Winter reproduction in the greater mouse-eared bat (Myotis myotis)
in South Iberia
C. IBAFEZ
Estación Biológica de Doflana, Apartado 1056, 41080 Sevilla, Spain
Introduction
One of the characteristics shared by temperate zone bats is the ability to delay reproductive events
(such as ovulation and fertilization and, more rarely, implantation). It has been suggested in different
vertebrate groups that these delays allow the females to time copulation and birth optimally in order to
obtain the best quality mates (Birkhead & MØller, 1993). In accordance with this hypothesis, mating
takes place in autumn in temperate zone bats, when males are in good physical condition. This timing
furnishes to females a better selection choice and allows the delivery of offspring in late spring or
summer when the availability of food resources is maximal.
During a study of cave-bat populations in Andalusia, southern Spain, some cases of winter
reproduction in a colony of mouse-eared bats (Myotis myotis) were observed and herein reported.
Methods
The colony is located in an abandoned mine in La Puebla de los Infantes (province of Seville, Spain) (37 °47’N,
5°25’W) at 180m a.s.l. The mine consists of a single gallery about 150m long, 2m high and I m broad. It has
neither lateral galleries nor shafts of any size but another comdor 20 m long near the entrance. The surrounding
area consists of pastures with holm- and cork-oaks (Spanish: ‘dehesa’), olive groves and cereal fields.
The mine was visited 5 times during winter and spring 1995 (18 and 24 January, 22 February, 31 May and 19
June). Population estimates were always attempted, although estimates became less accurate when the number of
individuals of M. myotis exceeded a thousand. In some captured and ringed (metallic rings, Lambournes Ltd.,
Birmingham, U.K.) individuals, forearm length was measured with dial callipers (to nearest 0.1 mm), body
weight, gender and reproductive status were recorded and age estimated (young or adult, and degree of teeth wear
in adults). The total epiphyseal gap between metacarpal and proximal phalanx of the fourth digit of the right wing
was additionally measured in young individuals (Kunz & Anthony, 1982) with a dial calliper while spreading the
wing over a source of light. Age estimations were based on the equations of postnatal growth of M. myotis,
calculated by Paz (1986) in Guadalajara, Central Spain. All captured young individuals had forearms smaller than
56 mm (age > 30 days). Therefore, total gap length (TG) was used for age estimations corresponding to the
equation of regression:
age = —15.87 +0.76TG.
Results
At the first inspection (18 January) we found a cluster of five individuals of M. myotis at the end of
the main gallery. Four of them were young whose epiphyseal gap between metacarpal and phalanx was
still apparent. They showed the typical grey coloured fur. The fifth specimen was an adult lactating
0
female with very worn teeth. The temperature in this zone of the mine was 20°C
and the bats were in
shallow torpor. Another cluster in the smaller gallery was formed by seven M. myotis and four
Miniopterus schreibersii. All M. myotis, two males and five females, were adults with worn to very
worn teeth. Three of the females had their nipples developed as if they were lactating, but had no milk
at that moment and the subjacent mammary glands were not swollen. The nipples of the other two
females were moderately developed. The bats of this cluster were in deep torpor. The temperature
inside the gallery is influenced by the outside temperature and, though it could not be measured, it was
notably lower than that in the first gallery. In fact, it was freezing in previous nights, with a minimum
record of —6°C four days earlier (14 January). On this occasion, no measuring, weighing or ringing
could be carried out.
In the same spot in which we had observed the five young M. myotis, some 50 individuals of this
species were found six days later (24 January). They were awake but did not show much activity. The
temperature in this part of the mine was 22°C. Five adults and three young individuals occupying the
centre of the cluster were captured. The measurements of the young and their age estimates are shown
in Table I. The age of the three young would be between 44 and 57 days (95% confidence interval).
According to this estimate, their birth would have taken place at the beginning of December 1994.
There appeared to be no more young in the cluster. Three of the adults were females, one in an
advanced stage of gestation (body mass: 36 g). The other two females were not apparently pregnant,
although they weighed 28.5 g and 30 g, respectively. Two of the females had very worn teeth, while
the third female and the males showed worn teeth.
On 22 February, a colony of more than a thousand M. myotis were roosting in the main gallery.
