CHEMICAL PROFILES OF MALE AFRICAN ELEPHANTS,
LOXODONTA AFRICANA: PHYSIOLOGICAL AND
ECOLOGICAL IMPLICATIONS
L. E. L.
RASMUSSEN, ANTHONY
J.
HALL-MARTIN, AND DAVID
L.
HESS
Department of Chemistry, Biochemistry, and Molecular Biology,
Oregon Graduate Institute of Science & Technology, Portland, OR 97291-1000 (LELR)
South Parks, National Parks of South Africa, Cape Town, South Africa (AH-M)
Division of Reproductive Sciences, Oregon Regional Primate Center, Beaverton, OR 97006 (DLH)
This study reports concentrations of testosterone and dihydrotestosterone in both serum and
temporal-gland secretions of male African elephants (Loxodonta africana), including radiocollared elephants, and identifies a spectrum of volatile components in the temporalgland secretions. Androgens in the serum (testosterone and dihydrotestosterone) were measured in 111 adult male African elephants, ages 21-40 years, from two national parks in
South Africa during several years and seasons. About one-fifth (18.6%) of these mature,
male, African elephants exhibited dramatically increased concentrations of testosterone in
serum characteristic of male Asian elephants during musth. In Kruger National Park, six
radiocollared male African elephants, ages 25-35 years, were tracked and serially sampled
for both serum and temporal-gland secretions during a 5-year period. Concentrations of
testosterone in serum and temporal-gland secretions were elevated cyclically at times when
typical musth behaviors, including aggression, were observed. This study reports the first
chemical characterization of the volatile compounds of the temporal-gland secretions from
male African elephants in musth. It reveals many similarities between the chemical constituents of the temporal-gland secretions of these male African elephants and the compounds identified in male Asian elephants. In addition, several compounds, not previously
identified in temporal-gland secretions of African elephants, are described. Such chemical
data support the behavioral observations by ourselves and other researchers that male African elephants experience musth. Especially convincing are the concurrent hormonal and
chemical data from the radiocollared males during episodic periods of behavioral musth.
Implications of the incidence of musth in the past and present ecology of African elephants
are discussed in view of the increasing compression within national parks.
Key words: Loxodonta africana, musth, temporal-gland secretions, serum, testosterone,
dihydrotestosterone, radiocollar, organic-solvent-soluble volatiles
In recent years throughout Africa, the elephant, Loxodonta africana, has been increasingly contained within the confines of
national parks. Male elephants, especially,
may present management problems, including direct conflict with humans. Knowledge
of the behavior and physiology of these
unique mammals is of basic biological interest and has the potential to contribute to
more effective management strategies.
Field observations by early explorers,
hunters, and even managers of lumber
Journal of Mammalogy, 77(2):422-439, 1996
camps did not describe musth (a period
characterized by radical behavioral
changes, including an increase in aggressiveness and dominance displays, and by
physiological and biochemical events including temporal-gland secretions) in the
African elephant. Anecdotal and fragmentary mention of musth among captive male
African elephants has been reported. These
reports are increasing in frequency, apparently as more male African elephants are
maintained in captivity (Brannian et aI.,
422
May 1996
RASMUSSEN ET AL.-CHEMISTRY OF MUSTH IN ELEPHANTS
1989; Cooper et aI., 1990). Recently, behavioral observational studies in the wild
(Hall-Martin, 1987; Poole, 1989; Poole et
aI., 1984) have shown that male African elephants, like males of their different-genera
relatives, the Asian elephant, Elephas maximus, experience episodes of musth, often
exhibiting aggressive behaviors. Specifically, close observations of individually identified males have revealed aggressive and
associated dominance behaviors (Hall-Martin, 1987). These observations and limited
chemical measurements (Poole et aI., 1984;
Rasmussen et aI., 1990) have demonstrated
that a certain proportion (Hall-Martin and
van der Walt, 1984) of male African elephants exhibit a musth-like state.
In contrast, the unusual physiological and
behavioral state of musth occurring in male
Asian elephants, both wild and captive, has
been observed and studied for centuries
(Edgerton, 1931). Only the males exhibit
musth, while the female Asian elephants
seldom secrete from their temporal glands
(Rasmussen, 1988, 1994). Recent chemical
studies, such as measurements of concentrations of steroid hormones in serum and
temporal-gland secretions, have expanded
our knowledge of musth (Jainudeen et aI.,
1972a, 1972b; Niemuller and Liptrap,
1991; Rasmussen, 1988; Rasmussen et aI.,
1984, 1990, 1994a). However, even in this
species, many behavioral and physiological
aspects of musth remain elusive (Schmidt,
1989). The biological rationale of musth
and its control by the central nervous system remain poorly understood. The musthlike state described in selected male African
elephants appears to have behavioral and
physiological similarities to classically described musth in male Asian elephants.
With the emergence of behavioral descriptions of a similar condition in some
male African elephants (Hall-Martin, 1987;
Poole, 1989), the chemical analyses of the
serum and temporal-gland secretions, both
in a large-sample population, and in individual elephants monitored periodically
over a number of years, would offer rea-
423
sonable data for the comparison of musth
in these two genera of elephants. The present three-part study provides chemical evidence, including the first chemical analyses
of temporal-gland secretions from male African elephants in musth, supporting this
hypothesis.
Our first goal was to determine concentrations of testosterone and dihydrotestosterone in serum in large-sample populations
of adult, male African elephants. Previous
studies on values of hormones in serum
have only reported on small numbers of animals (Hall-Martin and van der Walt, 1984;
Rasmussen et aI., 1984). The present large
database reduced sample biases resulting
from small samples and provided more statistically substantiated data. The addition of
chemical data to behavioral observations of
musth-like behavior allowed more precise
assessment of the percentage of males experiencing musth. Second, we wanted consecutive samples from individual elephants
as well as concurrent chemical data on serum and temporal-gland secretions. Serial
samples of blood and temporal-gland secretions from individual, radiocollared, male
African elephants allowed us to achieve this
goal. Our study was in coordination with a
long-term behavioral and ecological study
involving the relationships between clans
and bachelor herds (Hall-Martin, 1987). We
measured concentrations of androgen and
identified and quantified volatile compounds in temporal-gland secretions from
these male elephants.
In the male Asian elephant, secretions of
temporal-glands are chemically unique with
high concentrations of testosterone and dihydrotestosterone and characteristic volatile
compounds, as demonstrated by gas-chromatographic analyses (Rasmussen, 1988;
Rasmussen et aI., 1984, 1990). In the third
part of this study, we present the first chemical analyses of temporal-gland secretions
of male African elephants in musth, using
gas-chromatographic-mass-spectrometric
techniques. A decade ago we described the
few, dominant, chemical components of
JOURNAL OF MAMMALOGY
424
temporal-gland secretions of female African
elephants and male African elephants not in
musth (Wheeler et aI., 1982). Now, we describe numerous, new compounds in the
temporal-gland secretions of male African
elephants in musth and compare the gaschromatographic traces from these males
with analyses from male Asian elephants in
classic musth. In male Asian elephants in
musth, elevated concentrations of testosterone in serum and increased concentrations
of certain volatiles occur concurrently with
clearly recognized aggressive behaviors
(Rasmussen et aI., 1990; Schmidt, 1989),
although the two may not be directly, or
causally, related (M. J. Schmidt, pers.
comm.).
