12. Almendros, G., Gonzfilez-Vila, F. J.,
Martin, F. : Soil Biol. Biochem. 21, 481
(1989); Griffith, S. M., Schnitzer, M.:
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13. Hatcher, P. G., Schnitzer, M., Dennis
L. W., Maciet G. E.: Soil Sci. Soc. Am.
J. 45, 1089 (1981)
14. FrOnd, R., Liidemann, H.-D.: Sci. Tot.
Environ. 81/82, 157 (1989)
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Berlin: de Gruyter 1984
16. Kumada, K., Hurst, H. M.: Nature
214, 631 (1967)
17. Eglinton, G., Hunneman, D. H.,
Naturwissenschaften 78,362- 365 (1991) © Springer-Verlag 1991
0028104291001207
Unusual Mating Behavior of Malaysian Treefrogs,
Polypedatesleucomystax
A. S. Feng
Department of Physiology and Biophysics, University of Illinois,
Urbana, IL 61801
P. M. Narins
Department of Biology, University of California, Los Angeles, CA 90024
In most anuran species, reproduction
involves complex inter- and intraspecies
interactions. Males produce species-
specific advertisement calls to signal
their reproductive readiness and loca-
tions to potential mates. Since a breed-
ing pond is often shared by many an-
uran species, females play a critical role
in the interspecies intersexual interac-
tions. Females are preferentially at-
tracted by calls of conspecific rather
than heterospecific males and they can
reliably extract calls produced by con-
specific males from a mixed chorus,
thus minimizing cross-species fertiliza-
tion [1].
In most breeding ponds, a large
number of male frogs compete in-
tensely for opportunities to mate with a
much smaller number of females [2].
This intrasexual male-male competition
is primarily intraspecies and involves
competition for: (1) territories or re-
sources, (2) chance to broadcast adver-
tisement calls, (3) access to approach-
ing females, and (4) reproductive suc-
362
McCormick, A.: Org. Mass Spectrom.
1, 593 (1968); Holloway, P. J.: Chem.
Phys. Lipids 9, 158 (1972); Kolattu-
kudy, P. E.: Science 208, 990 (1980)
18. Grandou, P., Pastour, P.: Peintures et
Vernis. P a r i s " Hermann 1966;
Gunstone, F. D., Harwood, J. L.,
Padley, F. B.: The Lipid Handbook.
New York: Chapman and Hall 1986
19. Largeau, C., Derenne, S., Casadevall,
E., Kadouri, A., Sellier, N.: Org. Geo-
chem. 10, 1023 (1986)
20. Harvey, G. R., Boran, D. A., in: Humic
Substances in Soil, Sediment and Water,
p. 223 (Aiken, G. R., McKnight, D. M.,
cess and the ultimate transfer of
gametes through fertilization of eggs
laid by females. In many species, males
defend individual territories and main-
tain male-male spacing through the
emission of territorial calls and/or en-
counter calls. In a chorus, a calling
male has been shown to change his mat-
ing to territorial/encounter or aggres-
sive calls when he is approached by a
conspecific male [3]. In some species,
the intruder responds by emitting terri-
torial/encounter (or aggressive) calls
himself in a graded fashion depending
on the distance of the nearest neighbor
[4]; both males continue to elicit calls
until they fight and one of them retreats
[5, 6]. The ability of a male to defend a
superior territory from which to broad-
cast his advertisement calls often de-
termines his reproductive success.
Females of a number of frog species
have been shown to select their mates
on the basis of resources controlled by
the conspecific male [ 6 - 8 ] , or phe-
notypic characteristics such as the dora-
Naturwissenschaften 78 (1991) © Springer-Verlag 1991
Wershaw, R. L., MacCarthy, P., eds).
New York: Wiley 1985
21. Nip, M., Tegelaar, E. W., de Leeuw, J.
W., Schenck, P. A.: Naturwissen-
schaften 73, 579 (1986); van Aarsen, B.
G. K., de Leeuw, J. W., Tegelar, E. W. :
4tb Workshop on the Chemistry and
Analysis of Environmental Hydro-
carbons, p. 28, Strasbourg 1990;
Hatcher, P. G. : Sci. Tot. Environ. (in
press); K6gel-Knabner, I., de Leeuw, J.
