a) criterion. A
recent study of Myotis daubentonii also suggested that
the coloration of epididymides was not a valid indicator
of sexual maturity in that species, since ®rst-year males
(de®ned from the presence of black pigmented chin
spots: Richardson, 1994), were found with spermatozoa
in their testes and had undergone some epididymal
distension, despite the presence of black caudae epididymides (Kokurewicz & BartmaÂnska, 1992).
The present study suggested that, in P. auritus, the
size and shape of the caudae epididymides were more
appropriate indicators of sexual maturity than was
colour. Pearson et al. (1952) also found that caudae
epididymides in young male Plecotus townsendii were
small and inconspicuous until the year after birth,
compared to those in adult males.
Timing of sexual maturity in males
Sexual maturity in male vespertilionids is usually attained at the age of 15 months, although some individuals appear to undergo spermatogenesis in their natal
year (Kunz, 1973; Racey, 1982; Tuttle & Stevenson,
1982). This applies to P. auritus, with most individuals
undergoing their ®rst spermatogenesis in the summer
after birth, although some may show some testicular
and epididymal growth at three months of age (Stebbings, 1966; this study). Limited testicular development
in some individuals in their natal year may not necessarily indicate that sexual maturity has been attained,
since the spermatozoa may not be fertile (`silent spermatogenesis': Gustafson & Damassa, 1984). In the present
study, testicular growth and epididymal distension in
bats in their natal year was substantially less than that
recorded from mature animals, and it may be that
further development could not proceed in the face of
decreasing food supply, in the autumn. The ®ndings of
the present study support this proposal, since the occurrence of rudimentary testicular growth was related to
body condition. A similar pattern has also been demonstrated in captive Myotis lucifugus, where puberty was
delayed when food was restricted (Damassa & Gustafson, 1985). However, the appearance of testes and
caudae epididymides in males having undergone spermatogenesis as yearlings did not differ from that in
older males in P. auritus, and it was assumed that sexual
maturity had been achieved. At this point, at least some
males were still associated with their natal roost (Entwistle, 1994), and hence were potentially capable of
mating with related females.
Acknowledgements
We are greatly indebted to all householders who
allowed us access to their homes in order to catch bats.
Bats were ringed and taken into captivity under licence
Reproductive cycle in male Plecotus auritus
from Scottish Natural Heritage. ACE was supported by
the Natural Environmental Research Council. Andy
Lucas took the photographs of bats, and Sue Swift
allowed us access to her ringing records.
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