6
ARTICLE Evolutionary view of waste-management behavior using volatile chemical cues in social spider mites Yukie Sato Yutaka Saito Received: 19 January 2007 / Accepted: 24 July 2007 / Published online: 13 November 2007 Ó 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 Á Nest sanitation Á Waste management Á Volatile chemical cue Á Host plant shift Introduction Many social insects and arachnids keep their nests sanitary (Wilson 1975; Saito 1983, 1995, 1997; Ho ¨lldobler 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 Á 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

Evolutionary view of waste-management behavior using volatile chemical cues in social spider mites

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Page 1: Evolutionary view of waste-management behavior using volatile chemical cues in social spider mites

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

Page 2: Evolutionary view of waste-management behavior using volatile chemical cues in social spider mites

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

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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

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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

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Page 5: Evolutionary view of waste-management behavior using volatile chemical cues in social spider mites

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

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