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ARTICLE
Evolutionary view of waste-management behavior using volatilechemical cues in social spider mites
Yukie Sato Æ Yutaka Saito
Received: 19 January 2007 / Accepted: 24 July 2007 / Published online: 13 November 2007
� Japan Ethological Society and Springer 2007
Abstract Spider mites of the genus Stigmaeopsis (Acari:
Tetranychidae) construct and live gregariously inside
woven nests on the leaf surface of host plants. This genus
shows waste-management behavior—they defecate at par-
ticular sites—but the rules for management differ between
species. The utilization of chemical cues for waste man-
agement is known in two species, Stigmaeopsis miscanthi
inhabiting Miscanthus sinensis and S. longus inhabiting
Sasa senanensis, but not in any others. In this study, we
first investigated the origin of the chemical compounds to
understand how the behavior evolved, and then investi-
gated the responses of each species to chemical compounds
from different sources. The results show that the chemical
compounds are commonly contained in the feces of several
Stigmaeopsis species, as well as in their host plant juices,
suggesting this behavior evolved using the chemical com-
pounds originally contained in their feces. Our results also
show that the chemical compounds used by S. miscanthi
and S. longus are subtly different and involve host plant
differences, and that S. miscanthi could respond to both
compounds, but S. longus could not. Considering this in
terms of their phylogenetic relationship, it is expected that
these two species may have evolved from a common
ancestor living on Sasa senanensis.
Keywords Spider mite � Nest sanitation �Waste management � Volatile chemical cue �Host plant shift
Introduction
Many social insects and arachnids keep their nests sanitary
(Wilson 1975; Saito 1983, 1995, 1997; Holldobler and
Wilson 1990; Donze and Guerin 1994; Choe and Crespi
1997; Weiss 2006). These behaviors are thought to be
important adaptations for nest-building and group-living
animals because poor sanitation may facilitate disease
infections and reduce living space (Lee 1994; Hamner and
Parrish 1997; Hart and Ratnieks 2002; Little et al. 2003).
Many studies have described nest sanitation behavior, but
few have addressed the evolutionary aspects of such
behavior (Weiss 2006).
Waste-management behavior is found in nest-building
and group-living spider mites and is considered to be clo-
sely associated with the evolution of mite sociality (Saito
1983, 1995, 1997). Spider mites are minute arachnids
whose bodies range from 300 to 500 lm in length. They
suck the juices of their host plants, and their liquid wastes
are sticky like honeydew. The leaf surface not only pro-
vides the mites’ food resource but also their living space.
Spider mites of the genus Stigmaeopsis Banks (Acari:
Tetranychidae) construct tunnel-like woven nests having
no specific structure except for two entrances and a roof on
the leaf undersurface of host plants; they live within the
nests in groups (Saito 1983, 1995, 1997; Saito et al. 2004).
All species of this genus show obvious waste-management
behavior—nest mates defecate at particular sites—but
these sites and the rules underlying the waste management
differ among species (Sato and Saito 2006). Stigmaeopsis
Y. Sato � Y. Saito
Laboratory of Animal Ecology,
Department of Ecology and Systematics,
Graduate School of Agriculture,
Hokkaido University, Sapporo, Hokkaido 060-8589, Japan
Y. Sato (&)
National Institute for Agro-Environmental Sciences,
3-1-3 Kannondai, Tsukuba,
Ibaraki 305-8604, Japan
e-mail: [email protected]
123
J Ethol (2008) 26:267–272
DOI 10.1007/s10164-007-0069-5
takahashii Saito et Mori and S. saharai Saito et Mori
establish defecation sites at two locations, just outside each
nest entrance, which they recognize by tactile cues (Sato
and Saito 2006) because their primitive eyes cannot form
sharp images (McEnroe 1969). In contrast, S. miscanthi
(Saito) and S. longus (Saito) establish their defecation sites
at only one entrance, and waste management is maintained
by two simple rules: they use tactile cues to defecate near
the nest entrances like S. takahashii and S. saharai when
there is no feces, and they use volatile chemical cues from
the feces to defecate at sites where feces have previously
been deposited (Sato et al. 2003; Sato and Saito 2006).
