Primates (2006) 47:272–274
DOI 10.1007/s10329-005-0171-7
SH O RT CO MM U N IC A T IO N
Ruth Thomsen Æ Joseph Soltis Æ Miki Matsubara
Kiyoaki Matsubayashi Æ Manabu Onuma
Osamu Takenaka
How costly are ejaculates for Japanese macaques?
Received: 20 December 2004 / Accepted: 28 October 2005 / Published online: 9 February 2006
Japan Monkey Centre and Springer-Verlag 2006
Abstract Much sexual selection theory is based on the
idea that ejaculate is cheap. Since further details are
unknown our aim was to determine the energy that
primate males require for ejaculate production. We addressed this problem by measuring the energy content
(in kJ) of ejaculates from Japanese macaques (Macaca
fuscata) using standard bomb calorimetry. Then, we
estimated the relative amount of energy that individuals
require for ejaculate production by relating the net energy content of ejaculates to males’ daily basal metabolic
rate (BMR). Fresh macaque ejaculate contains
3.0 kJ ml1. Assuming a mean volume of 2.7 ml an
average macaque ejaculate contains 8.1 kJ. Depending
on the individuals’ body mass (6–13 kg) and the number
and volume of the ejaculates, macaque males are assumed to use between at least 0.8% and at most 6.0% of
their BMR for ejaculate production per day during the
breeding season. Even when regarding only the minimal
energy investment of 0.8% of daily BMR for ejaculate
production, clearly ejaculates come with some cost for
primate males.
R. Thomsen (&)
Institute of Zoo and Wildlife Research, Alfred-Kowalke-Str. 17,
10315 Berlin, Germany
E-mail: thomsen@izw-berlin.de
Tel.: +49-30-5168701
J. Soltis
Education and Science, Animal Programs Administration,
Disney’s Animal Kingdom, Lake Buena Vista,
FL 32830, USA
M. Matsubara
Laboratory of Human Evolution Studies,
Department of Zoology, Kyoto-University,
Sakyo-ku Kitashirakawa, Kyoto 606-8502, Japan
K. Matsubayashi Æ M. Onuma
Center for Human Evolution Modeling,
Primate Research Institute, Inuyama 484-8506, Japan
O. Takenaka
Department of Cellular and Molecular Biology,
Primate Research Institute, Inuyama 484-8506, Japan
Keywords Ejaculate Æ Energy Æ Japanese macaques Æ
kJ Æ Yakushima
Introduction
The current discussion of primate male reproductive
strategies involves males’ investment in body size,
secondary sexual traits, mate searching, mate guarding, male coalitions, fighting against competitors and
sperm competition (Kappeler and van Schaik 2004).
While many aspects of primate male reproductive
strategies are expensive the production of sperm typically is assumed to be ‘‘cheap’’ in terms of lacking
any costs.
In other species than primates males are known to
invest non-trivial amounts of energy for sperm production (Dewsbury 1982). For example, grasshoppers
(Isophya kraussi) use approximately 20% of their total
body energy to produce one spermatophore (Voigt et al.
2005). Adders (Vipera berus) lose as much body mass
during the period of spermatogenesis as during the
subsequent breeding season (Olsson et al. 1997), and
lemon tetra males (Hyphessobrycon pulchripinnis) invest
high energetic costs in sperm production (Nakatsuru
and Kramer 1982).
In seasonally breeding primates males are known to
reduce their testes sizes during the non-breeding season
implying that testicular tissue, spermatogenesis and the
production of ejaculates entails energy demands that are
worth saving (Harcourt et al. 1995; Dixson 1998). But
nothing at all is known about the energetic costs of
primate ejaculates.
To estimate these costs we measured the energy
content (kJ) of ejaculates from Japanese macaques
(Macaca fuscata). Then we related the net energy
content of ejaculates to the daily basal metabolic rate
(BMR) and calculated the relative amount of
energy that individuals may require for ejaculate
production.
273
Methods
Japanese macaques belong to those primate species in
which captive as well as wild living males regularly
masturbate, thus allowing the non-invasive collection of
ejaculates (Enomoto 1974; Thomsen et al. 2003;
Thomsen and Soltis 2004).
Using pipettes (fluid part) and tweezers (plug part) we
collected a total of 21 ejaculates from 11 males immediately after masturbation. Six males were housed at the
Primate Research Institute of the Kyoto University and
five males belonged to the free-ranging NINA-A troop
on Yakushima Island (Soltis et al. 2001). The ejaculates
were kept frozen (20C) in plastic bags until analysis.
After 24 h of drying of the ejaculates at 20C (Neocool
DIP BD 22, Yamato Science) to constant mass, the loss
of water was calculated and the dried ejaculates were
pooled together, powdered and formed into small pellets. The energy was measured by bomb calorimetry
(Auto-calculating bomb calorimeter CA-4P, Shimazu) in
kcal g1 and converted into kJ g1 (factor 4.1868).
Results
Before drying, the 21 pooled ejaculates weighed 56.7 g
and afterwards the remaining dried mass was 8.1 g.
Therefore, the fresh ejaculate contained of 48.6 g
(85.7%) water and 8.1 g (14.3%) of sperm mass or any
other of the constituents in solution. From the dried
ejaculate powder we formed seven pellets each of 1 g for
caloric measurements. The measured energy content of
the powder was 20.3±0.6 kJ g1. From this, we calculated an energy content for 1 ml fresh Japanese macaque
ejaculate by the following equations:
20:3 kJ 85:7% : 100% ¼ 17:3 kJ
ð1Þ
and
20:3 kJ 17:3 kJ ¼ 3 kJ.