MATERIALS AND METHODS
Study of two large populations of male African elephants.-Elephants studied in this part of
the investigation were 21-40 years old. Ages
were known from park records for some animals, estimated by the method of Laws (1966)
for others, and some were estimated by comparison of body size and confirmed at the time they
were injected by darting (Hall-Martin and van
der Walt, 1984). One focus of this study was the
concentrations of testosterone and dihydrotestosterone in male African elephants. The levels of
these hormones in females were measured as
controls and for comparison to values of males.
The elephants studied were from two discrete
geographic popUlations, in two parks in the Republic of South Africa; Kruger National Park
(23°30/S, 31 40/E) and Addo Elephant National
Park (33°58/S, 31°40/E), two areas with distinct
differences in habitats. The majority of elephants
sampled for this study (93 of III males, 46 of
49 females) resided in Kruger National Park in
the eastern transvaal lowveld. Kruger National
Park has a unimodal peak in summer rainfall
(October-March). The quantity and quality of
available food is closely correlated to this rainfall, and in Kruger National Park these months
are the times when the maximum number of successful matings occur (Hall-Martin, 1987).
Samples were obtained from elephants in
Addo Elephant National Park in the eastern
Cape Province during 2 summers. In contrast to
Kruger National Park, Addo Elephant National
0
Vol. 77, No. 2
Park has intermittent short cycles of rainfall and
drought with no predominant season or peak
rainfall, and conceptions of elephants are spread
throughout the year.
Blood samples from 77 males and 46 females
were obtained during culling operations at Kruger National Park during January and February,
in the latter one-half of the breeding season. Additional samples (from 16 males) were taken
May-September during 2 successive winters.
Samples from 18 males and 3 females were obtained at Addo Elephant National Park during
summer over a 2-year period (1986-1987). Animals were sacrificed 0800-1200 h by overdoses
of the neuromuscular-relaxant succinylchloride.
Blood samples (2 ml) were obtained immediately from the leg vein, refrigerated, and centrifuged, after formation of clot, to obtain serum.
After subdivision into aliquots, all samples were
kept frozen until analysis. Samples of temporalgland secretions (1-3 ml) were collected in specially cleaned and modified glass syringes and
stored frozen in glass vials until analysis. From
Kruger National Park, samples of temporalgland secretions were collected from 12 males
and 7 females. Simultaneous samples of blood
and temporal-gland secretions were collected
from eight male African elephants at Addo Elephant National Park during the second summer.
Aliquots (500 JLI) of serum and temporalgland secretions were extracted with redistilled
ether and the extract sequentially chromatoc
graphed on two different Sephadex LH-20 chromatographic columns prior to analyses by radioimmunoassay (Resko et aI., 1973, 1980). The
first column (1.0 g LH-20, elution phase, hexane-benzene-methanol, 62:20: 13 volume: volume : volume) separated neutral and phenolic
steroids. The second column (2.5 g LH-20, elution phase, hexane-benzene-methanol, 85:15:5
volume: volume: volume) isolated progesterone,
dihydrotestosterone, and testosterone.
Extraction and chromatographic losses were
monitored by adding known amounts of tritiated
authentic steroids to independent samples of serum or temporal-gland secretions and processing
in parallel with the samples for assay. Recoveries following the final chromatographic step
were 72.0 and 70.0% for dihydrotestosterone
and testosterone, respectively. Water blanks also
were processed in parallel to provide solventmethod blanks for each steroid (dihydrotestosterone, 18.6 ::!:: 9.8; testosterone, 3.5 ::!:: 1.9 pg).
May 1996
RASMUSSEN ET AL.-CHEMISTRY OF MUSTH IN ELEPHANTS
Reported values were corrected for both procedural losses and method blanks before correcting
for aliquots assayed. Each sample was diluted
with 500 ILl of ethanol after chromatography and
assayed at three or four different volumes. The
reported values are the average concentration
calculated from aliquots whose values fell between the 5-95% binding limits of the standard
curve following linearization with a logistic-logarithmic transformation. Intra- and interassay
coefficients of variation did not exceed 17% for
either assay, and sensitivity limits for both the
androgens were 5 pg/tube. Further details of the
methods are presented in Hess et al. (1981) and
Resko et al. (1973, 1980).
Serial sampling of individual radiocollared
elephants.-Six male elephants, 25-35 years
old, free-roaming within the confines of Kruger
National Park, were tracked using radiocollars
for 2-5 consecutive years (1985-1989). These
animals were selected for. radiocollaring on the
basis of previously observed musth behaviors.
All males were sampled sequentially for both
serum and temporal-gland secretions. From each
male, 6-17 samples of serum or temporal-gland
secretions were obtained for a total of 75 samples of serum and 18 samples of temporal-gland
secretions. Concurrently with most samples of
serum and temporal-gland secretions, behavioral
observations were recorded (for 66 and 13 samples, respectively). Observational data were obtained most frequently at monthly intervals, with
occasional weekly data included. The timing of
sampling could not be absolutely equally spaced
throughout the year; i.e., data collections were
not possible every month for every wild, radiocollared elephant.
Monthly samples of blood and temporal-gland
secretions were obtained as follows. A radiocollared male was approached as expeditiously as
possible by helicopter between 0830 and 0930 h
and injected with the tranquilizer, MS 99 (Reckett Pharmaceuticals, Cape Town, South Africa),
by dart. After the animal was sedated, blood (2
ml) and temporal-gland secretions (1-3 ml) were
quickly obtained, as described in the previous
section. Within 45 min of the initial injection,
the male recovered substantially. All six males
survived this multiple-sampling procedure. Testosterone and dihydrotestosterone were measured in both the serum and temporal-gland secretions as outlined previously. Behavioral observations before sampling included the pres-
425
ence of temporal-gland secretions, their extent,
urine dribbling, the position of the penile sheath,
aggressive displays not associated with the approach of the helicopter, and the composition of
the population (i.e., age, gender, number, and secretions from the temporal glands) of any accompanying elephants.
During analyses, data were grouped according
to three types of associations among conspecifics occurring in the wild; alone, with other
males, or near breeding females. Further segregation of data categorized males that were, or
were not, secreting from the temporal gland.
