Rules for Nest Sanitation in a Social Spider Mite, Schizotetranychus miscanthi Saito (Acari: Tetranychidae)

Research Papers

Rules for Nest Sanitation in a Social Spider Mite,

Schizotetranychus miscanthi Saito (Acari: Tetranychidae)

Yukie Sato, Yutaka Saito & Takane Sakagami

Laboratory of Animal Ecology, Department of Ecology and Systematics,Hokkaido University, Sapporo, Japan

Abstract

Waste management behavior is essential to achieve nest sanitation that ishighly inferential on the evolution of group living because nest waste is aninevitable cost. However, how group living animals dispose of waste has notattracted much attention. Schizotetranychus miscanthi Saito is a social spider miteinfesting a perennial grass (Miscanthus sinensis Anderss), in which all nestmembers tend to defecate at specific sites. We investigated the mechanisms bywhich the individuals select the site of defecation. The results show that nestmembers defecate at only one site inside the nest, and that waste management ismaintained by two simple rules. First, mites defecate near the nest entrances if novolatile chemical cues are available, and secondly, when chemical cues areavailable from feces deposited previously, they defecate at this site. We discuss theadaptive significance of these mechanisms, as well as their role in the evolution ofsociality in mites.

Corresponding author: Yukie Sato, Laboratory of Animal Ecology, Depart-ment of Ecology and Systematics, Graduate School of Agriculture, HokkaidoUniversity, Sapporo 060-8589, Japan. E-mail: [email protected]

Introduction

Nest sanitation has been found in most social insects and arachnids, frombasal to derived groups (Wilson 1975; Holldobler & Wilson 1990; Choe & Crespi1997). In nest-building animals, negligent defecation habits may increase theprobability of infectious diseases and also decrease the living space within the nest,thereby shortening its longevity. Thus, nest sanitation behavior is an importantadaptation in group-living animals (Lee 1994; Hamner & Parrish 1997).

Waste management behavior is essential to achieve nest sanitation, and hasbeen observed in many social insects and arachnids. For example, in ants, beesand wasps, workers carry the defecation wastes of their queens and larvae outof the nest (Holldobler & Wilson 1990). In some eusocial gall forming aphids,

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soldiers remove honeydew, exuviae and any other waste (such as dead aphids)from their infesting site (Benton & Foster 1992). Furthermore, sub-social crickets,earwigs, webspinners, cockroaches and ambrosia beetles perform nest hygienebehaviors (West & Alexander 1963; Radl & Linsenmair 1991; Edgerly 1997;Kirkendall et al. 1997; Nalepa & Bell 1997).

In the two taxa of group-living mites that have been studied, wastemanagement behavior is also known, and the sociality in mites is often associatedwith waste management behavior (Donze & Guerin 1994; Saito 1995; Saito 1997).The sub-social mesostigmatid mites, Varroa jacobsoni Oudemans and Dichroch-eles phalaenodectes Treat, which infest the brood cells of the European honeybeeand the ear chambers of noctid moths respectively, both show waste managementbehavior (Treat 1975; Donze & Guerin 1994). In 14 group-living (under webnests) tetranychid mite species of the genera Eotetranychus, Oligonychus andSchizotetranychus, waste management behaviors occur in all nine species so farstudied (Saito 1995). They appear to avoid soiling their living space or nests bydefecating only at specific sites (Saito 1983). However, apart from the studies onwaste management in ants (Hart & Ratnieks 2002), very few studies haveaddressed mechanisms for waste management decisions.

Here we investigated the mechanism responsible for establishment ofdefecation site in the social spider mite, Schizotetranychus miscanthi Saito, whichalways deposits fecal piles in a certain place (Saito 1995; Saito 1997). We firstobserved where mites select their defecation site(s). Next we used experimentalmanipulations to determine whether the mites recognize their defecation sites bytactile and/or olfactory stimulus, vision being unlikely because they have veryprimitive eyes that can not form images (MacEnroe & Dronka 1969).

Methods

Biological Materials

Schizotetranychus miscanthi is a phytophagous haplodiploid mite speciesliving gregariously in woven nests on the leaf undersurface of perennial grass(Miscanthus sinensis Anderss; Gramineae). Three generations (at most) overlap ina nest, and the number of nest members is sometimes more than 100. Allindividuals living in the large nest defecate at one specific site. Schizotetranychusmiscanthi comprises two taxonomical groups distinguished by differences in male–male aggressiveness, the relative lengths of male first legs, and by reproductiveisolation between them (Saito & Sahara 1999; Saito 2000; Saito et al. 2000; Satoet al. 2000a,b). In this study, we used a population showing strong male–maleaggression (HG in Sato et al. 2000a,b). We collected S. miscanthi from Tobuko(Nagasaki Prefecture, Japan) on 29 July, 1998. The mites were reared on detachedleaves of the host plant (M. sinensis) under controlled conditions of 23 ± 2�C,40–70% relative humidity (RH), and 15:9 h light:dark cycle. The labora-tory culture was initiated from more than 50 females collected arbitrarily in thefield.

