Embed Size (px)
Citation preview
Journal of Chemical Ecology, Vol. 22, No. 8, 1996
LIPID COMPOUNDS IN SECRETIONS OF FISHING BAT, Noctilio leporinus (CHIROPTERA: NOCTILIONIDAE)
A N N E P. B R O O K E * and D E N I C E M. D E C K E R
Graduate Program in Ethology Universi~., of Tennessee
Knoxville, Tennessee 3 7996
(Received November 13, 1995; accepted April I, 1996)
Abstract--The distinctive odor of Noctilio leporinus arises from oily secre- tions found beneath the wings in the subaxillary region. Analysis of secretions by gas chromatography-mass spectrometry identified 372 lipid compounds. Differences in number and chemical composition of glycolipids suggest that secretions of males from the same roost are more similar to each other than to other males or females. Differences in number and chemical composition of nonpolar lipids indicate that secretions of males are more similar to each other than to females. Since secretions differ between sexes, information on sexual identity and reproductive condition may be communicated. Individually unique lipid compositions further suggest that bats may be recognizable by their odor within the roost and while flying.
Key Words--Bats, scent marking, lipids.
INTRODUCTION
Bats (Order Chi rop te ra ) , like o t h e r m a m m a l s , p ro d u ce an a s s o r t m e n t o f scen t s
that are used in in t raspecif ic c o m m u n i c a t i o n (Schmid t , 1985). A l t h o u g h dis-
t inct ive odors are c o m m o n in many bat spec ies , the func t ion o f mos t o f these
scents is poor ly k n o w n . Indiv idual ident i f ica t ion f rom o l fac tory s igna ls has been
sugges t ed by research on g r o u p s o f little b r o w n bats (Myotis lucifigus) ( T h o m a s
et a l . , 1979) and for individual v amp i r e bats (Desmodus rotundus) (Schmid t and
Manske , 1973). M o t h e r M e x i c a n f ree- ta i led bats (Tadarida brasiliensis) use
o l fac t ion to he lp d i s t ingu i sh the i r y o u n g in d en s e l y packed nursery c r ech es that
*To whom correspondence should be addressed at: Department of Marine and Wildlife Manage- ment, P.O. Box 3730, Pago Pago, American Samoa 96799.
1411
14t2 BROOKE AND DECKER
contain tens of thousands of similarly aged young (McCracken and Gustin, 1991).
A few instances are known of bats using secretions to mark territories. Harem boundaries are delineated by male gray-headed flying foxes (Pteropus poliocephalus) (Nelson, 1965) and insular fruit bats (P. tonganus) (Grant and Banack, 1995) by rubbing secretions from neck and shoulder glands against tree branches. Both male and female Samoan flying foxes (P. samoensis) mark veg- etation within foraging areas with secretions from neck glands (Brooke, personal observation).
Bats also use secretions to mark conspecifics. Dominant male velvet free- tailed bats (Molossus molossus) mark both females and subordinate males with musky smelling secretions from their throat glands (Schmidt, 1985). Displaying male sac-winged bats, Saccopteryx bilineam, shake their wings at females and rival males dispensing secretions from wing pockets (Bradbury and Emmons, 1974).
Increases in secretions corresponding with seasonal mating have been found in male gray-headed flying foxes, P. poliocephalus (Ratcliff, 1932; Herreid, 1960: Nelson, 1965), velvet free-tailed bats, M. molossus (Schmidt, 1985), and Mexican free-tailed bats, T. brasiliensis (Davis et al,, 1962), suggesting that scent production is a secondary sexual signal. In addition, sexually dimorphic chest glands are present in the Phyllostomidae (Valdivieso and Tamsitt, 1964) and Molossidae (Weruer and Lay, 1963).
The fishing bat, Noctilio leporinus, has a particularly strong and distinctive odor. Goodwin (1928) identified flying N. leporinus on nights too dark to make visual observations on the basis of their distinctive musky odor. This smell has been attributed to their fish-eating diet (Gudger, 1945; Goodwin and Greenhall, 1961) or, alternatively, to the rank odor from the inguinal glands (Ruschi, 195t; Studier and Lavoie, 1984). Two different smells present are produced in different places: the skin and hair of the subaxial area beneath the wings of both males and females is covered by varying amounts of an oily yellow fluid that had a strong, musky-sweet odor, and second in males there is a rank or bitter scent that comes from the inguinal pockets found on either side of the testes.
Subaxial secretions have been reported only in one other bat species, the smaller N. albiventris (Dunn, 1934). In both IV. atbiventris and IV. leporinus the musky-sweet odor is stronger and more noticeable in males than in females (Goodwin, 1928; Dunn, 1934; Gudger, 1945), The odor is persistent: people who have handled bats of either species reported that the distinctive odor remains on their hands for several days, despite removal efforts (Dunn, 1934; Goodwin, 1928). No obvious gland can be found in the subaxial region of either species (Dunn, 1934; Brooke, personal observation).
Noctilio leoprinus has a polygynous social organization where discrete groups of 3-10 females cluster together with a single harem male in the roost
FISHING BAT LIPID SECRETIONS 1413
(Brooke, 1994). Many groups may utilize the same hollow tree or rock crevice, but each group exclusively uses a specific area within the roost. Female groups may remain together in the same location for several years regardless of turnover in harem males, who may retain their tenure for two or more reproductive seasons. Bachelor males roost alone or in small groups separate from females.
Female bats marked themselves with the subaxial secretions of other females in the same group (Brooke, 1994). "Head rubs" occurred when a female pressed her head beneath the wing of another and rotated her head from side to side, thereby transferring the scent of the other bat. Females also rubbed their fore- heads or chins against the foreheads of other females in their group. Females did not rub against either the subaxial area of resident males or the males' head. Female bats routinely "vis i ted" different groups within the roost (Brooke, 1994). When a visitor first entered the group of roosting bats, her head and wings were thoroughly smelled by the groups. Conversely, group members did not elicit any interest when entering their group,
In this paper we investigate whether the scent ofN. leporinus differs between adult males and females. Bats were captured to measure the amount of secretions and collect a sample for analysis. Secretions were collected and analyzed to determine differences in the chemical compounds between individuals, within social groups, and among different roosts. We compare lipids of adult males and females and of individuals from different roosts, Bats of known sex and social status were followed while foraging and when entering and exiting a night roost to detect odor in flight.
M E T H O D S A N D M A T E R I A L S
This study was conducted on the island of Culebra, 40 km east of Puerto Rico. Culebra is approximately 11 km × 3 km at its longest and widest points, respectively (for a complete description of the study site see Brooke, 1994).
Bats were captured in mist nets while exiting or returning to their day roost. Relative age, adult or juvenile (less than 1 year old) was determined by tooth wear and fused epiphysial joints (Brooke, 1994). The area covered by subaxial secretions was measured in square millimeters with a ruler.