Twenty-one individuals were captured, 18 adults (2 males and 16 females) and 3 young (2 males and 1
femak). The measurements and age estimates of the young are shown in Table I. Two of the young had
TABLE
I
Characteristics of young bats captured at dfferent occasions during the study. Forearm length
(FA) and total epiphyseal gap length (TG) in mm, weight in g and age in days. The fledging in
Central Spain occurs at the age of 43 days with a mass of 23.1 g anda forearm length 0161.2 mm
(Paz, 1986)
Date and Individual
Sex
FA
Weight
TG
Age
M
F
F
58.3
57.8
56.8
18.5
19.5
21.0
4.0
4.6
4.2
53.5
48.9
52.0
M
F
M
59.0
58.9
59.3
23.5
23.5
21.5
1.0
0.8
4.8
76.9
78.5
47.3
M
M
M
M
M
F
F
F
60.3
60.6
62.2
61.5
62.3
59.6
64.5
62.9
25.0
24.5
23.5
21.0
24.5
21.5
26.5
23.5
3.4
5.7
4.7
3.6
5.6
6.4
5.5
7.0
58.2
40.3
48.1
56.7
41.1
34.8
41.9
30.2
24 January
2
3
22 February
1
2
4
31 May
5
6
7
8
9
10
11
12
been captured before (specimens No. 1 and No. 2 in Table I). The age differences between the two
estimates (made 29 days apart) on the recaptured individuals were 22 and 29 days, respectively. The
other young, estimated 47 days old, was born at the beginning of January and should have been around
20 days old at the previous visit. This young was probably born elsewhere, since its presence would
have been certainly detected if it had been in the mine at the previous visit. None of the adult females
captured was lactating. The temperature of the zone in which the colony was located, varied between
20 and 22 °C in the two visits.
On 31 May, the colony consisted of several thousand individuals of M. myotis, many of them young.
Eight young were captured and measured. The age estimates varied between 30 and 59 days (mean 44
days, see Table I), which indicates that they were born throughout April.
On 19 June, the colony again consisted of several thousands of bats, some of them M. blythii. The
majority of the young showed a total gap length of less than1 mm, even though all were still nonvolant suckling. The young individual No. 2 (ringed in January and checked again in February), was
again recaptured. The temperature between February and June was constant in the range of 20—22 °C.
Discussion
Myotis myotis is one of the early-breeding bat species which has its young during a broad range of
time (Brosset, 1955; Brosset & CaubIre, 1959; Kowalski et al., 1986). As an extreme case, a female
carrying two foetuses was captured in October in Tunisia (Baker et a!,, 1974). Mouse-eared bats of
North Africa are considered here as M. myotis, according to Arlettaz et al. (1997). This earliness could
be due to their feeding preferences on rather big-sized terrestrial arthropods (Bauerová, 1978; Audet,
1990; Arlettaz, Ruedi & Hausser, 1993), whose abundance is less temperature-dependent than for
flying insects (Lewis, 1993).
Birth took place during April for the greater part of the colony. If the intra-uterine life span is about
50 days (Herlant, 1956), ovulation and fertilization must have occurred during February, when the
colony arrived at the refuge. The reported birth dates are the earliest known for Europe (Brosset &
Caubère, 1959; Paz, 1986), including Central Spain (end of May and June), and are similar to those
described by Kowalski et al. (1986) for Algeria. Ovulation for young born in December must have
occurred at the beginning of October. It means that these bats did not hibernate that year, possibly
owing to the warm and dry conditions of that autumn (Table II) and the associated greater prey
availability. The three females with developed nipples that were found on 18 January in the smaller
gallery probably are the mothers of three of the young of the main gallery. The use of alternate low
temperature day roosts during cold periods related with no foraging activity is known at lactation in M.
myotis and Myotis emarginatus (Audet, 1990; Krull et al., 1991). This behaviour contributes to reduce
thermoregulatory costs as bats could use deep torpor in energetic deficit periods (Audet, 1990).