W., Hatcher, P. G. : ibid. (in press)
22. Wilson, M. A.: NMR Techniques and
Applications in Geochemistry and Soil
Chemistry. Oxford: Pergamon 1987
inant frequency in the male's adver-
tisement calls [9], the rate of calling
[10], or male's body weight [11, 12]; in
other frog species, however, mate selec-
tion is less dependent on these attrib-
utes (see review in [13]). In the lepto-
dactylid frog Physalaemus pustulosus
of Panama, females select larger males
on the basis of the dominant frequency
in the call [9]. In the Australian lepto-
dactylid Uperoleia laevigata, however,
Robertson [12, 14] showed that using
the males' calls as a basis females select
mates that are about 70 % of their own
body weight; heavier males hamper
oviposition, whereas lighter males do
not have sufficient sperm to fertilize the
entire clutch of eggs. Thus, it appears
that the ability of females to select
mates in the optimal weight range de-
termines the fertilization success in
Uperoleia laevigata. It has been
suggested [15] that fertilization by
optimal males is one of the most im-
portant factors in evolution, i.e., more
important than an increase in genetic
diversity.
If female choice were to determine fer-
tilization success, the female should
only mate with the selected male and
not with any other males. Namely, if
there are optimal characteristics in a
male, the sexual partner needs to be
carefully chosen and ideally it should
be limited to one. Indeed, although an-
urans are polygamous, namely, a
female may mate with more than one
male within a breeding season (or vice
versa for a male), she normally mates
with one male at any one time. Females
spotted in amplexus invariably have
just one sexual partner [16, 17]. Here
we report the sighting of an unusual
amplexus involving one female and
three male sexual partners.
Sighting occurred on the evening of
February 21, 1990 at a small pond on
the edge of the tropical rain forest
located about 0,8 km south of Ulu
Gombak Field Study Centre (Selangor)
of the University of Malaya, approx-
imately 25 km north of Kuala Lumpur
(3°20'N, 101°45'E). During the 2-
week study period ( 2 / 1 3 / 9 0 - 2/26/90),
Fig. 1. "Group sex" mating sequence in Polypedates leucomystax. These photos were taken
from a tree branch at the study site
Naturwissenschaften 78 (1991) © Springer-Verlag 1991
males of over a dozen species called
every night from 2030 to 0100 h at this
study site. In his study of Malaysian
frogs' calling behavior, Arak [18] has
shown that males of these different
species call at different periods and
geographical locations to minimize
acoustic interference. For example,
males of Rana nitida begin calling
immediately after sunset and cease call-
ing at ca. 2100 h, whereas males of Rana
erythraea seldom call before 2200 h;
the former call from swampy areas and
the latter while sitting in water. In con-
trast, males of Polypedates leu-
comystax 1, the subjects of our study,
call from 2100 to 0000 h but from tree
branches or stems at high elevations
(1.2 - 2.1 m above ground level). It was
in the midst of our study of the charac-
teristics and functional significance of
the different components of advertise-
ment calls of this and a related species
(Narins and Feng, in preparation) when
we observed the unusual mating en-
counter involving a female and three
males of Polypedates leucomystax.
The amplexus took place on a tree
branch about 1.7 m above the water.
As was typically the case with Poly-
pedates leucomystax, amplexus oc-
curred when a male pursued an ap-
proaching female. The presence of a
female (but not a male) in an area of
the pond generally caused several
nearby males to stop calling. In this
particular case, one male detected and
located the approaching female and
successfully clasped her. The female
then carried him to the egg deposition
site on the vertical tree branch 1.7 m
above the water. Once at the site, she
initiated foam nest production into
which she would deposit her eggs; egg
laying occurs only after a substantial
foam nest is constructed in both the
Rhacophoridae [19] and the Leptodac-
tylidae [20]. Before she laid her eggs,
however, a second male was seen to en-
croach upon the amplexed pair (Fig.
1 A). This led to a physical struggle be-
tween the two males in which the
second male attempted to dislodge the
first male, and the first male tried to re-
pel the second male (Fig. 1 A - D). The
female did not appear to participate in
the fight. The physical struggle between
the two males did not resolve the con-
flict. But in the process, the first male
succeeded in positioning himself so that
According to R. Inger, this is most likely a
Polypedates leucomystax. However, it is
distinguishable from typical Polypedates
leucomystax (formerly Rhacophorus leuco-
mystax) found extensively in the region in
terms of its size (i.e., distinctly smaller),
color (lighter with no stripes dorsally), width
of head (wider across the temporal region),
webbing between toes (slightly fuller), struc-
ture of mating calls, male's calling behavior,
and breeding site (i.e., occupying tree
branches and stems at higher elevations in-
stead of reeds and bushes at ground level)
363
he could clasp the female more
securely, i.e., with both his hands cling-
ing tightly into the female's arms and
his body lowered so that his cloaca
pressed closer toward the female's
cloaca (Fig. 1 C). When the subsequent
attempt by the second male to dislodge
the first male (Fig. 1 D) failed, he simply
clasped the first male (Fig. 1 E).