Samples of subaxial secretions from 12 individuals (five males and seven females) from three different roosts were collected on sterile swabs, sealed in glass containers, and frozen. Secretions were extracted by a modified Bligh- Dyer solvent system (While et al., 1979) by D. Decker. Samples were analyzed for lipid composition following methods described for extraction, lipid isolation, gas chromatography, and mass spectrometry in Decker et al. (1992). The non- polar lipid sample from one female was lost.
To determine how the lipid components of secretions varied among indi-
1414 BROOKE AND DECKER
viduals, sexes, and different roosts, the presence and quantities (in picomoles) of each lipid compound were compared using an unweighted paired-group clus- ter analysis using arithmetic averages (UPGMA) using the NTSYS computer program (Rohlf, 1987).
To establish differences between males and females in flight, we followed two harem males and 23 females by radio telemetry (Brooke, 1994). On 10 occasions when bats flew within 5 m of us, we noted whether the distinctive smell was evident. Behavioral observations were made inside a building used as a night roost by up to 30 bats during May 1989. Whenever bats entered the building and flew from the roost we noted whether we could detect the musky odor. Sex of bats was established when each roosted.
RESULTS
The area covered by subaxial secretions was determined in 199 bats. The area covered by secretions in adults varied among individuals and between the sexes. There were no visible secretions on 43 juvenile bats examined. Of the 80 adult females examined, 59 individuals (73%) had no visible subaxillary secretions, 11 (14%) had only trace amounts visible, and 10 (12%) had 15-100 mm 2 covered by secretions. None of the 59 females without secretions had the sweet odor typical of males, while the 21 females with visible secretions carried the odor. Of the 76 adult males examined, 22 individuals (29%) had no visible secretions, while 54 (71%) had up to 200 mm ~- covered by secretions. Only males with secretions carried the distinct odor.
A total of 372 lipid compounds was identified in the secretions of 13 individuals: 52 glycolipids (Table 1), 196 nonpolar lipids (Table 2), and 124 phospholipids. Males and females shared 45 glycolipid compounds, 95 nonpolar compounds, and 13 phospholipid compounds. Males had an additional five glycotipid compounds, 55 nonpolar lipid compounds, and 13 phospholipid com- pounds not shared with females. Females had two glycolipid compounds, 46 nonpolar lipid compounds and 40 phospholipid compounds not shared with males. Three glycolipid compounds (12, 26, and 40) were found in large quan- tities in both sexes (Table 1).
The UPGMA showed differences by sex and roost atfiliation in glycolipid (Figure 1) and nonpolar lipid fractions (Figure 2). Since there was no apparent separation of individuals by either sex or roost affilitation by phospholipids, we have not reported further on these samples. There was no clear separation by sex within the glycolipid analysis. Harem males from the same roost (two indi- viduals from roost 1 and two individuals from roost 3) were more similar to each other than to any other individual (Figure 1). Glycolipid results from a third male, however, were closer to females than to any of the other males.
TA
BL
E
1.
RE
LA
TIV
E Q
UA
NT
ITIE
S IN
PIC
OM
OL
ES
OF
GL
YC
OL
IPID
CO
MPO
UN
DS
IN 5
M
AL
E A
ND
8
FE
MA
LE
Noc
tili
o le
pori
nus
-~
Mal
e F
emal
e
# C
ompo
und
775
764
126
328
712
218
229
781
760
761
327
777
778
z r.-
1 12
:0
2 Ph
enol
3
Thi
ocya
nic
acid
4
Unk
now
n 5
14:0
6
Unk
now
n 7
15:1
8
Hyd
roca
rbon
9
18:2
10
16
:1w
9c
11
16:1
w7c
12
16
:0
13
Unk
now
n 14
17
:2
15
a17
:0
16
17:1
17
17
:1w
8 18
H
ydro
carb
on
19
17
:0
20
Unk
now
n 21
18
:2w
6 22
18
:3w
3 23
18
:1w
9c
24
18
:lw
7t
25
18:1
w5c
26
18:0
0 0
0 5,
121
0 0
0 45
3 1,
478
0 63
1 0
126
0 3,
886
3,98
6 87
0 0
1,33
1 85
3 I3
5 0
0 0
0 0
0 1,
187
30
0 39
1 2,
849
155
2,89
1 0
0 54
0
171
0
0 0
8,51
7 0
0 0
682
686
487
3,20
0 4,
096
3,32
9 1,
237
1,77
4 69
9 1,
863
1,47
3 1,
157
0 0
0 0
0 0
941 0
0 55
0 84
1 0
0 0
0 0
1,03
0 61
9 0
0 0
0 75
8 91
8 0
0 0
0
0 0
0 0
0 0
0 0
706
723
3,25
0 19
.092
0
768
740
0 1.
097
1,54
6 92
9 0
954
0 0
0 0
0 5,
295
0 0
0 0
0 0
3,99
1 3,
848
0 0
0 0
521
35,5
37
17,2
80
27,6
66
11,3
58
23,5
27
14,4
45
36,9
00
42,4
18
143,
818
13,0
90
9,12
3 16
,225
40
,226
42
3,28
7 31
8,74
0 0
343,
016
389,
156
328,
353
396,
261
439,
635
5,05
5,03
6 42
4,45
7 34
9,19
1 43
7,67
2 32
9 0
5,94
1 10
,583
12
,142
8,
523
10
,64
1
3,22
2 4,
023
0 1
0,1
91
10
,675
0
186
3,77
7 1,
278
1,51
4 0
890
0 1,
221
627
18,6
04
0 0
0 1,
509
25,6
65
6,52
9 15
,525
1,
725
9,66
5 6,
970
7.01
7 10
,628
13
3,80
4 4,
954
5,02
4 8.
329
1,29
5 0
1,83
8 9,
305
5,23
0 5,
112
2,51
5 6,
783
12.4
88
0 4,
873
0 0
350
0 0
6,13
2 0
0 0
2,02
1 0
0 0
0 6.
176
0 3,
146
0 0
0 0
0 0
0 0
0 0
0 2,
266
15,6
80
19,5
07
26,2
64
9,92
4 23
,723
0
22,6
81
21,2
45
368,
545
26.4
27
28,2
27
2,32
3 29
2 1
,67
1
2,11
7 4,
151
1,87
2 0
22,8
69
1,02
8 2.
909
0 4.
463
0 0
1,36
4 0
0 22
7,48
0 0
0 11
,489
18
,473
18
.473
0
9,13
2 0
0 2,
887
69,8
14
18,6
78
0 15
,587
16
,863
0
6,70
4 8,
981
229.