Gas-chromatographic-mass-spectrometric
analyses of temporal-gland secretions.-We
identified and semi-quantified dichloromethanesoluble, volatile compounds from the temporalgland secretions, using the same methods as employed for analyses of temporal-gland secretions
from male Asian elephants in musth (Rasmussen
et aI., 1990). We separated the organic compounds by capillary-column, gas chromatography and identified components by gas chromatography-mass spectrometry. One-milliliter aliquots of temporal-gland secretions were thawed
and each aliquot was extracted three times at
room temperature using dichloromethane (aqueous : solvent ratio, 1:3). The combined extracts
were filtered through sodium sulfate for removal
of water before gas-chromatographic analysis.
Samples were reduced in volume of solvent under a high-purity nitrogen stream to a standardized volume (100 ILl). For all samples, three separate extracts were prepared. As initial analyses
demonstrated distinct patterns for the volatile
compounds from temporal-gland secretions, we
selected samples at three levels of testosterone
in the serum to examine in detail. Three samples
of temporal-gland secretion were extracted from
three separate male African elephants in each
category of concentrations of testosterone in serum, I ng/ml, 26 ng/ml, and 64 ng/ml, for a total
of nine samples. We present the results with respect to retention time, the time interval after
injection that components are eluted from the
column.
Extracts (0.5 ILl) were injected directly by a
fused silica needle onto a polymethyl, siliconecoated, capillary column. The column used was
a DB-I, 0.32 mm inside diameter by 60 m by
1.0 IL film thickness (J&W Scientific, Inc., Folsom, CA). The carrier gas was helium at a flow
rate of I mllmin. The gas chromatograph used
426
JOURNAL OF MAMMALOGY
for initial analyses of the extracts of temporalgland secretions was a Hewlett-Packard 5790A
with a flame-ionization detector. Makeup gases
were a 40:60% mixture of purified O 2 and N 2 •
respectively. The oven of the gas chromatograph
was programmed to initiate a warming sequence
at 35°C, increasing at a rate of 6°C/min. The
sequence required 48 min for completion and
attained a maximum temperature of 323°C. The
output of the flame-ionization detector was processed via a Hewlett-Packard 3392 integrator.
Standards used during the on-column, capillary-column, gas-chromatographic analyses included compounds identified in temporal-gland
secretions by gas chromatography-mass spectrometry (Rasmussen, 1988; Rasmussen et aI.,
1984, 1990; Wheeler et aI., 1982). Standards
were used both separately and as internal standards. These reference compounds included phenol, 4-methylphenol, propylphenol, E(trans)-farnesol (3,7, II-trimethyl-2,6, 10 dodecatrien-l-ol),
farnesol monohydrate, and farnesol dihydrate.
Initial identification was made on the basis of
retention times relative to those of these standards. Quantitative comparisons were obtained
through peak-integration routines (HewlettPackard 5792). All samples were analyzed in
triplicate; the data were analyzed statistically for
reproducibility of 3%. This employment of highresolution and precise analyses by on-column,
capillary column, gas chromatography allowed
the relative quantitation of volatile compounds.
Chromatograms of each of the three extracts
from individual elephants were compared within
each of three groups based on concentrations of
testosterone in serum. Within groups, the chromatograms were virtually identical. Therefore, a
representative chromatogram was selected from
each group. As the method is semi-quantitative,
statistical analyses were not conducted between
samples of elephants.
After the screening analyses by gas chromatography, more specific analyses were obtained
with a gas-chromatographic-mass-spectrometric
system. While quantitative comparisons were
obtained through peak-integration routines,
identification of the constituents of specific profiles was accomplished by gas chromatographymass spectrometry. Conditions for gas chromatography for the analyses by gas chromatography-mass spectrometry were identical to those
used for the routine, gas-chromatographic analyses. Analyses were performed on a VG 7070
Vol. 77. No.2
E-HF, double-focusing, mass-spectrometer system using electron-impact ionization at 70 eY.
The mass spectrometer was equipped with an
111250 data system. The library of chemical
compounds of the National Bureau of Standards,
with amended additions, was used in computer
searches involving identification of compounds.
Both the library information and retention times
of gas chromatography with authentic samples
were used for identification. Selected compounds were manually re-checked with National
Institutes of Standards and TechnologylEnvironmental Protection AgencylNational Institutes of
Health Mass Spectral Data Version 4.0 (Standard Reference Data Program, National Institutes of Standards and Technology, United
States Department of Commerce, Washington,
D.C.). Concentrations were estimated both by
use of authentic standards and by relative peak
areas.
Data were analyzed statistically by several
methods. Means, standard deviations, and standard errors were calculated for hormonal data
where appropriate. Data that met the criteria for
parametric statistics were analyzed and compared by standardized t-tests. Nonparametric
data that failed the Kolmogorov-Smirnov test of
normality (Sokal and Rohlf, 1981) were analyzed and compared by Kruskal-Wallis one-way
analysis of variance (ANOVA) on ranks. Results
that were significant (P < 0.05) were then analyzed using either a Mann-Whitney rank-sum
test or Dunn's method for pairwise multiple
comparisons (Dunn, 1964) to isolate any group
that was significantly different. Determinations
of whether two variables were correlated were
determined by Pearson product-moment or
Spearman rank-order correlation coefficients
(Downie and Heath, 1965). Two-way ANOVA
was conducted on data with several factors. Factors that varied significantly were subjected to
multiple pairwise comparison using the StudentNeuman-Keuls test and the Bonferroni t-test (for
few groups). Sigma Stat statistical program was
used (Jandell Scientific, Corte Madera, CA).
RESULTS
Concentrations of testosterone and dihydrotestosterone in serum of African elephants.-Concentrations of testosterone in
the serum were significantly higher, although the ranges overlapped, in males than
May 1996
RASMUSSEN ET AL.-CHEMISTRY OF MUSTH IN ELEPHANTS
427
TABLE I.-Concentration of testosterone in serum of African elephants 21-40 years old from two
national parks. For comparison, ranges of concentration of testosterone are shown for Asian elephants in musth and not in musth (Rasmussen et aI., 1984, 1990).
Males
n
X±
I SE
Females
Range
n
X ± 1 SE
Range
46
0.20 ± 0.04h
0.02-1.60
3
0.80 ± 0.40b
0.10-1.50
African elephants
Summer
Kruger National Park
Addo National Park
Year I
Year 2
77
11.7 ± 2.8'
0.1-144.8
10
8
19.1 ± 6.1'
29.8 ± 9.6'
1.1-72.0
6.6-74.6
10
6
2.1 ± 0.5'
37.7 ± 19.7'
0.4-6.6
2.8-109.0
20
8
20
3.1 ± 0.4
11.9 ± 1.5
62.7 ± 6.1
Winter
Kruger National Park
Year I
Year 2
Asian elephants
Nonmusth
Premusth
Musth
a.b.,
0.1-5.4
4.3-17.6
19.0-125.0
Similar superscripts indicate means that are not statistically different.
in females in the summer months of January and February in Kruger National Park
(Mann-Whitney rank-sum tests, P < 0.001;
Table 1). For dihydrotestosterone, the actual
concentrations ranged in males from 0.01
to 38.02 ng/ml (mean ± 1 SE is 3.03 ±
0.83), and in females from 0.01 to 0.43 ng/
ml (0.06 ± 0.01). In males and females,
concentrations of testosterone were significantly higher than levels of dihydrotestosterone (Mann-Whitney rank-sum tests, P <
0.001). Concentrations of dihydrotestosterone were significantly higher in males than
in females (Mann-Whitney rank-sum tests,
P < 0.001).