Before the second male could securely
clasp the first male (i.e., with his hands
clinged toward the first male's arms or
armpits), a third male joined in the
mating act (Fig. 1 E). His arrival did
not elicit as profound a physical
struggle as when only two males were
involved. He soon managed to securely
clasp the second male (Fig. 1 F); by this
time the foam nest was of sufficient size
to engulf the cloacal regions of all three
males. This mating posture was main-
tained for more than 3 h (i.e., no
change occurred until 0100 h when we
left the study site that night); pre-
sumably during this period the female
laid her eggs (eggs are laid after a sub-
stantial foam nest is constructed; [19]).
Since the males were vertically stag-
gered in an orderly fashion and their
cloacal regions were surrounded by the
large foam nest, they all presumably
participated in fertilization of eggs laid
by the female.
Amplexus involving a female and mul-
tiple males rarely occurs in anurans
[17]. The most common anuran re-
productive mode involves one-to-one
amplexed pairs. Although polyandry
has been recently observed [17] in
Afrixalus delicatus, a female of this
species may mate with several males
over several nights but only one male
per night or, one male per nest if she
mates with more than one male per
night. To the best of our knowledge,
this is one of the first reports 2 to de-
scribe the occurrence of "group sex" in
frogs where several males mate with
one female simultaneously. Due to the
short study period, however, we could
not determine the extent to which
females of Polypedates leucomystax
practice "group sex", nor do we know
if and how they select their mating
partners. Nevertheless, our observa-
tions indicate that even if the female
z Group sex may not be so rare in anurans
(pers. commun, with Drs. R. Inger, Y. S.
Lin and H. S. Yong) but its occurrence is
seldom reported
364
did select the first male for her sexual
partner she did not exhibit any overt at-
tempt to ensure that her eggs be fer-
tilized exclusively by this male. Clearly,
further studies are necessary to fully
unravel their reproductive behavioral
pattern.
The existence of group sex in anurans
raises an interesting question. Namely,
does this mating strategy offer any ad-
vantages? We could envision two pos-
sible advantages. It is thought that a
single mating usually results in the fer-
tilization of all the eggs one female lays
[15, 21]. On the other hand, consider-
ing the differential size of males and
females (i.e., females considerably lar-
ger than males) in Polypedates leu-
comystax, it is possible that females can
produce many more eggs in one clutch
than can be fertilized by a single male
as Robertson [12] described for Upero-
leia laevigata. If this were the case,
selection would favor multiple males
fertilizing the eggs since each male
would have a nonzero probability of
contributing his genetic material to sub-
sequent generations. Second, "group
sex" would put less premium on female
choice; a less than optimal choice is not
fatal when multiple sexual partners are
allowed. Moreover, as argued recently
for birds and mammals [22], sexual
promiscuity or sexual infidelity actually
may offer a selective advantage, i.e., in
providing genetic diversity. This is par-
ticularly applicable to anurans in which
parents do not recognize their young
and thus inbreeding is presumably wide-
spread. Fertilization of eggs by several
males can therefore increase genetic
diversity of the offspring, resulting in
potentially greater adaptation to fluc-
tuating environments than would be the
case for inbred animals.
Alternatively, "group sex" may simply
be a consequence of a skewed sex ratio
in the local population due to the un-
usually high density of males, or that
the first male is too small and too weak
to dislodge other males. But even if this
were true, the males and female in-
volved must accept the practice of
"group sex" to tolerate the presence of
extra sexual partners during mating.
From the point of view of a male, in-
stead of engaging in a risky physical
confrontation to ensure exclusive fer-
tilization of the egg clutch, an indi-
vidual male may be better off accepting
the presence of other males, if the
Naturwissenschaften 78 (1991) © Springer-Verlag 1991
number of eggs is nonlimiting. And as
for females, fertilization by optimal
males is desirable and is thought [15] to
be more essential than the increase in
genetic diversity for mate choice. How-
ever, if the size of their egg clutches is
large, their fertilization success may be
increased by the presence of multiple
partners, albeit the quality of the
offspring may be compromised as a
consequence (i.e., when eggs are fer-
tilized by suboptimal males). There-
fore, while one-to-one mating is the
most common reproductive strategy in
anurans, it appears to be just one of
many viable strategies.
We thank SERU (of the Prime Minis-
ter's Dept. of Malaysia) for granting us
a research permit, Prof. H. S. Yong
f o r his hospitality during our visit, R.