387
0 9,
039
15,6
70
2,94
2 19
,630
28
,783
49
,000
27
.821
17
,795
13
,002
14
,657
26
.474
19
8,79
5 32
,217
37
,788
35
,928
72
1 0
7,03
5 14
,145
9,
647
4,79
9 11
,323
3,
262
5.98
1 19
,226
12
,623
10
,695
0
0 0
0 0
0 7,
435
0 62
,861
69
,283
0
74,1
10
0 8,
026
10,1
91
0 20
1,38
7 22
8,79
5 28
1,82
9 20
4,82
0 31
6,50
0 16
4,88
7 11
6,26
5 3,
330,
835
202,
077
322,
919
214.
424 0
398
7~
o 0 z
0
TA
m,
t< I
. C
onti
nued
Mal
e F
emal
e
# C
on'tp
ound
77
5 76
4 12
6 32
8 71
2 21
8 22
q 78
1 76
0 76
i 32
7 77
7 77
8
27
18:2
28
U
nkno
wn
29
18:2
30
18:2
31
19
:1
32
20
:4w
6
33
20
:2w
3
34
20
:5w
3
35
20
:2w
3
36
20
:2w
6
37
20
:3w
3
38
20:
Iw9c
39
20
: lw
gt
40
20
:0
41
Phe
nol
42
22
:6w
3
43
22
:4w
6
44
22
:5w
3
45
22
:0
46
Unk
now
n 47
a2
9 48
B
enzo
fum
n 49
2
0:4
w6
50
a33
51
18:
Iw5c
52
20
: Iw
9c
I .(X
)2
0 3
.2t9
4,
039
0 83
1 2.
'447
4.
694
5.2'
45
17.3
115
11
1,6l
~5
902
9.53
6 1,
21 I
2,
625
542
11
11
11
3311
11
t}
0 7.
263
0 0
11
11
0 11
11
11
0 12
11
(1
0 11
0
479
8.11
74
2.87
6 11
2,
227
2. 1
45
3,81
14
1,11
14
856
26,3
7,",
1,
020
0 23
3 1,
398
44.8
85
9,3
I11
8,77
2 8,
368
14.7
58
4.49
3 16
.113
6,
598
183,
676
7.4'
42
0
6,62
6 6,
567
67,6
86
29,9
00
411,
922
24,2
97
36,4
07
11
39.9
42
35,1
55
3211
,345
(I
14
.517
55
.816
0
7%79
1 0
0 0
0 0
16,4
22
23.6
69
11
23,3
43
11
0 0
0 1.
218
0 0
0 0
11
0 0
0 o
0
338
7.32
9 4,
115
6,02
0 7,
557
0 10
,797
89
9 2.
309
91.1
011
7.81
111
7.62
3 50
8 690
2,9[0
0
0
0
0
0
0
0
(1
0
0
0
4.67
9 8(
),31
8 31
,945
43
,510
21
.382
29
,083
20
,286
13
,103
12
.687
29
8,66
3 14
,114
9 16
,452
23
.965
1,08
4 14
,945
12
,116
15
.403
I1
,929
%
007
6,90
8 8,
416
4,43
8 13
4.42
7 5.
222
8.38
11
5.8/
14
297
3,07
8 6
.49
9
8,14
5 3,
844
1,84
4 1.
817
0 1.
6111
29
.649
I,
II3
1.
198
1.67
9 4,
178
14,4
05
108,
469
116.
827
89,8
25
64.7
71
142.
941
89.2
111
45.4
36
1.37
11.9
33
85.5
611
1111
.935
81
.53l
0
0 4
.36
8
4.68
1 3.
015
0 1.
408
I.II
3
11
11
l)
0 0
1.31
5 0
20.6
92
(1
I 1.2
93
9.40
3 23
,959
0
11
)1
3.31
7 20
.¢~9
2 t7
.061
t 60
0
332
11
1/
0 34
2 0
1.96
3 2.
376
1,24
t 71
4 2,
926
I 1,7
58
11
50,5
82
31,1
16
0 0
0 0
472
11
24,9
41
0 0
1,51
2 (I
67
4 0
307
7.58
8 4.
867
4,34
3 1,
185
11
6,6211
11
11
52.775
0 (1
0
42,5
52
38.4
83
0
33,2
79
0 0
0 0
645
1J
565
0 98
7
0 19
6 52
,869
1)
31
1.35
9 11
11
0 29
,626
68
1 0
0 0
0 26
7
I) 11
11
0 76.332
0 46,496
33.443
18.7
59
0
0 0
0 0
0 0
25,0611
663
14.4
52
253.
327 0 11
I)
II
(1
11
0
398
0 1)
1,
049
fi21
0
0 1)
0
0 0
36,7
33
(I
0 (1
56
8 (1
1)
0
(I
11
0 0
1)
(I
28./
112
27.2
55
28,6
36
0 0
11
0
7:
> Z
TA
BL
E 2
. R
EL
AT
IVE
QU
AN
TIT
IES
, IN
PIC
OM
OL
ES
, O
F N
ON
PO
LA
R L
IPID
CO
MP
OU
ND
S I
N 5
M
AkE
AN
D 7
F
EM
AL
E N
octil
io l
epor
inus
.'r
-
Mal
e F
emal
e
Co
mp
ou
nd
77
5 76
4 12
6 32
8 71
2 22
9 78
1 76
0 76
t 32
7 77
7 77
8
1 U
nkno
wn
2 T
etm
deca
nat
3 U
nkno
wn
4 U
nkno
wn
5 U
nkno
wn
6 U
nkno
wn
7 U
nkno
wn
8 T
ride
cana
l 9
Unk
now
n 10
U
nkno
wn
11
14:0
12
N
apht
hale
ne c
pd.
13
Unk
now
n 14
U
nkno
wn
15
15
:lw
16
U
nkno
wn
17
Unk
now
n 18
N
apht
hele
ne c
pd.
19
Tet
rade
cana
l 20
U
nkno
wn
21
15:0
22
U
nkno
wn
23
Unk
now
n 24
U
nkno
wn
25
Unk
now
n 26
U
nkno
wn
0 0
0 0
0 0
7,16
0 88
7 0
1.95
3 0
0 0
0 0
0 0
0 15
7 0
0 0
0 0
133
0 13
9 0
250
0 0
0 0
0 0
0 0
0 35
2 24
9 23
1 0
0 0
0 0
0 0
0 0
0 I O
0 0
0 0
0 0
0 0
0 0
298
0 0
0 0
0 0
0 0
0 0
0 0
0 0
0 0
0 3,
170
0 0
0 0
0 8,
754
0 0
0 0
3.27
5 4,
355
0 0
0 0
0 84
8 0
0 0
0 13
1 12
4 0
0 0
0
0 0
0 0
0 0
0 0
0 2,
065
0 0
0 0
0 0
0 0
0 0
2.06
2 1.
442
0 I.
145
0
0 0
0 0
5,20
3 0
0 9,
773
0 12
,926
10
,882
7,
562
9,89
2 0
5,94
6 0
0 17
,678
21
.566
0
11.4
48
0 0
0 0
0 2,
160
0
0 0
0 0
0 0
0 0
0 0
0 0
0 0
154
0 0
0 0
1,04
2 2
,82
0
0 90
6 0
0 48
8 1.