In Kruger National Park, the 16 male African elephants sampled during 2 winter
seasons (10 males the 1st season, 6 different
males the 2nd season) had ranges of concentrations of testosterone that were similar
to those of elephants sampled in summer.
There was no significant difference between
the summer group and the group from the
1st winter (Mann-Whitney rank-sum tests,
P = 0.452; Table 1). However, the levels in
the 10 males sampled the 2nd winter were
significantly higher than in those sampled
the 1st winter (Mann-Whitney rank-sum
tests and Kruskal-Wallis one-way ANOVA
on ranks, pairwise comparison by Dunn's
method, P < 0.001), and higher than those
sampled in summer (P < 0.046). Levels of
dihydrotestosterone in the males from Kruger National Park during the 1st winter
ranged from 0.09 to 1.41 ng/ml. There was
no significant difference between these levels of dihydrotestosterone and those of the
summer group of males. Again levels of
dihydrotestosterone were significantly lower than levels of testosterone (P < 0.001).
At Addo Elephant National Park, there
was no significant difference in concentrations of testosterone in serum of 18 male
African elephants (10 males the 1st summer, 8 different males the 2nd summer)
sampled during 2 summers (P = 0.230).
Concentrations of testosterone in males
from Addo Elephant National Park in both
summers were significantly higher than in
males from Kruger National Park during
summer (Mann-Whitney rank-sum tests, 1st
and 2nd summers, respectively, P < 0.004
and 0.002). Although concentrations in elephants from Addo Elephant National Park
JOURNAL OF MAMMALOGY
428
Vol. 77, No.2
TABLE 2.-Percentages of male and female elephants in Kruger National Park in summer exhibiting various categories of concentrations of testosterone in serum.
Category
II
III
IV
IV
IV
IV
IV
A
B
C
D
E
Testosterone
(ng/m!)
<0.1
0.1-1.0
1.0-2.0
2.0-10.0
11.0-20.0
21.0-50.0
51.0-100.0
>100
Males
Status
nonmusth
nonmusth
nonmusth
possibly premusth, postmusth
premusth, postmusth
musth
heavy musth
very heavy musth
in both summers were significantly higher
than the elephants from Kruger National
Park in the I st winter, these two groups in
Addo Elephant National Park did not differ
significantly from the elephants from Kruger National Park in the 2nd winter (nonparametric data tested by Kruskal-Wallis
one-way ANOVA on ranks).
Range in testosterone in serum from female African elephants from two locales
was 0.02-1.6 ng/ml and did not differ statistically from each other (Mann-Whitney
rank-sum test). Among elephants from
Addo Elephant National Park, levels in females were significantly lower than levels
in males, both in the 1st summer and the
2nd summer (Kruskal-Wallis one-way analysis of variance on ranks, Dunn's method,
or Mann-Whitney rank sums, P < 0.007, P
< 0.012).
Elephants from Kruger National Park,
sampled in summer, were categorized into
four groups, based on their concentrations
of testosterone in serum (Table 2). Group
IV was further divided into five subgroups.
Concentrations of testosterone in serum
were lower in females in Kruger National
Park than in males. Most females (66% of
46) had concentrations <0.1 ng/ml, and all
had levels <2 ng/mI. By contrast, all males
(n = 77) had levels >0.1 ng/ml; 54% had
concentrations >2 ng/ml, and most (33% of
77) were in the range of 2-10 ng/mI. In
21 % of the male elephants, levels of testosterone in serum were 2:: 11 ng/ml (subgroups IV B-E). Of the males in Group IV
Females
(%)
(%)
0
36.0
10.0
33.0
6.5
8.0
5.1
1.4
66.6
28.6
4.8
0
0
0
0
0
B, 6.5% had levels of testosterone in serum
equivalent to levels measured before or after musth in Asian elephants, whereas
14.5% of the mature males had elevations
of testosterone in serum 2::21 ng/ml, equivalent to moderate or heavy musth in male
Asian elephants (Jainudeen et aI., 1972a,
1972b; Rasmussen et aI., 1990). These samples were obtained during the summer
months of January and February, months
that encompassed about one-half of the
breeding season.
Concurrent measurements of hormones
in serum and temporal-gland secretion.Samples of serum and temporal-gland secretions were obtained at the same time
from a number of elephants. Data from
eight males from Addo Elephant National
Park are listed in Table 3. In addition, three
females from Kruger National Park had
concentrations of testosterone in serum of
1.0-1.6 ng/ml (X = 1.1 ng/ml), and concentrations of testosterone from temporalgland secretions of 0.01-0.70 ng/ml (X =
0.10 ng/ml). Concentrations of testosterone
from the temporal-gland secretions in the
few males measured from Kruger National
Park ranged from 0.89 ng/ml to 3,632 ng/
ml (X = 3.6 fLg/ml). The group of eight
concurrently sampled males from Addo Elephant National Park demonstrated considerable variability in concentrations of hormones in the temporal-gland secretions (Table 3). However, a moderate and positive
correlation was demonstrated between the
concentrations of testosterone in serum and
May 1996
RASMUSSEN ET AL.-CHEMISTRY OF MUSTH IN ELEPHANTS
TABLE 3.-Relation between concentration of
testosterone in the serum and in temporal-gland
secretions in eight male elephants (measured
during the 2nd summer in Addo Elephant National Park).
Concentration
(ng/ml) of
testosterone
CateTemporalgory
Num- (from
gland
ber Table 2) Serum secretion
2
3
4
5
6
7
8
X
SE
IV A
IV A
IV B
IV C
IV C
IV C
IVD
IVD
6.6
9.4
10.8
21.6
22.0
23.0
71.0
74.6
29.6
9.6
26.6
0.5
2.0
0.9
3.3
5.8
64.4
501.0
75.6
61.3
Concentration
(ng/ml) of
dihydrotestosterone
Temporalgland
Serum secretion
2.0
0.3
1.8
1.6
3.8
12.7
10.2
25.0
7.2
2.9
50.1
0.8
3.2
1.6
9.8
14.6
73.7
610.0
95.5
74.1
temporal-gland secretions (r = 0.748, P <
0.033), as well as for concentrations of dihydrotestosterone (r = 0.91, P < 0.002).