These differences between species correspond to the
differences in their nest and group sizes and reflect dif-
ferent strategies for defending against predatory mites. S.
takahashii and S. saharai construct many small, separate
nests to prevent predator intrusion (Mori and Saito 2004,
2005). S. miscanthi and S. longus construct a few large
nests by continuously enlarging their original nests to live
in large groups, and counterattack against the intruding
predators in large numbers (Mori and Saito 2004, 2005).
Using volatile chemical cues to ensure that feces are
deposited at a single place in a nest is thought to be
adaptive for S. miscanthi and S. longus, whose nests are
large and continuously expanding. If they were to deposit
feces at every nest entrance like S. takahashii and S. sa-
harai, they would construct new defecation sites whenever
they expand their nests, and as a result, unnecessary def-
ecation sites would be constructed inside their nests (Sato
and Saito 2006). Based on a molecular phylogenetic
analysis, S. miscanthi and S. longus are known to be
derived from the common ancestor of S. takahashii and S.
saharai (Sakagami 2002), and the waste-management
behavior of using volatile chemical cues from feces in
addition to the behavior of using tactile cues would be
newly evolved for waste management (Sato and Saito
2006).
In this study, we attempted to learn how the usage of
volatile chemical cues for waste management has evolved.
First, we investigated whether this practice developed
through the addition of some volatile chemical compounds
into feces or by the use of such compounds originally
contained therein. We investigated this by confirming
whether volatile chemical compounds were contained in
the feces of S. takahashii, which does not use volatile
chemical cues for waste management. Second, we inves-
tigated whether the volatile chemical compounds used by
S. miscanthi and S. longus are the same by observing the
effect of S. miscanthi feces on the defecation behavior of S.
longus and vice versa. Third, we investigated whether or
not the chemical compounds contained in the mite feces
originated from the host plants. We investigated this by
confirming the effects of ether-soluble substances extracted
from host plants on defecation behaviors, because ether-
soluble substances extracted from mite feces are known to
affect defecation behavior (Sato et al. 2003).
Materials and methods
Biological materials
S. miscanthi is comprised of two taxonomic groups dis-
tinguished by differences in male–male aggressiveness, the
relative lengths of male first legs, diapause attributes, and
by reproductive isolation between them (Saito and Sahara
1999; Saito et al. 2000, 2002; Sato et al. 2000a, b). These
two groups are referred to as the high-aggression form (HG
form) and the low-aggression form (LW form). We used a
population of the HG form collected from Tobuko
(Nagasaki Prefecture, Japan) in July 1998. S. longus and S.
takahashii were collected from a forest in Sapporo
(Hokkaido Prefecture, Japan) in May 2000 and August
1999, respectively. These mites were all reared on detached
leaves of host plants on water-soaked cotton in petri dishes
under controlled conditions of 23 ± 2�C, 40–70% relative
humidity, and a 15:9 h light-to-dark cycle. All bioassay
experiments mentioned hereafter were also conducted
under these same conditions between May and June 2001.
Each of the laboratory cultures was initiated from more
than 50 females collected arbitrarily in the field. The host
plant of S. miscanthi, the perennial pampas grass Miscan-
thus sinensis Anderss (Gramineae), was originally obtained
from Hiroshima Prefecture 16 years ago and since then has
been cultivated in a greenhouse in Hokkaido University.
Leaves of the host plant of S. longus, the dwarf bamboo
Sasa senanensis Franchet et Savatier, were collected from a
forest on the Hokkaido University campus.