143
0 0
0 0
0 ! ,
206
0 0
0 0
232
572
0 0
0 0
0
0
7,457
0
6.332
0
0
0
0
0
0
t)
700
0 20
4 28
8 24
7 0
0 0
0 0
0 0
0 1,
085
0 0
0 0
858
975
0 0
0 0
298
0 50
6 44
4 67
5 0
0 0
0
1.73
1 2,
127
0 0
306
169
0
0
0
0
0
0
0
0
0
13,5
63
27,8
35
0 10
,547
12
,140
8,
692
19,9
87
24,4
17
12,5
30
15.2
11
16,6
85
15,1
I0
0
540
0
0
0
0
()
0
0
0
0
0
0 0
0 0
0 0
0 31
I
0 0
0 0
165
2,78
2 0
1,98
4 3,
028
0 5,
880
6,08
1 0
9,47
1)
0 0
C7
m
7.
TA
BL
E 2
. C
on
tin
ued
.~
Mal
e F
emal
e
Com
poun
d 77
5 76
4 12
6 32
8 71
2 22
9 78
1 76
0 76
1 32
7 77
7 77
8
27
Unk
now
n 28
11
6:0
29
16:
lw
30
16
:lw
9
31
16:1
w7
32
Unk
now
n 33
U
nkno
wn
34
Unk
now
n 35
Pe
ntad
ecan
al
36
Unk
now
n 37
U
nkno
wn
38
Alc
ohol
brl
6:1
39
U
nkno
wn
40
15:
tw
41
Unk
now
n 42
1
7:l
w8
43
1
7:l
w9
44
U
nkno
wn
45
17:0
46
1
7:l
w6
47
U
nkno
wn
48
Unk
now
n 49
U
nkno
wn
50
17:0
51
U
nkno
wn
52
Hex
adec
anal
783
0 0
0 0
0 24
0 54
1 0
0 0
0 0
0 1.
405
0 0
3,79
0 0
0 2,
167
0 8,
068
4,16
9 0
171
0 0
0 3,
901
0 0
0 0
0 0
10,8
65
25,8
02
0 9,
052
8,21
8 6,
883
7,53
8 11
,043
8.
452
76,0
27
9.66
4 8.
459
1,69
0 1,
558
0 1,
067
0 0
1,89
0 1,
792
0 0
0 0
0 0
0 0
0 0
0 2,
246
5,61
4 0
7,32
9 0
13,5
83
26.6
51
0 12
,819
13
,310
6,
802
10,2
99
14,7
27
8,92
1 12
,996
14
.690
9,
626
0 0
14,4
72
0 0
0 0
1,63
5 0
0 0
0 0
0 2,
374
0 0
0 0
1,01
7 0
0 4,
363
3,13
0 0
0 0
0 0
0 0
0 23
5,52
6 28
8,68
3 28
2,02
3 33
7,57
8 18
6,66
9 5,
098
150,
900
0 0
0 0
0 0
4,85
6 0
0 0
0 0
0 0
0 0
0 0
1,17
6 0
0 0
297~
156
0 15
4,83
3 16
2.65
0 72
,645
34
9,66
4354
,935
0
0 0
0 52
9 99
2 0
516
579
0 89
5 85
3 0
0 0
0 10
,206
0
6,96
1 6.
934
6,55
2 7,
838
8,62
2 I 1
,190
10
,059
1,
405
10.0
20
9.50
9 0
1,91
7 0
0 0
0 3,
489
1,69
1 0
0 0
0
0 0
0 0
0 0
0 0
0 0
0 0
2,13
3 3,
974
0 2,
012
1.25
3 0
0 0
0 5,
855
0 0
0 0
0 0
0 0
0 0
0 99
2 0
0 0
8,11
8 11
,415
5,
851
5,16
8 5
~0
58
4,
369
2,58
1 5,
060
7,05
8 0
7,40
3 3,
637
0 0
0 1,
922
0 0
0 0
0 0
0 0
0 m
0
0 0
0 0
0 0
203
0 0
0 0
>
Z
0 0
0 0
0 0
920
826
0 0
0 0
0 0
0 0
0 0
12,3
14
12,0
44
0 0
0 0
0 0
0 0
0 0
270
0 0
0 0
0 21
3 92
9 0
31 I
0
0 0
0 0
0 82
3 0
53
Unk
now
n 54
U
nkno
wn
55
Unk
now
n 56
U
nkno
wn
57
1,13
-Hex
adec
adie
ne
58
18
:3w
6
59
Unk
now
n 60
U
nkno
wn
61
Unk
now
n 62
U
nkno
wn
63
18
:3w
3
64
Unk
now
n 65
1
8:3
w3
66
18
:1w
9c
67
18
:1w
7c
68
18:
lw7t
69
Unk
now
n 70
U
nkno
wn
71
18
:1w
5c
72
18:0
73
b
r:1
82
w
74
br:
18
2w
75
Unk
now
n 76
U
nkno
wn
77
Unk
now
n
78
19:1
q12
79
19:1
w8
80
19
:1w
6
81
Unk
now
n 82
U
nkno
wn
83
Unk
now
n 84
2
0:5
w3
85
U
nkno
wn
934
0 0
0 0
0 30
7 0
199
0 0
0
8,77
8 8,
846
6.65
5 6
,05
0
5,94
4 8,
505
2,32
2 5,
730
765
598
0 0
4,66
5 5,
529
0 0
0 0
0 0
0 24
6 0
0 0
0 0
0 0
176
0 0
1.71
9 1,
029
1,94
4 56
1 0
0 0
682
0 0
0 0
0 0
0 2,
235
0 0
0 0
0 0
87
412
0 0
300
0 0
0
0 0
0 0
0 0
0 0
0 0
0 0
0 0
11,7
87
12,5
97
14,4
97
12,5
59
0 2,
298
0 0
0 0
0 0
0 0
0 0
0 0
0 0
0 0
0 0
0 0
0 0
0 0
0 0
15,2
89
8,48
9 6,
083
4,50
2 7,
521
6,62
2 10
,052
8.
083
7.75
5 2,
024
3,05
4 2,
283
43,8
53
47
,20
4
42.5
92
42,3
03
0 0
0 0
0 0
0 4
5,8
26
0
0 0
0 38
,468
48
,623
26
,845
26
.581
44
,935
26
,895
48
,427
0
57,8
52
85,5
18
60,6
97
48,0
93
46,1
33
76.1
53
83,4
54
58.7
49
75,6
65
58,9
01
87,5
63
70,6
33
14,4
94
11.6
50
0 25
,623
24
,098
4,
989
4,35
9 13
,331
10
.252
19
,108
28
,091
32
,105
52
7 0
18.9
69
3,59
3 0
0 0
0 0
0 0
0 0
0 1.