The time of breeding is an important fitness factor in animals. Generally, individuals born first
within the breeding period have important advantages regarding survival and social dominance. These
advantages are maintained for an important part of their lives (i.e. Svensson, 1995 for birds and Green
& Rothstein, 1993 for mammals). It has been shown in temperate zone bats that young born early have
more opportunities to accumulate reserves in order to survive their first winter (Racey, 1982). The
advantages of an earlier birth can be maintained throughout life. Individuals of Rhinolophus
ferrumequinum which were born during the second half of the breeding period had a lower probability
of living for more than 10 years than those which were born earlier (Ransome, 1989). It is therefore not
surprising that females try to have their young as early as possible, although it may be that only
females in good physical condition are able to reproduce early. In R. ferrumequinum, older females
TABLE II
Meteorological variables in the study area. Monthly mean values oft maximun temperature (maxT), minimum temperature
(minT), number of days with minimum temperature below zero (minT<O°C), number of days with maximun temperature over
25°C (maxT> 25 °C) and precipitation (precip). Mean temperature values of last 10 years, and mean precipitation values of last
20 years. Same values of 1994 within parentheses
Month
8
9
10
11
12
maxT
(°C)
minT
(°C)
minT<0 °C
(days)
maxT>25 °C
(days)
precip
(mm)
36.4/(37.5)
32.0/(31.3)
24.0/(26.5)
18.8/(20.7)
15.21(15.7)
17.1/(17.8)
14.9/(13.4)
11.5/(11.5)
6,91(6.9)
4.41(2.3)
01(0)
01(0)
01(0)
21(0)
51(10)
31/(31)
29/(28)
151(24)
11(0)
01(0)
4.41(0)
17.4/(3.5)
79.71(45.5)
121.6/(89.5)
113.91(7.1)
were in better physical condition with higher body mass both at the beginning and end of hibernation
(Ransome, 1968). Milligan & Brigham (1993) found that early reproduction and age were coincident
in females of Myotis yumanensis. In the present study, the females that gave birth in winter were old
too (worn to very worn teeth), and the survival rate of the young seems not to have been affected, in
spite of the low temperatures; which reached below zero during 10 nights in December and 16 more
nights in January (on none of our visits in January and February was any carcass of young found).
Although as a result of their early birth date, body masses and forearm lengths of the winter-born
young were lower than those born in spring in this colony and in the one of Central Spain (Table I)
(Paz, 1986). This fact, atso shown in late-born R. ferrumequinum, appears to be a long-term handicap
to successful breeding (Ransome, 1989).
I am grateful to A. Lafuente, L. Lara, E. Migens, J. L. Pérez-Jordá and J. Quetglas for assistance in field work.
J. Juste, R. Arlettaz and P. Racey provided helpful comments on the manuscript. This study was supported by the
Agencia de Medio Ambiente (Junta de AndalucIa).
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Are major roads a barrier to small mammals?
J. H. RICHARDSON, R. F. SHORE’, J. R. TREWEEK
N.E.R.C., Institute of Terrestrial Ecology, Monks Wood, Abbots Ripton, Huntingdon,
Cambridgeshire, PEI7 2LS, U.K.
AND S. B. C. LARKIN
S.A.F.E., Cranfield University, Silsoe Campus, Silsoe, Bedford MK45 4DT
Introduction
Road networks are developing and expanding in many countries. Great Britain alone has
approximately 365,000 km of roads and this figure is increasing each year (Department of Transport,
1995). Although verges associated with roads may provide suitable habitat for small mammals (Way,
1977; Adams & Geiss, 1983; Perrow, 1994; Ardeshir et at., subm.), roads themselves are linear
features which may act as a barrier to movement. Thus, roads may fragment habitats.
Several studies have specifically investigated the impact of roads on the movement of small
mammals. Oxley, Fenton & Carmody (1974) trapped small mammals adjacent to roads of varying
width and traffic density in the U.S.A. and concluded that roads inhibit movement, the most important
factor probably being road clearance (distance between vegetation cover on either side of the road). In
Canada, white-footed mice Peromyscus leucopus were recorded crossing a 3.3—6.4 m wide gravel road
infrequently, even though traffic density was only 1—2 vehicles per hour (vph), and it was concluded
that small forest roads were inhibitors of movement but not absolute barriers (Merriam et at., 1989).
‘Author to whom correspondence should be addressed