Experiment 1: effects of different species feces
on defecation behavior
Three females, taken arbitrarily from each S. miscanthi and
S. longus laboratory culture, were introduced onto a
1.0 9 3.0 cm area of detached host leaf surrounded by
water-soaked cotton and allowed to construct nests. Three
days after introduction, all fecal piles (the solid fecal pellets)
were removed, and fecal piles from other nests, in which
either three conspecific females or three females of another
species had lived for 3 days, were transferred to the middle
of the nest roof exterior (Fig. 1). To confirm whether volatile
chemical cues were contained in the feces of S. takahashii,
which does not use volatile chemical cues for waste man-
agement, we took fecal piles from S. takahashii nests and
placed them in the nests of S. miscanthi and S. longus. To
268 J Ethol (2008) 26:267–272
123
confirm whether the volatile chemical cues used by S. mi-
scanthi influence the defecation behavior of S. longus and
vice versa, we placed fecal piles from S. miscanthi or S.
longus nests into the nests of S. miscanthi or S. longus. We
also used the fecal piles from other conspecific nests to learn
their effect. For the control treatment, we used fecal piles
from a group’s own nests (Fig. 1). One day after each
treatment, we checked the locations of newly deposited feces
using a dissecting microscope. If the females use volatile
chemical cues from the feces, then the new fecal piles should
be found at the new sites (on the leaf surface) under the nest
roofs where the fecal piles had been placed (Sato et al. 2003;
Sato and Saito 2006). We compared the frequencies of the
nests where new fecal piles could be found at the new sites
between treatments for each species.
Experiment 2: effects of ether-soluble substances
extracted from host plants on defecation behavior
To investigate whether the chemical compounds used for
waste management originate from the host plant juices, we
assayed the effects of ether-soluble substances extracted
from each host plant on the defecation behavior of S. mi-
scanthi and S. longus. Clean leaves (i.e., without mite
infestations) of each host plant were cut into 1.0 9 1.0 cm
pieces using sterilized scissors and placed into diethyl ether
at room temperature for 24 h (200 g M. sinensis in 2.1 l
diethyl ether; 670 g S. senanensis in 3.4 l diethyl ether).
Each solution was filtered using absorbent cotton, and a
1.75 l solution of M. sinensis and a 3.1 l solution of S.
senanensis were obtained. Next, 17.5 ml of M. sinensis
solution and 9.25 ml of S. senanensis solution, each
equivalent to about 2 g of host plant leaf, were concen-
trated by volatilizing diethyl ether until approximately 1 ml
of each solution remained. A piece of filter paper was then
soaked in the concentrated solution. After drying for 3 min,
the filter paper was cut into 1.0 9 1.0 mm pieces using a
sterilized razor and placed on the middle of the exterior
roof of a nest in which three females had been living for
3 days and all feces had been removed. One day after the
above treatment, we checked the location of the newly
deposited feces. If the filter paper contained a sufficient
amount of the volatile chemicals used for waste manage-
ment, then any new fecal piles should be found at the new
site under the spot on the nest roof where the filter paper
had been placed (Sato et al. 2003). There were 16–32
replicates for each treatment. We compared the frequencies
of the nests where new fecal piles were found at the new
site between the treatments for the M. sinensis extract, S.
senanensis extract and the control in experiment 1 (fecal
piles from their own nests).
Statistical procedures
We used log-likelihood ratios (G-test) to test the differ-
ences between the treatments in the frequency at which
new fecal piles were found at the new site. These analyses
were performed using JMP (ver. 5.0.1, SAS Institute, Cary,
NC, USA).
Results
Experiment 1: effects of different species feces
on defecation behavior
In S. miscanthi nests, new fecal piles were often found at
the new sites under the nest roof where different fecal piles
had been placed, and there were no significant differences
in frequency between treatments (G2 = 1.805, df = 3,
P = 0.614; Fig. 2a). In S. longus nests, some of the new
fecal piles were found at the new sites, and there were
significant differences in frequency between treatments
(G2 = 28.129, df = 3, P \ 0.0001; Fig. 2b): the frequency
in the S. miscanthi fecal pile treatment was significantly
lower than that in the control treatment using the fecal piles
from their own nests (G2 = 21.305, df = 1, P \ 0.0001),
whereas there were no significant differences in frequency
between the treatment using the conspecific fecal pile
treatment and the control treatment (G2 = 2.132, df = 1,
P = 0.144), or between the S. takahashii fecal pile treat-
ment and the control treatment (G2 = 0.053, df = 1,
P = 0.819).