833
0 33
,263
0
0 I.
100
0
0 0
0 0
0 1,
076
0 0
2,22
3 0
1.05
0 0
0 0
0
182
0 0
841
702
0 1,
406
306
0 0
4.30
1 0
13.9
76
15.2
55
19.8
54
15.1
52
16.4
04
22.4
96
18,4
26
16,8
54
36,4
38
25.9
41
55.9
86
28,8
56
0 0
216
0 49
4 0
0 0
0 0
0 0
0 0
0 0
0 0
1,25
1 3.
318
0 49
8 0
0
7,69
0 0
0 0
0 0
1.15
1 1,
493
0 0
0 0
44
6,8
00
0
0 2.
727
0 0
0 0
0 0
0 0
8.99
6 0
8.93
2 0
1,49
4 10
,576
5,
184
4,09
8 8.
023
4.82
2 9,
325
8,63
4
0 9,
541
0 7.
338
0 0
0 0
0 0
0 0
0 1,
091
864
0 0
0 52
0 0
0 0
0 0
15,0
30
17,8
25
15,1
21
15,6
31
14,3
69
14,1
43
13,3
76
17,9
93
20,0
91
23,2
42
26,7
35
12,3
66
0 0
0 67
.559
66
,057
0
0 0
0 0
0 0
0 0
0 0
0 3,
450
0 0
2,14
6 0
3,20
9 15
9 4,
222
8,68
7 0
2,41
3 6,
640
0 0
0 0
0 3,
068
0 48
7 1.
984
0 52
8 47
0 0
0 0
0 0
0 0
685
0 39
9 0
251
0 0
0 0
0 0
0 xO
TA
BL
E 2
. C
on
tin
ued
-7
, i,,
.a
o
Mal
e F
emal
e
Com
poun
d 77
5 76
4 12
6 32
8 71
2 22
9 78
1 76
0 76
1 32
7 77
7 77
8
86
Unk
now
n 87
C
ycio
prop
yt 1
9
88
Unk
now
n 89
U
nkno
wn
90
Unk
now
n 91
P
oiyu
nsat
. 2
0:3
92
Unk
now
n 93
U
nkno
wn
94
20
:4w
6
95
Unk
now
n
96
Unk
now
n 97
U
nkno
wn
98
20:
2w?
99
Unk
now
n
I00
20
:Iw
9
101
21-a
ne (
C,iH
.,.a)
MW
=
296
102
20
:0
103
Unk
now
n
104
Unk
now
n 10
5 U
nkno
wn
106
20
:3w
3
107
20
:Iw
9
108
20
:lw
7
109
Unk
now
n 11
0 U
nkno
wn
111
Unk
now
n
0 0
0 0
0 0
0 0
0 0
0 0
0 0
0 0
0 0
0 0
44,4
27
13,8
58
49
.50
0
47
,90
8
39,9
77
0 IA
43
1,
539
1.10
4 98
9 0
0
0 0
1,95
4 0
0 0
0 0
0 0
1,41
7 0
0 0
0 0
0 3,
323
0 0
0 0
1)
9,51
7 2,
673
1.72
4 0
1.00
3 0
772
0 2.
124
0 0
431
0 0
0 o
0 o
0 0
134,
709
0 85
,832
76
,193
85
,896
0 0
0 0
0 0
257
487
0 20
0 21
2 0
16,8
58
19.4
97
21.8
00
15.6
17
16.0
76
9.66
7 0
0 20
5 0
374
0
3.07
0 4.
013
0 6
.52
0
5,33
5 0
0 62
4 0
0 0
0 83
.625
1,
114
103.
943
0 0
6.6
t3
7.69
5 0
13.3
37
9.51
3 8.
791
0
0 0
5,90
9 0
0 0
177
0 0
161
0 0
0 0
0 0
0 0
6,02
9 0
6.78
2 5,
253
4,8
78
4,
654 0
4,8
28
5.
237
0 7,
419
0 t)
0
0 76
I
0 46
,557
6
3.6
06
38
.57I
32
,905
0
6.7
96
5,
799
0 8
A5
7
41.7
47
50,8
77
0 17
,959
0
0 0
0
0 0
0 0
0 58
1 1,
892
0 0
0 0
0 2,
420
0 0
0 0
0 0
0
0 0
1,04
5 0
0 0
0 0
0 0
0 0
0 0
19.5
63
39,4
45
28.2
27
62,9
77
46,9
71
80,7
71
3,36
9 1,
643
0 0
0
165
0 0
I,II
0
0 9,
104
8,75
5 I 1
.903
7,
361
17,6
83
397
532
0 0
0
0 82
6 0
0 1,
863
0 18
0 0
0 0
0 0
0 0
0 0
o 0
0 0
0 0
o 0
0 0
o 0
0 0
0 0
0 0
0 2.
648
1.96
4 3.
838
3.13
9 4,
742 0
0 0
0
0 0
0 0
0 0
0 0 0 0
2.74
4 0 0 0 4,
868
72,3
33 0 0
9,56
5 0 0 o 8
0 :~
0
> z 1,
201 0
661
4.2
68
ll2
U
nkno
wn
0 0
10,0
90
0 0
0 11
3 2
1:l
w
0 4
,71
0
458
0 0
0 11
4 U
nkno
wn
0 0
342
0 0
0 11
5 2
2:4
w6
0
0 5,
649
0 0
0 [1
6 U
nkno
wn
0 0
113
0 0
0 11
7 2
2:4
.5 o
r 6
9.78
9 10
.546
0
8.33
5 7.
365
7.48
8 11
8 2
2:6
w3
2.
780
4,6
49
0
2.58
5 2.
809
0 11
9 U
nkno
wn
535
392
0 23
5 0
0
120
Unk
now
n 77
9 1,
815
0 72
0 0
0 12
1 U
nkno
wn
876
0 0
1,03
3 0
0 12
2 U
nkno
wn
23,2
44
29,4
46
0 22
,354
23
,885
23
,159
12
3 U
nkno
wn
5,85
0 9,
826
31,0
24
7,52
7 7,
559
3,73
5
124
Unk
now
n 0
0 0
0 0
0 12
5 2
2:2
w6
0
0 0
0 0
0 12
6 22
: lw
7 0
0 2,
633
3,27
4 3,
097
0 12
7 2
2:0
0
0 36
,778
0
0 0
128
22
:lw
9
0 0
10,3
16
0 0
0 12
9 U
nkno
wn
0 0
305
0 0
0 13
0 U
nkno
wn
1.14
3 0
0 60
1 0
0 13
1 U
nkno
wn
391
0 0
0 0
0
132
Unk
now
n 0
0 2,
221
0 0
0 13
3 U
nkno
wn
0 0
4,88
5 0
0 0
134
Unk
now
n 0
0 36
,781
0
0 0
135
C2~
0
0 0
0 0
0 13
6 2
2:0
6.