Comparisons, in these same males, of
concentrations of testosterone and dihydrotestosterone in serum and temporal-gland
secretions demonstrated only one statistically significant difference. Levels of testosterone in serum were consistently and
significantly higher than levels of dihydrotestosterone (Mann-Whitney rank-sum
tests, P < 0.014). In contrast, there were no
statistically significant differences between
levels of testosterone and dihydrotestosterone, despite the consistently higher levels
of dihydrotestosterone than of testosterone
in all samples of temporal-gland secretions
(Mann-Whitney rank-sum tests and Kruskal-Wallis one-way ANOVA on ranks, P =
0.323). No significant differences were observed between levels of testosterone in serum and temporal-gland secretion (P =
0.117), or between levels of dihydrotestosterone in serum and temporal-gland secretions (P = 0.164).
Relationships between testosterone and
dihydrotestosterone, and concentrations in
429
serum and temporal-gland secretions for all
the samples, as analyzed both by Pearson
product-moment correlation and Spearman
rank-order correlation, demonstrated several positive correlations. A strong positive
correlation was apparent between concentrations of dihydrotestosterone in serum and
temporal-gland secretion (r = 0.910, P <
0.002; r = 1.000, respectively, for Pearson
and Spearman correlation coefficients).
Both Pearson and Spearman correlation coefficients demonstrated a strong positive
correlation in the temporal-gland secretion
between testosterone and dihydrotestosterone (Pearson, r = 0.999, P < 0.001). A
moderate, positive linear relationship was
observed between the two levels of testosterone in serum and temporal-gland secretions (r = 0.748, P < 0.033), between testosterone in serum and dihydrotestosterone
in serum (r = 0.897, P < 0.003), and between testosterone in serum and dihydrotestosterone in the temporal-gland secretion
(r = 0.740, P < 0.035). Apparently, levels
of testosterone and dihydrotestosterone in
the serum and temporal-gland secretion are
positively correlated.
Serial sampling of radiocollared male
African elephants.-All six free-roaming
male elephants, tracked by radiocollars and
sampled sequentially for several years,
demonstrated periodic elevations in concentrations of testosterone and dihydrotestosterone in serum. These elevations were not
synchronous among animals. Individual
males appeared to have some degree of
year-to-year rhythmicity. In 66 of 75 samples of serum and 13 of 17 samples of temporal-gland secretion, behavioral data were
obtained. Of these samples of serum, 35
(53%) were obtained from December
through April, and 31 (47%) from May
through November. A higher percentage of
elevation of testosterone occurred during
May through November. Fourteen samples
of 35 (40%) were elevated in the December-April period, whereas only eight of 31
samples (25%) were elevated during MayNovember. Males showed cyclic peaks in
430
Vol. 77, No.2
JOURNAL OF MAMMALOGY
levels of testosterone in serum, with the
peaks occurring in all months except May
and June, and intervals between peaks in
individuals ranging from 1 to 12 months
with a mode of 7 months.
Concurrent data from field observations
and on concentrations of testosterone and
dihydrotestosterone in serum and, on occasion, levels of testosterone in temporalgland secretions from these six males, are
summarized in Table 4. Concurrent elevations of testosterone and dihydrotestosterone were observed in serum and temporalgland secretions of these wild, free-roaming
males (Table 4). This observation was consistent with the simultaneous elevation of
hormones in the serum and temporal-gland
secretions of single-sampled elephants presented in Table 3. Conspecifics for males
either were alone, associating with male
conspecifics, or associating with female
conspecifics, and they either were or were
not secreting from the temporal gland. The
categorizing of 66 observations of conspecific associations of males with concurrent,
serum-hormone assays demonstrated that
about one-half of the males were solitary
(50%) and about one-third (36%, 24 of 66)
were near other males, whereas only 14%
(nine of 66) were near breeding females.
Among lone males, about one-third (36%,
12 of 33) were secreting from their temporal glands, whereas only a relatively
small percentage (12.5%, three of 24) of
males near other males were secreting. In
contrast, 44% of males near females were
secreting from their temporal glands.
Levels of testosterone In serum were
compared among the three groups of males
secreting from their temporal glands. The
highest levels of testosterone in serum were
observed among males that were secreting
and were either alone or near breeding
herds (Table 4). There was no statistically
significant difference between these two
groups by two-way ANOVA using the multiple-comparison, Bonferroni t-test. However, concentrations of testosterone in serum were significantly lower in males that
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May 1996
RASMUSSEN ET AL.-CHEMISTRY OF MUSTH IN ELEPHANTS
were secreting, and that were near other
males, than in the other two groups of
males that were secreting, those near females (t = 3.069), and those alone (t =
3.085, two-way ANOVA, P < 0.05). Numbers of samples in the group near other
males and the high variance in these samples did not permit statistics on samples of
temporal-gland secretion. The few statistical tests allowable did not reveal any differences among the groupings of temporal
glands.
Concentrations of dihydrotestosterone in
serum of males that were secreting and that
were located near females were statistically
significantly higher than levels of serum in
males in the following four groups: secreting males near other males; non-secreting
males alone; near males; near females (multiple-comparison, Bonferroni t-tests, t =
3.960, 3.415, 3.762, 3.976, respectively, P
< 0.05).
Statistical examination of significant differences between levels of testosterone or
levels of dihydrotestosterone between these
nine groups demonstrated only three valid
differences. Levels of testosterone were significantly higher in males that were secreting than in those not secreting (P < 0.001),
dihydrotestosterone in serum also was higher in males that were secreting than in the
non-secretors, and the lone males that were
secreting had higher concentrations of testosterone than dihydrotestosterone.
Figure 1, depicting concentrations of testosterone in serum and temporal-gland secretion in a single male elephant throughout
several years, is a unique dataset from a
wild male elephant. Data from other, radiocollared, male elephants were similar. The
most complete set of data (from elephant
9880) showed that, during 3 successive
years, levels of testosterone in serum and
temporal-gland secretion during musth
were high during January (Fig. 1). Levels
of testosterone in temporal-gland secretion
were elevated primarily when testosterone
in serum was elevated.