Experiment 2: effects of ether-soluble substances
extracted from host plants on defecation behavior
In the S. miscanthi experiments, new fecal piles were often
found at the new sites underneath where the pieces of filter
Leaf under sideWebMite
Original site
Remove
New site
Original site
Move
New site
Treatment using the fecal piles from their own nest (control treatment)
Treatment using the fecal piles from the other nest
From the other nest ofS. TakahashiiS. Micanthior S. longuscon-species
Fecal piles
Fig. 1 Manipulation of the fecal piles in S. miscanthi nests and S.longus nests in experiment 1
J Ethol (2008) 26:267–272 269
123
paper had been placed, and there were no significant dif-
ferences in frequency between treatments (G2 = 0.827,
df = 2, P = 0.662; Fig. 3a). In S. longus, new fecal piles
were sometimes found at the new sites, and there were
significant differences in frequency between treatments
(G2 = 19.755, df = 2, P \ 0.001; Fig. 3b): the frequency in
the M. sinensis extract treatment was significantly lower
than that in the control treatment using fecal piles from the
mites’ own nests (G2 = 16.281, df = 1, P \ 0.0001), and
Their own nest(Control)
Con-species(S. miscanthi )
S. takahashii S. longus
0
20
40
60
80
100
Freq
uenc
y (%
)Fr
eque
ncy
(%)
32 23 26 27
Original site
New site
Original site
New site
Other nest
Treatment
Other nest
Treatment
0
20
40
60
80
10030 16 27 30
Their own nest(Control)
Con -species(S. longus)
S. takahashii S. miscanthi
S. longus
***
NSNS
S. miscnathi
(b)
(a)
Fig. 2 The frequencies of nests where new fecal piles were found at
the new site and the original site in a S. miscanthi and in b S. longusin experiment 1. Horizontal lines show the results of a post-hoc test
(G-test) between the treatments using fecal piles from another nest
and the control treatment when there is a significant difference among
treatments (G-test). NS denotes an insignificant difference at
P \ 0.05. ***P \ 0.001. The number of nests tested (sample sizes)
is given above each bar
M. sinensis S. senanensisTheir own nest
(Control)
0
20
40
60
80
100
Freq
uenc
y (%
)Fr
eque
ncy
(%)
23 1532
Fecal piles Extract from plant
M. sinensis S. senanensisTheir own nest
(Control)
Fecal piles Extract from plant
S.miscnathi
0
20
40
60
80
10023 2330
***
NS
S. longus
Original site
New site
Original site
New site(b)
(a)
Treatment
Treatment
Fig. 3 The frequencies of nests where new fecal piles were found at
the new site and the original site in a S. miscanthi and in b S. longusin experiment 2. The column marked Their own nest is the data from
experiment 1. Horizontal lines show the results of a post-hoc test
(G-test) between the plant extract treatments and the control treatment
when there is a significant difference among treatments (G-test). NSdenotes insignificant differences at P \ 0.05. ***P \ 0.001. The
number of the nests tested (sample sizes) is given above each bar
270 J Ethol (2008) 26:267–272
123
lower than that in the S. senanensis extract treatment
(G2 = 15.061, df = 1, P \ 0.0001). In contrast, the
frequency in the S. senanensis extract treatment was not
significantly different from that in the control treatment
(G2 = 0.004, df = 1, P = 0.948).
Discussion
Two social spider mites, S. miscanthi and S. longus, are
known to use volatile chemical cues from their feces to
manage their waste (Sato et al. 2003; Sato and Saito
2006). In experiment 1, S. miscanthi and S. longus
females tended to defecate at the new sites in response
to fecal piles from other conspecific nests and also to the
fecal piles deposited by S. takahashii in the same manner
as to their own fecal piles (Fig. 2). If S. longus and S.
miscanthi produce their own specific chemicals for waste
management, this phenomenon would be curious because
S. takahashii itself does not use volatile chemical cues
for waste management (Sato and Saito 2006). Therefore,
it can be said that the volatile chemical compounds used
by these two species are commonly contained in the
feces of several Stigameopsis species, and the behavior
of using volatile chemical cues for waste management
might have evolved by using compounds originally
contained in their feces.