841
8.89
0 13
.011
8.
739
9,40
4 5.
188
137
Unk
now
n 2,
335
2.54
3 0
2.08
2 2,
020
1,95
2 13
8 U
nkno
wn
2,22
7 1,
872
0 1,
728
1,73
5 1,
603
139
Met
hyl
phen
yl i
mid
azol
idin
one
0 0
0 0
0 0
140
23
:0
6,30
9 3,
975
0 3,
768
20,2
46
2,45
3 14
1 U
nkno
wn
0 0
0 37
2 28
1 0
142
Unk
now
n 30
0 0
0 42
9 0
0 14
3 C
_~
0 0
0 0
0 0
0 0
0 0
0 0
0 0
0 0
0 0
459
227
1,25
5 0
0 0
0 0
0 0
0 0
0 0
0 0
0 0
3.55
0 2.
809
8.80
6 5,
705
9.67
4 5.
178
2.53
4 1.
687
2.25
9 1.
615
3.26
4 0
0 0
0 0
0 0
0 0
0 o
0 o
o 0
0 o
0 0
0 0
16,9
14
0 23
.235
18
,485
3.
I(K
I 2,
121
0 0
0 0
718
286
0 0
0 0
13,7
27
10,7
49
I.)
19,7
58
0 0
0 38
5 0
0 0
0 0
3,06
3 0
0 0
0
0 0
0 2,
809
0 0
o 0
0 o
o o
0 0
0 0
0 0
0 0
0 0
o 0
0 0
0 o
0 o
0
0
0 0
0
0
0
0
0
0
0
0
0 0
0 72
6 0
0
3.93
8 0
6.24
5 4.
514
8,99
0 5,
255
1.44
0 I,
I13
t,71
5 0
2,02
3 0
[, 1
50
1,03
9 1.
940
2,03
9 2,
077
0 23
2 34
6 0
0 0
0
2,35
7 1,
857
6,15
9 0
3,57
5 2,
492
o 0
0 o
o o
o o
0 o
o o
0 0
0 55
8 0
0 t.~
TA
BL
E 2
. C
on
tin
ued
.~
t,,
a t,,
a
Mal
e F
emal
e
Com
poun
d 77
5 76
4 12
6 32
8 71
2 22
9 78
1 76
0 76
1 32
7 77
7 77
8
144
15:0
14
5 9-
24-s
ene
146
24
:lw
9
147
24:1
H
ydro
carb
on
148
Unk
now
n 14
9 2
4:0
15
0 U
nkno
wn
151
Unk
now
n 15
2 U
nkno
wn
153
Hyd
roca
rbon
15
4 D
imet
hyld
iene
15
5 U
nkno
wn
156
Unk
now
n 15
7 U
nkno
wn
158
Unk
now
n 15
9 U
nkno
wn
160
Unk
now
n 16
1 U
nkno
wn
162
Unk
now
n 16
3 U
nkno
wn
164
Unk
now
n 16
5 U
nkno
wn
166
Unk
now
n 16
7 U
nkno
wn
168
Unk
now
n 16
9 U
nkno
wn
0 0
0 0
0 0
0 0
0 2,
174
0 0
I 1,6
95
7,13
5 0
9,96
3 11
,792
13
,590
8,
482
7,43
8 13
,606
16
.128
16
,242
13
,369
21
,784
16
,147
0
20.1
34
23,7
56
17,2
05
12,3
76
6,04
8 8,
838
9,60
9 1
0,4
61
8,
285
3,76
7 2.
297
8,35
8 8,
981
10,4
87
1,51
8 94
9 5,
752
0 4,
649
4.73
5 3,
557
0 0
0 1,
363
1,56
8 5,
680
0 11
,763
0
0 0
0 25
,595
15
,641
0
0 0
16,6
87
15,1
35
I 1,9
25
18,2
08
16
,48
1
21.4
78
0 0
0 0
0 0
0 17
1 0
0 0
0 0
711
642
0 1
.07
1
442
626
484
361
2,49
1 71
0 0
0
2,02
4 0
0 1,
876
1.40
0 1,
623
1.05
0 l,
193
0
2,56
9 2,
886
1,22
3 0
0 0
217
0 0
0 0
0 0
0 0
1,54
1 44
3 4.
360
1,44
0 2.
004
2,93
9 4,
158
2,93
3 10
,164
1,
315
10,4
76
6,01
7 0
2,72
6 0
6,08
0 8,
443
5,84
7 5,
272
4,71
1 7,
045
6,53
9 7,
561
7,25
9 0
256 0 0
2.38
4 0
184
0 3.
198
0 19
,580
5.
823
3.90
3 93
9 0
0 6,
988
0 23
7 0
140
0 11
6,93
5
726
0 0
1,95
0 0 0 0
136.
578
12,8
67
115,
198
220.
585
78,3
48
63,1
75
164
0 0
0 33
1 0
1,72
5 0
0 23
3 1,
471
543
1,76
9 1,
936
0 1,
382
0 0
0 0
1,95
4 0
0 0
0 0
0 0
721
0 47
6 0
0 0
0 0
0 0
0 2,
403
0 65
8 28
8 0
0 0
0 0
0 50
5 0
0 0
0 0
0 0
0 0
1.95
2 2.
440
3.65
5 1.
993
1,7
71
3,
662
4,12
4 3,
966
3.18
9 0
0 19
,115
19
.726
12
,254
5,
034
10
.44
1
9,23
7 41
,069
8.
581
0 5,
336
6.25
3 0
394
952
0 3,
742
4,20
0 3.
546
m
0 0
0 49
2 0
0 0
0 0
0 z
0 7,
285
9,t
79
6,
451
5.73
3 4,
598
7,59
2 7,
262
7,76
3 8,
009
0 0
0 0
566
524
0 0
0 0
m
0 0
436
0 0
0 0
0 0
0
o o
o o
.~
170
Unk
now
n 17
1 S
tero
l
172
Unk
now
n 17
3 U
nkno
wn
174
Unk
now
n 17
5 U
nkno
wn
176
Unk
now
n
177
Unk
now
n 17
8 U
nkno
wn
179
Unk
now
n 18
0 U
nkno
wn
181
Unk
now
n 18
2 U
nkno
wn
183
Unk
now
n 18
4 U
nkno
wn
185
Unk
now
n 18
6 U
nkno
wn
187
Unk
now
n 18
8 U
nkno
wn
189
Unk
now
n 19
0 U
nkno
wn
191
Unk
now
n 19
2 U
nkno
wn
193
Unk
now
n 19
4 U
nkno
wn
195
Unk
now
n 19
6 U
nkno
wn
2,47
0 0 0 94
4 0 0 0
66,4
06 0
2,90
5 0 0 0 1,
785 0 0
0 43
4 2,
884
2.69
4 2,
233
948
500
0 0
0 0
0 77
3 0
0 0
0 0
0 0
0 0
0 0
0 0
0 0
0 3,
617
862
0 0
0 2,
365
710
1,57
6 0
0 0
4.23
3 0
2.43
1 0
0 0
0 0
0 0
0 15
8,32
8 70
.938
0
149,
705
0 0
0 0
0 I,
I 15
87
5 0
2,27
3 0
0 0
0 0
71,5
70
63.8
99
20,4
81
13,1
48
41
,48
8
18,8
11
41
.24
8
31.1
45
0 10
1,81
9 90
,363
0
0 0
0 0
0 0
0
0 0
0 0
0 0
0 0
0 2,
120
2,68
5 0
3,38
0 0
269
3,06
8 1.