Analyses of gas chromatography and
431
mass spectrometry of volatile compounds
from temporal-gland secretions.-The volatile compounds, soluble in dichloromethane, in the temporal-gland secretions of
male African elephants were compared at
three levels of testosterone in serum (i.e., 1
ng/ml, nonmusth; 26 ng/ml, musth; 64 ng/
ml, heavy musth; Fig. 2). These chromatograms are representative of three samples of
secretion from three different elephants for
each of three levels of testosterone in serum
(i.e., low, high, and very high concentrations of testosterone). Qualitatively and
quantitatively, the compounds in temporalgland secretions differed with varying levels of testosterone in serum. As these analyses are only semi-quantitative, the
amounts (i.e., peak areas) of the compounds
are depicted relative to the highest concentration of testosterone, 64 ng/ml, set at
100% (as in the lower graph in Fig. 2). At
low levels of testosterone in serum (1 ng/
ml), the pattern was similar to that reported
by Wheeler et al. (1982), including phenol,
4-methylphenol, famesol, fame sol monohydrate, famesol dihydrate with the addition
of several other identified compoundsbenzoic acid, phenylpropanoic acid, 2-npropylphenol, 4-n-nonylphenol, hexadecanoic acid (Fig. 2), tetradecanoic acid, and
pentadecanoic acid (not depicted).
At levels of 26 ng/ml of testosterone in
serum, concentrations of 5-nonanol, 2-nonanone, and 3-nonen-2-one were substantial.
In addition, phenol decreased, several other
phenols increased, hexadecanoic acid increased, and 4-hexanoic acid was detected.
At the level of 64 ng/ml of testosterone,
levels of 5-nonanol and hexadecanoic acid
were even higher. Cyclohexanol appeared
as a prominent compound. Proportionally
the farnesols were reduced (Fig. 2).
Close examination of the volatile components, soluble in an organic solvent, from
temporal-gland secretions of male African
elephants with high levels of testosterone,
revealed that most of the compounds identified had been described previously in temporal-gland secretions from male Asian el-
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Vol. 77, No.2
JOURNAL OF MAMMALOGY
432
•
:-/•
G>
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0
o
5
10
15
20
25
30
serum
•
35
Months
FIG. l.--Cycles in concentration of testosterone in serum of a representative male African elephant,
showing the relationship of elevated testosterone in serum to elevated testosterone in secretions of
the temporal gland; simultaneous low levels of serum and testosterone of the temporal-gland secretion
are seen in March of year 2 and August of year 3. Samples were obtained for 35 months starting in
December 1987. Circles are values of serum, squares are values for temporal-gland secretions.
ephants in musth (Rasmussen et aI., 1990).
The exceptions included cyclohexanol, farnesol monohydrate, and farnesol dihydrate,
which appear to be unique to the African
elephant. However, only 16 compounds
were resolved in the temporal-gland secretions of African elephants, as compared to
the >23 major and 16 minor compounds
previously described in the temporal-gland
secretions of male Asian elephants (Rasmussen et aI., 1990).
DISCUSSION
There were similarities and differences in
concentrations of testosterone in the two
species of elephants. First, the observed
similarity in concentrations of testosterone
in serum provides hormonal evidence of the
May 1996
RASMUSSEN ET AL.-CHEMISTRY OF MUSTH IN ELEPHANTS
100
(a)
13
80
60
E
80
.5
60
CD
c
2
SII)
7
4
5
1
10 11
*
*
15
*
100
2CD
II)
14
3
40
-:I
433
(b)
3
7
10
2
40
5
16
12
6
9
20
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S
'0
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o
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100
CJ
80
16
(c)
CD
C
oCJ
~
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G)
a:::
12
60
*11
2
40
6
20
o
o
5
10
15
20
25
30
35
Retention time (min)
FIG. 2.-Relative concentrations of compounds identified in dichloromethane extracts of temporalgland secretions from male African elephants with three concentrations of serum testosterone at (a)
1.0 ng/ml, (b) 26.4 ng/ml, and (c) 64.0 ng/ml. Compounds are 1) phenol, 2) 5-nonanol, 3) 4-methylphenol, 4) benzoic acid, 5) phenylpropanoic acid, 6) 2-nonanone, 7) 2-n-propylphenol, 8) 4-hexanoic acid, 9) 3-nonen-2-one, 10) 4-n-nonylphenol, 11) cyclohexanol*, 12) hexadecanoic acid, 13)
E-farnesol, 14) farnesol monohydrate*, 15) farnesol dihydrate*, 16) testosterone. Compounds with
an asterisk were only detected in temporal-gland secretions of male African elephants, not male
Asian elephants in musth. Retention time is the time it takes each component to pass through the
chromatographic column. The Y-axis is set at 100%, equated to a concentration of testosterone in
temporal-gland secretions of 64 ng/ml.
Vol. 77, No.2
JOURNAL OF MAMMALOGY
434
(8)
~S~s
--E-
1,000.00
C)
c
I I)
c 100.00
e
sen
.sen
S
c
0
~
....
c
1.00
0
-
1,000.00
E
c;,
-e
c
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c 100.00
s
.senen
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10.00
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c
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u
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c
u
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c
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0
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NM
S
S
0.10
0
tgs
0.01
B
tgs
~S
0.01
Asian
African
Males
Asian
African
Females
FIG. 3.-Concentrations of testosterone in serum and temporal-gland secretions of African and
Asian elephants. Musth (M), incipient musth or pre-musth (P-M), and nonmusth (NM) conditions
are indicated for male Asian elephants. Some of the data on Asian elephants are from Rasmussen
(1988, 1994) and Rasmussen et al. (1984, 1990). Some data are non-parametric and therefore expressed as median and percentiles and plotted as box plots. The lines of the box plot mark the 10th,
25th, 50th, 75th and 90th percentile points in the data. The box encompasses the 25-75th percentiles;
its lower boundary indicates the 25th percentile, the line within the box marks the median, and its
upper boundary indicates the 75th percentile. The 5th and 95th percentiles are shown as circular
symbols below and above the 10th and 90th percentiles, respectively. Samples of temporal-gland
secretions are indicated by tgs and serum samples by S.
similarity of musth in the two species.
When male Asian elephants that are musth
and nonmusth were considered together,
concentrations of testosterone in serum
ranged ca. 100X (Fig. 3). Male African elephants exhibited a 1,000X variation and
overlapped considerably with reported levels in male Asian elephants (Fig. 3). Male
Asian elephants in heavy musth had concentrations of testosterone in serum of >20
ng/ml, whereas males in moderate musth or
post-musth often had levels of 10-20 ng/ml
(Jainudeen et al., 1972a; Rasmussen et al.,
1984, 1990). One male Asian elephant,
studied during a 4-month, single-musth episode, had concentrations of testosterone in
serum during the 1st 2 quarters (59 days)
of 40-126 ng/ml, whereas in the 3rd quarter
it had levels of 26-74 ng/ml, and during the
last quarter it had levels of 10-24 ng/ml
(Rasmussen et aI., 1990). Using the criteria
from these reports, concentrations of testos-
May 1996
RASMUSSEN ET AL.-CHEMISTRY OF MUSTH IN ELEPHANTS
terone in serum of >20 ng/ml can be considered heavy musth, and concentrations of
10-20 ng/ml are indicative of either incipient or declining periods of musth. In Kruger National Park, 14.5% of males had concentrations of testosterone in serum equivalent to those of male Asian elephants in
moderate or heavy musth (Table 2), whereas 62.5% of the eight male elephants from
Addo Elephant National Park sampled the
2nd summer had musth levels of testosterone in serum (Table 3). However, using the
criteria of elevated testosterone in temporalgland secretion, as reported for Asian elephants (Rasmussen et aI., 1990), only
37.5% of these males from Addo Elephant
National Park were in the musth category
(Table 3). Interestingly, in this same group,
concentrations of dihydrotestosterone were
elevated (X = 7.2 ± 2.9 ng/ml) in a fashion
similar to the periodic elevations of dihydrotestosterone during musth in Asian elephants (3.9 ± 0.6 ng/ml-Rasmussen et aI.,
1990).