At the same time, this study suggests that the volatile
chemical cues used by S. miscanthi and S. longus are not
entirely the same, because the response of S. longus
females to the fecal piles of S. miscanthi was significantly
lower than to their own fecal piles (Fig. 3). We hypothesize
that the reason why S. longus females responded to the
fecal piles of S. takahashii but rarely responded to those of
S. miscanthi might be related to the difference in their host
plants: S. longus and S. takahashii infest the dwarf bamboo,
S. senanensis, whereas S. miscanthi infests the perennial
grass, M. sinensis. This idea was strengthened by the
results of experiment 2: both S. miscanthi and S. longus
females tended to defecate at new sites corresponding to
their respective host plant extracts as well as to their own
fecal piles. However, the latter rarely responded to the M.
sinensis (the host plant of S. miscanthi) extract, even
though it was sufficient to elicit a response from S. mi-
scanthi females (Fig. 3b). These results show that some of
the volatile chemical compounds used for waste manage-
ment in these spider mites originate from their host plant
juices, and that there is a difference in the composition of
volatile chemical cues between S. miscanthi and S. longus
that may be caused by host plant differences.
Why did S. miscanthi females respond to the fecal piles
of S. takahashii and S. longus and to the ether extract of S.
sinanensis (the host plant of S. takahashii and S. longus)
(Fig. 3a)? This question may be explained by their evolu-
tionary history. If the common ancestor of these three
species infested S. senanensis as suggested by Sakagami
(2002), S. miscanthi might have retained an ability to
respond to the volatile cues originating from S. senanensis.
Similarly, if S. longus has lived continuously on S. sen-
anensis, it would have no experience of M. sinensis. If the
composition of volatile chemical compounds or the com-
position ratio differs between M. sinensis and S.
senanensis, then S. miscanthi can be expected to recognize
both types of volatile chemicals originating from the two
host plants as cues for waste management, but S. longus
cannot. To confirm or reject this idea, we must investigate
the composition of the volatile chemical compounds in
greater detail. If these host plants contain volatile chemical
compounds, it would be very helpful for further investi-
gations, because unlike feces, the host plants are easy to
obtain in large quantities.
The utilization of host plants as more than just living
space and food resources has been found in some phy-
tophagous insects and arachnids. For example, plants often
produce secondary compounds to protect themselves
against herbivores and pathogens, and some herbivores
utilize these unpalatable or toxic substances to defend
themselves against their predators and as pheromones (e.g.,
Schulz 1998; Dobler 2001; Nishida 2002). Most reported
examples involve the utilization of herbivore-induced plant
volatiles by herbivores and their predators. Plants often
respond to herbivore infestations by emitting specific her-
bivore-induced plant volatiles. Some predators use these
volatiles to ascertain prey location (e.g., Sabelis and van de
Baan 1983; Vet and Dicke 1992; Takabayashi and Dicke
1996), and some herbivores also use them to avoid host
plants already infested by conspecific individuals (e.g.,
Dicke 1986; Landolt et al. 1999; Sato et al. 1999; De
Moraes et al. 2001). The present study shows that the
volatile chemical compounds used by S. longus and S.
miscanthi for waste management also originate from the
host plants. This waste-management behavior would be
another example of the utilization of host plants as more
than just living space and food resources. It is important to
further develop this study not only from the perspectives of
sociobiology and scatology, but also from the perspective
of herbivore–host plant interactions.
Acknowledgements We wish to thank Drs. Junji Takabayashi,
Yutaka Watanuki, Eisuke Hasegawa, Takane Sakagami, Kotaro Mori,
Katsura Ito, Teruhiko Yoshihara, Yoshito Suzuki, Shun-ichi Miyai,
and Hideshi Naka for their valuable suggestions and help. This work
was supported by Research Fellowships for Young Scientists, by a
Grant-in-Aid for Scientific Research (KAKENHI: B-17370005) from
the Japan Society for the Promotion of Science, and by MEXT
through Special Coordination Funds for the Promoting of Science and
Technology, entitled ‘‘Hokkaido University Sustainable Govenance
Project.’’
J Ethol (2008) 26:267–272 271
123
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