053
840
2,44
2 I 1
,788
0
0 0
1,02
4 0
470
0 0
0 0
0 0
0
0 0
0 0
0 0
1.21
2 0
0 0
0 0
0 0
0 0
617
410
0 0
0 0
0 1,
772
1,36
3 I,
177
1,
403
675
330
0 0
0 0
0 17
4 13
5 18
3 0
0 0
0 0
0 0
0 0
0 0
0 0
0 0
3,95
5 0
0 0
11,7
13
0 0
1,23
6 3,
815
9,4
36
0 0 0
415
9.42
6 0 0
0 0
668
0 0
0 0
0 0
0 0
0 0
0 46
7 0
0 1.
097
0 0
0 0
2,36
6 1,
558
1.32
0 1,
076
0 1,
789
2.07
3 0
0 1,
747
421
0 12
.411
95
2 5.
395
0 6.
271
6,33
4 0
0 94
1 1,
3798
5,
673
0 0
693
0 1,
399
0 0
0 86
4 0
0 0
0 0
0 0
0 0
0 0
0 0
0 16
4 0
0 0
0 0
0 0
211
0 0
136
371
0 0
0 0
0 0
9.83
0 0
19,6
28
0 0
0 0
6.34
1 9,
692
0 11
,591
0
11,0
16
0 14
,789
9,
827
0 8,
378
0 0
0 30
0 20
7 0
0 0
0 0
0 0
0
1424 BROOKE AND DECKER
I I
Bat # Roost i ........... 775 1
764 1
..................... I ........... 218 5
i 778 3
i .......................... 761 1
777 3
126 3
712 3
I 229 5
327 3
328 3
~ - - 781 5
- - 760 1
FIG. I. UPGMA cluster analysis of the relationships among glycolipid compounds found in the subaxial secretions of 13 Noctilio leporinus from Culebra, Puerto Rico. Males underlined.
Although two pairs of males from the same roost grouped together, females were not grouped by roost affiliation (Figure 1). After separation of lipids during analysis, the distinctive smell of secretions was present only in glycolipids,
In the nonpolar lipid analysis, five males were more similar to each other than to females in the concentrations and numbers of compounds (Figure 2). There was no clear separation of males from different roosts. Two females from the same roost were more similar to each other than to any other individual.
The odor of harem males was very noticeable to human observers as bats foraged for insects over fields at night. On six occasions when radio-tagged male bats flew within 5 m of our position, the musky scent was obvious. Arrivals and departures of resident males at the night roost were also evident from odor alone (N = 7). Conversely, females were not identifiable by their odor when foraging close to our position (N = 4) or when flying within the night roost (N = 9).
DISCUSSION
Subaxial secretions were a mixture of glycolipids, nonpolar lipids, and phospholipids that varied among individuals in composition, concentration, and
FISIt lNG BAT LIPID SECRETIONS 1425
Bat # Roost 775 1
328 3
[ t I
I
712 3
764 1
126 3
229 5
761 1
777 3
778 3
781 5
I 760 1
327 3
FIG. 2. UPGMA cluster analysis of the relationships among nonpolar lipid compounds found in the subaxial secretions of 12 Nocti/io leporinus from Culebra, Puerto Rico. Males underlined.
the number of compounds. A number of compounds were present only in males or females, suggesting that scents may be sex-specific (Tables 1 and 2). Further evidence of dimorphic scent comes from the similarity of nonpolar lipid com- pounds in the five males. Production of chemicals in scent glands has been linked with an individual's hormonal status (Ebling, 1977). As with secondary sexual characteristics of other mammals, the strong scent of males" subaxial secretions may advertise social status.
The individually unique chemical cocktail of subaxial secretions suggests that odor profiles differ among N. leporinus. Differences in type and quantity of chemicals in subaxial secretions may form the basis for individual recognition by olfaction. Individual N. /eporinus smelled the head and wings of conspecifics when they first met, both in day and night roosts. This interest in individual smell suggests that scent plays a role in individual identification. Whether N. leporinus is able to distinguish among conspecifics by scent was not tested in this study and remains to be answered.
The smaller amount of subaxial secretions in most females compared to males may be a result of behavioral removal of secretions by head rubs. When female N. /eporinus rub their heads together, secretions are probably transferred between individuals. Through this scent transfer, the mixture of individual scents may develop a group olfactory identity.
1426 BROOKE AND DECKER
The similarity in both concentration and specificity of glycolipids between males from the same roost suggests that these individuals may develop com- parable odor profiles, possibly as a result of frequent interactions. The presence of nonpolar lipids in males distinguished them from females but showed no apparent within-roost or within-group distinctiveness. As phospholipids are both odorless and tasteless to humans and, presumably, to other mammals, they may not contribute to a communicative scent. Consequently, lack of differences among bats of different sex and roost affiliation is not surprising,
Mammalian scent-marking behavior is recognized to play a role in signaling social status (Brown, 1979). Many terrestrial mammals, such as hyenas, bad- gers, and wolves, regularly mark territorial boundaries with chemical signals (Macdonald, 1985). Female little brown bats may mark trees, possibly to aid orientation between foraging areas and roost when young are first learning to fly (Buchler, 1980). Noctilio leporinus were not observed using subaxial secre- tions to scent mark; however, the strong odor of harem males is broadcast when the bat flies. Odor trails left by these males may serve to advertise foraging territories and arrivals at night roosts. Schnitzler et al. (1994) reported that a male N. leporinus they watched defending a foraging territory from other bats was accompanied by a strong wave of odor. Similarly, the sweet odor of two other neotropical bat species, Tonatia bidens and Mimon crenulatum, may also function in social behavior, as the males" secretions can be detected as a bat flies nearby (Brooke, personal observation).