Concentrations of testosterone in temporal-gland secretions were not significantly
different in male and female African elephants (P = 0.296); however, levels of testosterone in temporal-gland secretions in female Asian elephants were significantly
lower than for all other groups (P < 0.005;
Fig. 3). Although data from temporal-gland
secretions of male African elephants were
not segregated into musth and nonmusth
groups, the degree of male-female overlap
was striking among African elephants, suggesting a more gradated phenomenon in
this species (Fig. 3).
The six serially sampled, radiocollared,
male elephants had elevations of testosterone in serum >20 ng/ml on either a seasonal, biannual, or annual basis, more frequently between December and April (Fig.
1). Observations of concurrent behaviors
showed that, during these periods of high
levels of testosterone in serum, the males
tended to be solitary and often exhibited aggressive behaviors. In plantation and captive male Asian elephants (Jainudeen et aI.,
435
1972a, 1972b; Rasmussen, 1988; Rasmussen et aI., 1984), levels of testosterone in
serum were elevated at times of aggressive
behaviors and concomitant temporal-gland
secretions. These two datasets demonstrate
unequivocally that the concentrations of
testosterone in serum in a certain proportion
of male African elephants were equivalent
to the levels reported in male Asian elephants in classic musth.
Only during musth do the majority of
male Asian elephants secrete from the temporal glands. In the radiocollared male African elephants, with high levels of testosterone in serum and exhibiting aggression,
the secretion from the temporal gland had
specific characteristics that distinguished
this temporal-gland secretion from that of
male or female African elephants that were
nonmusth. First, the concentration of testosterone in the temporal-gland secretions
was high, reaching 3,632 ng/ml in one
male. This is comparable to the high levels
reported in male Asian elephants in musth
(Rasmussen et aI., 1990). Additional concurrent chemical and behavioral studies of
larger numbers of male African elephants
throughout several years is required to determine if the percentage of adult males exhibiting yearly musth is reflective of these
percentages of males with high levels of
testosterone in serum (62.5% as seen in the
males from the 2nd summer of Addo Elephant National Park, 14.5% as in the large
population in Kruger National Park, or
18.6% as in all the adult males considered
together). These percentages still contrast
strikingly with the high proportion (>90%)
of work on male Asian elephants that exhibit a yearly musth (Toke Gale, 1974).
Composition of population and environmental factors may also influence these percentages. A statistical evaluation of the data
in Table 1 demonstrates both yearly and
seasonal differences among various groups
of males. In addition, age is a probable factor. It may be that male African elephants
commence producing the temporal-gland
436
JOURNAL OF MAMMALOGY
secretion of musth at a later age than do
male Asian elephants.
A definitive chemical proof of musth in
male African elephants is the similarity of
the analyses of gas and ion chromatography
of temporal-gland secretions, from male
African elephants with high levels of testosterone in serum and exhibiting aggressive behaviors, and from male Asian elephants in musth. Additional proof is seen in
the dissimilarity to the chromatograms from
temporal-gland secretions of male African
elephants with low levels of testosterone in
serum (top of Fig. 2 versus lower panels).
Specifically, 16 compounds, including 11
new ones, were concurrently identified (Fig.
2). These included several phenols, organic
acids, ketones, alcohols, and a steroid. By
comparison, the temporal-gland secretions
of female or male African elephants that
were nonmusth had only five dominant
components; phenol, 4-methylphenol, farnesol, farnesol monohydrate, and farnesol
dihydrate (Wheeler et aI., 1982). The chemical compounds in extracts of dichloromethane of temporal-gland secretions of musth
from Asian elephants numbered >23 major
components and 16 minor components
(Rasmussen, 1988; Rasmussen et aI., 1990),
with an additional 30 compounds apparent
in the light headspace fraction; the fraction
that contains compounds that readily volatilize and can be collected in the vapor
phase as discrete entities (Rasmussen et al.,
1994a, 1994b). In the study by Rasmussen
et ai. (1990) on musth of Asian elephants,
several compounds, including 2-nonanol, 2nonanone, and several carboxylic acids,
demonstrated changes in concentration during the progression of musth, at times simultaneously with alterations in levels of
testosterone. These three compounds also
were identified in the musth secretions of
African elephants, again demonstrating an
interspecific similarity in temporal-gland
secretions. Cyclohexanol and two farnesols
appeared to be unique to the temporal-gland
secretions of male African elephants in
musth. These males exhibit aggressive be-
Vol. 77, No.2
haviors and have high levels of testosterone
in their serum.
The data suggest that current and future
chemical analyses of the more ephemeral
volatiles from temporal-gland secretions
may demonstrate more compounds that are
unique to the condition with a high level of
testosterone, perhaps with species specificity for male Asian (Rasmussen et aI.,
1994a) an African elephants. Males are
clearly interested in other males, but are observed to avoid each other in confrontational situations; perhaps, the temporal-gland
secretions are one vehicle for the transmission of information concerning the hierarchy of dominance. We suggest that male
African elephants, like their relatives the
male Asian elephants, may be using musth
as a mechanism to sort out and change the
dominance hierarchy. Male African elephants in nonmusth tend to avoid confrontational encounters with dominant males in
musth (Poole, 1989). Schmidt (1989) suggested that young male Asian elephants in
the altered state of musth may be "insane"
enough to challenge the established order,
and thus, in an indirect way, gain better access to females. Hall-Martin (1987) has
demonstrated that male African elephants in
musth leave their home range, travel further, initiate more contacts with distant
breeding herds, and show aggression that
overrides normal social hierarchies of
males.