ð2Þ
Fresh masturbatory ejaculates from Japanese macaques have a mean ± SD volume of 2.7±1.0 ml (minimum 0.8 ml; maximum 4.1 ml; n=21; Thomsen 2000).
Assuming a linear relationship between energy content
and ejaculate volume, a medium sized macaque ejaculate
of 2.7 ml contains 8.1 kJ (3 kJ · 2.7 ml). As a conclusion, macaque males invest at least 3 kJ to produce 1 ml,
or 8.1 kJ to produce one medium sized ejaculate, plus an
unknown value which represents the energy efficiency of
the testicular tissue and the semen glands.
Discussion
During the 4-month breeding season, free-ranging
macaque males ejaculate once daily by masturbation if
they are restricted from mating, indicating that they
continuously invest an energy of about 8.1 kJ day1 into
spermatogenesis independently of possible mating success (Thomsen and Soltis 2004). Males of higher social
status were observed to ejaculate by mating with a
female up to six times a day (unpublished data). This
would lead to a maximum of energy investment of
48.6 kJ day1, tentatively assuming that consecutive
ejaculations also contain an average volume of 2.7 ml.
Smaller, younger males of low social status, however,
never attain the observed maximum of six copulations.
Thus, our calculations concerning more than about
three ejaculates per day may apply most notably for
males of higher social status who are more likely to be
engaged in frequent copulations over a couple of days
(Soltis et al. 2001).
To estimate the relative minimal costs of ejaculate
production, we calculated the percentage of daily energy
investment for ejaculate in relation to the individual
BMR. We determined BMR using the classic allometric
scaling relationship BMR=aM0.75, with a being a species-dependent constant and M being body mass with an
exponent of 3/4 (Kleiber 1932; Savage et al. 2004). For a
we used 34 kcal g1, the value which is characteristic for
primates (Aiello and Wheeler 1995).
The daily relative energy investment of males for
ejaculates depends on body mass and on the number and
the volume of the ejaculates. Adult Japanese macaque
males weigh between 6 to 13 kg (Matsubayashi and
Mochizuki 1982). BMR therefore ranges between 546 kJ
for a young adult male (34 kcal g1 · 6 kg0.75 ·
4.1868 kJ) up to 975 kJ for an adult male (34 kcal g1 ·
13 kg0.75 · 4.1868 kJ). Due to a commonly observed
skew in mating frequency of males of different age and
social status (the higher the status the more mating
success) we argue that the realistic frame of relative
energy investment into ejaculates ranges between a
minimum of 0.8% for a 13-kg male with one ejaculation
(one masturbation or one mating success) and a maximum of 6.0% for a 10-kg male with six ejaculations on
days with high mating success (Table 1).
Table 1 Percentages of the daily BMR which Japanese macaques
(Macaca fuscata) use for the production of mean sized ejaculates
(mean volume: 2.7 ml, mean energy content 8.1 kJ, 1–6 ejaculates
day1)
Body
mass (kg)
6
7
8
9
10
11
12
13
BMR
(kJ) day1
545.7
612.6
677.1
739.7
800.5
859.8
917.8
974.6
Number ejaculates per day
1
2
3
4
5
6
1.5
1.3
1.2
1.1
1.0
0.9
0.9
0.8
2.4
2.2
2.0
1.9
1.8
1.7
3.3
3.0
2.8
2.6
2.5
4.0
3.8
3.5
3.3
5.1
4.7
4.4
4.2
6.0
5.7
5.3
5.0
Values are based on observations of masturbation and of males’
mating success on Yakushima, NINA-A-troop (minimum 0.8%
and maximum 6.0% of daily BMR)
274
However, as long as comparative data from other
primates are not available, we cannot estimate whether a
net energy use of 3 kJ ml1, or 8.1 kJ for one medium
sized ejaculate is high or low. But since ejaculates from
closely related species seem to resemble each other
(unpublished data) their net energy values should not
greatly differ. Our results, therefore, should be valid at
least for the genus Macaca and might fit also for other
plug-forming species within the order primates such as
mouse lemurs (Microcebus murinus), squirrel monkeys
(Saimiri sciureus) or chimpanzees (Pan troglodytes).
From our study, the realistic frame of relative energy
of ejaculates of macaque males may range from 0.8 to
6% of their daily BMR. This value constitutes the
minimum energy expenditure of males to achieve fertilization because it includes exclusively the energy of the
ejaculate. It does not yet include the energy which is
necessary for spermatogenesis (i.e. to produce and
maintain the testicular tissue) and for fluid production
(i.e. to produce and maintain the seminal glands). But if
indeed a minimal energy investment of about 1% of
daily BMR is used to achieve fertilization, clearly ejaculates come with some cost for primate males.
Acknowledgements We thank Prof. Dr. Heribert Hofer, Dr. Oliver
Höner, Dr. Christian Voigt and Dr. Sylvia Ortmann from the
Institute of Zoo and Wildlife Research and above all Prof. Dr.
Alexander Harcourt for comments on the manuscript. Furthermore, we thank Prof. Dr. Hideyuki Ohsawa and Prof. Dr. Juichi
Yamagiwa for support of our work in Japan. Ruth Thomsen was
financed by the German Academic Exchange Service (HSP III,
D/97/16290) and by the ‘‘Berliner Programm zur Förderung der
Chancengleichheit für Frauen in Forschung und Lehre (N-16/04)’’.
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