If male N. leporinus use odor trails to advertise their presence, other indi- viduals might be able to detect small amounts of the scent. The sensitivity of bats to intraspecific odors is unknown, but the sensitivity of some bats to fruit odors has been examined. The short-tailed fruit bat (Carollia perspicillata) is able to locate fruit exclusively by olfaction (Laska and Schmidt, 1986). When tested for sensitivity to fruit odors (esters, alcohols, and carbon acids), short- tailed fruit bats were able to detect from 3.6 × 10 ~5 to 2.7 × 10 ~° molecules/ cm 3 (Laska, 1990). In comparison, moths that orient toward the source of an airborne chemical plume can detect 103-106 molecules/cm 3 (Dusenbery, 1992). Bats may be able to detect airborne odor trails, but the morphological variation in the number of olfactory receptor cells and amount of olfactory muscosa suggest that bat species differ greatly in olfactory ability (Schmidt, 1985).
We have described the chemical constituents of subaxial secretions, but how the the secretions are important to N. leporinus remains unknown. Do bats distinguish the odors of other individuals? Do female groups have a distinct group odor'? Future experimental work should be considered with captive pop- ulations where diet can be both controlled and manipulated, reproductive status monitored, and subaxial secretions sampled repeatedly from the same individual over time.
FISHING BAT LIPID SECRETIONS 1427
Acknowledgments--We wish to thank M. Barnaby, A. Green, J. Howe, G. F. McCracken, D. Ridley, D. Simard, and T. Tallavast for assistance in the field. The staff of the Caribbean office of the United States National Wildlife Refuge and the United States Fish and Wildlife Service generously aided with logistical problems. G. McCracken, G. Gittleman, A. Green, and two anon- ymous reviewers offered helpful comments on the manuscript. Financial support for this research was provided to A. Brooke by a National Institute of Health Predoctoral traineeship to the University of Tennessee, the Theodore Roosevelt Fund of the American Museum of Natural History, the American Society of Mammalogists, the Animal Behavior Society, and the University of Tennessee Ethology Program.
REFERENCES
BRADBURY, J., and EMMONS, L. H. 1974. Social organization of some Trinidad bats. I. Emballon- uridae. Z. Tierpsychol. 36:137-183.
BROOKE, A. P. 1994. Ecology of the fishing bat, Noetilio leporinus. PhD dissertation. University of Tennessee, Knoxville, Tennessee.
BROWN, R. E. 1979. Mammalian social odours: A critical review. Adv. Study Mammal. Behav. 10:103-162.
BUCHLER, E. R. 1980 Evidence for the use of a scent post by Myotis lucifigus. J. Mammal. 61:525- 528.
DAvis. D. E., HERREID, C. F., II, and SHORT, H, L. 1962. Mexican free-tailed bats in Texas. Ecol. Monogr. 32:311-346.
DECKER, D. M., RINGELBERG, R., and WHITE, D. C. 1992. Lipid components in anal scent sacs of three mongoose species (Helogale parvula, Crossarchus obscurus, Suricata suricatta). J. Chem. Ecol. 18:1511-1524.
DUNN, L. H. 1934. Notes on the little bulldog bat, Diras ulbiventer minor (Osgood). in Panama. J. Mammal. 15:89-99.
DUSENBER¥, D. B. 1992. Chemical ecology. W. H. Freeman, New York, 558 pp. EBUNr, F. J. 1977. Hormonal control of mammalian skin glands, p 17-22. in D. Muller-Schwar-ze
and M. M. Mozell (eds.). Chemical Signals in Vertebrates. Plenum Press, New York, 609 pp.
GOODWIN, G. G. 1928. Observations on Noctilio. J. Mammal. 9:104-113. GOODWBN. G. G., and GREENHALL, A. M. 1961. A review of the bats of Trinidad and Tobago.
Bull. Am. Mus. Nat. Hist. 122:187-302. GRANT, G., and BANACK, S. A. 1995. Harem structure and reproductive behavior of Pteropus
tonganus in American Samoa. Dept. Mar. Wild. Res. Biol. Rept. 69:1-30. GUDGER. E. W. 1945. Fisherman bats of the Caribbean region. J. Mammal. 26: 1-15. HERREID, C. F., II. 1960. Comments on the odors of bats. J. Mammal. 41:396.
LASKA, M, 1990. Olfactory sensitivity to food odor components in the short-tailed fruit bats, Carollia perspicillata (Phyllostomatidae, Chiroptera). J. Comp. Physiol. A 166:395-399.
LASKA, M., and SCHMiDT, U. 1986. Untersuchungen zur olfaktorischen Orientierung bei der Bril- lenblallnase, Carollia perspicillata (Chiroptera). Z. S?iugetierkd. 51 : 129-138.
MACDONALD, D. W. 1985. The carnivores: Order Carnivora, pp. 619-722. in R. E. Brown and D. W. Macdonald Social Odours in Mammals. Vol. 2. Oxford University Press, Oxford.
MCCRACKEN, G. F., and GUSTIN, M. K. 1991. Nursing behavior in Mexican free-tailed bat mater- nity colonies. Ethology 89:305-321.
NELSON, J. E. 1965. Behavior of Australian Pterupodidae (megachiroptera). Anita. Behav. 13:544- 575.
1428 BROOKE AND DECKER
RATCLIFF, F. N. 1932. Notes on the fruit bats (Pteropus spp.) of Australia. J. Anita. Ecol. 1:32-57.
ROHLF, F. J. 1987. Numerical Taxonomy and Multivariate Statistical Analysis lot the IBM-PC. Applied Biostatistics, Inc.
Ruscl-ll, A. 1951. Morcegos do Espirito Santo. Bol. Mus. Biol. Zool. 7:1-11. SCriM]Dr, U. 1985. The bats: order Chiroptera, 217-234. in (R. E. Brown and D. W. Macdonald
(eds.). Social Odours in Mammals. Clarendon Press, Oxford.
SCHMroT. U., and MANSKE, U. 1973. Die jugendentwicklung der vampirfledermause (Desmodus rotundus). Z. Vergl. Physiol. 74:217 226.
SCHNITZLER, H., KALKO, E. K. V., KAIPF, I., and GRINNELL. A. D. 1994. Fishing and echolocation behavior of the greater bulldog bat, Noctilio leporim~s, in the field. Behav. Ecol. Sociobiol. 35:327-345.
STUDtER, E. H., and LAVOIE, K. H. 1984. Microbial involvement in scent production in nocti[ionid bats. J. Mammal. 65:711-714.
THOMAS, D. W., FENTON, M. B., and BArCLaY, R, M. B. 1979. Social behaviour of the little
brown bat, Myotis lucifigus. I. Mating behavior. Behav. Ecol. S~ciobiol. 6:129-136. V,XLDIWESO, D., and Tamsrr-r, J. R. 1964. The histology of the chest gland of the pale spear-nosed
bat. J. Mammal. 45:536-539. WErNEr, H. J., and LAY, D. M. 1963. Morphologic aspects of the chest gland of the bat. Molossus
ater. J. Mammal. 44:552-555. WHITE, D. C., Davis, W. M.. NICKEL'.', J. S., and BonniE, R. J. 1979. Determination of the
sedimentary microbial biomass by extractable lipid phosphate. Oeeolngia. 40:51-62.