The high concentration of testosterone in
the temporal gland secretions of certain
male African elephants may indicate an excretory role for the temporal gland. High
levels of testosterone in temporal-gland secretions of male Asian elephants during
musth (Rasmussen et al., 1990), as well as
the demonstration that the gland begins secreting testosterone subsequent to elevations of testosterone in serum (Rasmussen
et al., 1994a), imply both an excretory role
and a relationship between levels of testosterone in serum and concentrations of testosterone in temporal-gland secretions. It is
possible in the present study that the high
May 1996
RASMUSSEN ET AL.-CHEMISTRY OF MUSTH IN ELEPHANTS
levels of testosterone in temporal-gland secretions resulted from continued secretion
of constant, even low, levels of testosterone
over time, with subsequent concentration
by evaporation. However, in the study by
Rasmussen et ai. (1990), freshly expressed
temporal-gland secretions were obtained,
and the majority of field-collected secretions from the African elephants were collected directly from the temporal duct. In
the present study, eight male African elephants demonstrated a moderate, positive,
linear relationship between both levels of
testosterone and dihydrotestosterone in the
serum and temporal-gland secretions. Data
from an individual male Asian elephant
studied throughout a 4-month-long episode
of musth suggested a similar relationship
(Rasmussen et aI., 1990). High values of
temporal-gland secretion of testosterone in
several males in this study may indicate
heavy musth, or additional data may indi-.
cate a non-parallel time sequence between
levels of testosterone in serum and levels of
testosterone in temporal-gland secretion, as
also suggested by some high levels of temporal-gland secretions in Table 2. An excretory role for temporal-gland secretions is
suggested, not only by the high levels of
testosterone in the temporal-gland secretions and serum during musth, but also by
the dramatic increase in concentration of
several ketones in the temporal-gland secretions during heavy musth (Rasmussen et al.,
1994a). Only further studies with larger
numbers of male elephants, both Asian and
African, monitored behaviorally and chemically, before, during, and after an entire episode of musth, will resolve whether the
temporal gland has an excretory or secretory role with regard to testosterone or ketones. Ketones in the blood must be elevated, suggesting an excretory function of
the temporal gland.
Because this study emphasizes the chemical similarities of musth in the two species
of elephants, clarification of the historic
confusion with the term musth seems appropriate (Rasmussen, 1994). In the 1930s,
437
Blunt (1933) and Melland (1938) described
musth as being synonymous with the male
being in season, and suggested that this
state, rather than the female estrus cycle,
determined mating. At this time, no distinction was made between the rather frequent
temporal-gland secretions by both male and
female African elephants (perhaps in response to stress, pain, or excitement) and
the infrequent temporal-gland secretions by
male African elephants accompanied by aggressive behaviors. The confusion between
types of secretions and the failure to recognize proper categories resulted in several
contradictory conclusions: African elephants of both sexes showed musth (which
we now recognize has behavioral and
chemical criteria-Blunt, 1933; Melland,
1938; Murray, 1976; Sanderson, 1960),
musth was not related to the sexual cycle
of males (Perry, 1953; Sikes, 1971), and
musth did have a strong sexual significance
(Freeman, 1980).
Comprehensive studies of reproduction
in the African elephant during the 1960s
and 1970s failed to detect the significance
of musth (Laws, 1969). Buss and Johnson
(1967) and Short et ai. (1967) showed active spermatogenesis in African elephants
with low levels of testosterone in serum,
leading Hanks (1979) to conclude that there
was no link between temporal-gland secretion and reproduction in male African elephants. Buss et ai. (1976) discussed possible roles of temporal-gland secretions in
recognition of individuals and as indicators
of stress or alarm. In his definitive study of
morphology, evolution, and behavior of elephants, Kingdon (1979) also makes no
mention of the role of musth in the reproduction of African elephants. Use of the
term musth in African elephants in the scientific literature before the definitive papers
of Poole and Moss (1981), Poole (1987,
1989), Hall-Martin and van der Walt
(1984), and Hall-Martin (1987) often simply meant that temporal-gland secretions
were observed. Currently, it is impossible
to decipher whether or not these secretions
438
Vol. 77, No.2
JOURNAL OF MAMMALOGY
met the chemical criteria of secretions during musth.
The lack of clarity of the function of
musth in the African elephant before the
above publications has led to suggestions
that musth may be a recent phenomenon in
male African elephants. Perhaps musth
arose as a response to confinement within
national parks, or within areas where traditional migrations or seasonal movements
were cut off, or at locations such as Kruger
National Park where populations of elephants are controlled by culling. The linkage of musth to reproduction and observations of concurrent temporal-gland secretions and aggressive behaviors are recent.
The lack of chemical analyses of temporalgland secretions until recently makes it impossible to determine whether the temporalgland secretions described by early workers
(Blunt, 1933; Melland, 1938) were characteristic of the five-component secretions of
temporal-gland secretions in nonmusth by
both genders (phenol, 4-methylphenol, and
several farnesols), or the more chemically
complex secretion characteristic of musth
as described in this paper. Why the behavioral characteristics of musth were not recognized in African elephants by the trainers
in the Belgian Congo lumber camps of the
19th century is a mystery (Caldwell, 1927).
These worker elephants were of both sexes
and were often in captivity up to 20 years,
yet "no elephant has shown signs of
musth" (Caldwell, 1927:77).
The possible recent evolution of musth
in male African elephants is not strongly
substantiated from an evolutionary viewpoint or from the chronology of increased
pressures of stress. However, as the habitat
and ranges of the African elephant are compressed, and the elephants are increasingly
crowded and confined to national parks, the
incidence of musth may increase and some
of the characteristics of musth (e.g., chemical composition) may change. For example, in Kruger National Park (area, 19,000
km2) male African elephants in musth
moved long distances (300 km) in short pe-
riods of time, encountered many different
clans of elephants, and conflicted with other
males, resulting in fights (Hall-Martin,
1987). In comparison, in Addo Elephant
National Park (area, 80 km2) movement of
males was more restrictive. Fighting took
place more frequently and more often resulted in mortality (Hall-Martin, 1987). It is
possible that these effects could increasingly be seen in other ranges of elephants in
the future. Higher densities of elephants
may result in increased levels of hormones,
including testosterone and dihydrotestosterone, and increased secretions of unique
temporal-gland compounds dependent on
these androgen hormones.
ACKNOWLEDGMENTS
This research was supported in part by the
National Institutes of Health (HD18-185 and
RR00163) and Biospherics Research Corporation.
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BRANNIAN, J., F. GRIFFIN, AND P. F. TERRANOVA. 1989.
Urinary androstenedione and luteinizing honnone
concentrations during musth in a mature African elephant. Zoo Biology, 8:165-170.
Buss, I. 0., AND O. W. JOHNSON. 1967. Relationships
of Leydig cell characteristics and intratesticular T
levels to sexual activity in the African elephant. The
Anatomical Record, 156:191-196.
Buss, I. 0., L. E. RASMUSSEN, AND G. L. SMUTS. 1976.
The role of stress and individual recognition in the
function of the African elephant's temporal gland.
Mammalia, 40:437-451.
CALDWELL, K. 1927. Elephant domestication in the
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Submitted 23 December 1994. Accepted 11 August
1995.
Associate Editor was Barbara H. Blake.