Inger who kindly identified the frog
specimens for us and D. Gooler who
provided useful comments on an earlier
version of this manuscript. This re-
search is supported by grants from the
Research Board of the University of Il-
linois (to A.S.F.) and the Academic
Senate of the University of California at
Los Angeles (to P.M.N.).
Received January 21, 1991
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31, 1011 (1983)
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Naturwissenschaften 78,365- 367 (1991) © Springer-Verlag 1991
002810429100119J
High Ultrasonic Hearing and Tympanal Slit Function
in Rainforest Katydids
A. C. Mason, G. K. Morris and P. Wall
Dept. Zoology, Erindale College, University of Toronto, Mississauga, Ont.,
Canada L5L 1C6
Pseudophyllinae (false-leaf tettigo-
niids) are c o m m o n insects in the
world's tropical forests, and more than
1 000 species are described [1]. Both
their sound signals and ear structure
have unusual features; but their relative
inaccessiblity has left pseudophylline
auditory function unstudied till now.
The dominant frequency in the calls of
many species is in the ultrasonic range:
2 0 - 4 0 kHz [2]. But even higher car-
riers are now discovered in this sub-
family, at 65, 70, and 81 kHz (an un-
described species of Haenschiella, Dre-
panoxiphus angustelaminatus, Myo-
pophyllum speciosum), as well as the
highest dominant carrier currently at-
tributable to any acoustic insect: 102
kHz (Haenschiella ecuadorica, de-
scribed below).
Tracheal features of pseudophylline au-
ditory systems depart markedly from
those of katydids (mostly Tettigoniinae
and Conocephalinae) whose auditory
physiology has been studied to date [3].
In proportion to body size, their
acoustic spiracle is reduced: this feature
is universal and serves as a diagnostic
character for the subfamily [4]. Also re-
duced relative to other tettigoniids, are
the dimensions of the acoustic trachea
Naturwissenschaften 78 (1991) © Springer-Verlag 1991
(B. Fritzsch, M. J. Ryan, W.
Wilczynski, T. E. Hetherington, W.
Walkowiak, eds.). New York: Wiley
1988
14. Robertson, J. G. M. : Anim. Behav. 34,
773 (1986)
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The Amphibian Fauna of Peninsular
Malaysia. Kuala Lumpur (Malaysia):
Tropical Press 1975; Inger, R. F.: Fiel-
diana Zool. 33, 183 (1954)
[5]. By contrast, the openings to the
tympanal chambers and the volume of
the chambers themselves are larger
(Fig. 1). This morphology suggests dis-
tinctive mechanical properties for the
acoustic tracheal system of pseudophyl-
lines. With this in mind, we have ex-
amined the hearing of several species.
Specimens were collected in April 1990
from Ecuadorean rainforest and trans-
ported alive to Canada where we re-
corded and analyzed their sound and
vibratory signals and measured periph-
eral auditory responses. Auditory re-
sponses of M. speciosum (n = 10) and
individual specimens of H. ecuadorica
and Typophyllum nr trapeziforme were
measured by averaging summed action
potentials of the tympanal nerve re-
corded in the femur. Substrate signals
generated by tremulation were detected
with an accelerometer applied to the
woody stem of a potted plant upon
which males courted and mated with
females.
The principal carrier frequency of M.
speciosum centers on 81 kHz (Fig. 2A).
Its call is typically two trains of very
short pulses (20 pulses/train, pulse
duration 0.5 ms), lasting about 150 ms
and given at 4 - 12-s intervals at 22 °C.
17. Backwell, P. R. Y., Passmore, N. I.:
Herpetology 46, 7 (1990)
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20 (1984)
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(1950)
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Campbell, ed.). Chicago: Academic
Press
22. Gladstone, D. E.: Am. Nat. 114, 545
(1979); Stacey, P. B.: ibid. 120, 51
(1982)
Temperatures in the habitat are usually
lower (by about 10°C), and calling
intervals in the field are correspond-
ingly longer. H. ecuadorica has similar
call features: its principal carrier fre-
quency is at 102 kHz (n = 2) and the
call is a single train of 1 0 - 1 7 pulses
(each pulse less than 1 ms long), lasting
only 4 0 - 5 0 ms. Average interval be-
tween songs is 41 s (n = 32 intervals of
one singer). Typophyllum, chosen for
study as a pseudophylline having con-
trasting song parameters, has a carrier
frequency almost in the audio range (21
kHz), and emits a relatively sustained
sequence of prolonged, very high-Q
A
, M s osu
B
Tettigoniz~ ...........
Fig, 1. Comparative morphology of the
acoustic trachea and spiracle (right), and
tympanal slits (left) in A) pseudophylline,
and B) tettigoniine katydids; sl tympanal
slits, sp acoustic spiracle
365