714 Y. Sato, Y. Saito & T. Sakagami

Feces Deposition Patterns

Although we knew from field data that nest members of S. miscanthi depositwaste in certain places, we had no detailed information about where they tend todeposit. To determine the precise pattern of waste depositing behavior, we firstobserved the distribution of deposited fecal piles under laboratory conditions. Forthis purpose we introduced 213 sets of three arbitrarily selected females onto a0.5 · 3.0 cm area of detached host leaf surrounded by water-soaked cotton, andallowed them to construct a nest. Three days after introduction, we recorded thepositions of the fecal piles under a dissecting microscope. If the females mademore than two nests within 3 d, we omitted the trial from the present analysis. Weused different individuals for every trial. This was conducted under conditions of25 ± 2�C, 40–70% RH, and 15:9 h light:dark cycle.

To find out how a S. miscanthi female initially selects its defecation siteduring the process of nest foundation, we filmed the behavior of eight arbitrarilyselected females for 24 h after they had been introduced to a leaf disk. This wasdone using video tape apparatus [a video cassette recorder (VCR): Victor SR-S970, color video camera set: TK-800/TK-U800 (Victor Company, Yokohama,Japan)]. The VCR observations of defecation behavior were conducted under25 ± 2�C, 40–70% RH, and 24 h light conditions.

Manipulation Experiments

We designed manipulation experiments to find out whether female mites usetactile or odor stimuli to maintain their defecation site. If females use only thetactile stimulus of nest structure to maintain the defecation sites, they shouldalways defecate in the same places regardless of the location of the fecal pile(hypothesis 1). If they depend upon olfactory stimuli from their feces, they shoulddeposit their feces at the site of a relocated fecal pile, or an odor extraction thereof(hypothesis 2). To test these hypotheses, we carried out two series of experimentsunder conditions of 25 ± 2�C, 40–70% RH, and 15:9 h light:dark cycle.

Experiment 1

To test whether females use tactile or odor stimuli to select their defecationsite, we introduced females onto a leaf and allowed them to construct a nest asabove. In each of the 30 replicates we used three new females. Three days afterintroduction, when a nest had been constructed, we carried out four treatments asfollows (Fig. 1): Treatment 1 – all the fecal piles that had accumulated at theoriginal site were moved to a new site in the middle section of the nest interior.Treatment 2 – all fecal piles accumulated at the original site were moved to a newsite in the middle section of the nest exterior. Treatment 3 – the fecal piles weresimply removed. Treatment 4 – the fecal piles were not manipulated. The last twotreatments acted as controls for treatments 1 and 2. One day after the abovemanipulations, we checked the location of newly deposited feces.

715Nest Sanitation Mechanisms

If females use nest structure to detect defecation sites, new fecal piles shouldbe found mostly at the original site regardless of whether the old piles had beenmoved or not. Conversely, if females use odor cues, new fecal piles should befound at the new site where the old piles had been transferred to.

Experiment 2

To confirm that volatile odor cues are involved in the detection of defecationsites, we assayed the effect of ether-soluble substances extracted from feces on theselection of defecation sites as follows (Fig. 2). Treatment A: feces (approx. 2 lg)were collected and placed into 200 ll diethyl ether at room temperature for 24 h.The sample was precipitated into a pellet by centrifugation (18 500 g for 15 s).Then a piece of filter paper was soaked in the supernatant (mainly lipid). The filterpaper was then divided into 1 · 1 mm pieces, and one desiccated piece was placedat a new site in the middle of the nest exterior. Treatment B and C: the procedurefor treatment A was repeated, but using distilled water and pure etherrespectively, instead of ether-extracted material. Treatment D: the fecal pilesobtained as sediment after centrifugation in treatment A were washed repeatedlywith ether until de-coloration occurred. The sediment was then desiccated andplaced on a new site in the middle of the nest exterior. As before each treatmentcomprised 30 replicates with different sets of three females in each. The location ofthe fecal piles was recorded 1 d after the manipulation. If the mites use volatile

Fig. 1: Manipulation of the fecal piles to examine the effect of the feces on defecation behavior inexperiment 1


cues for selecting their defecation sites we expect the new fecal piles to befound at the new site in treatment A and at the original site in the three othertreatments.

Statistical Procedures

We used log-linear models to compare the observed and expected frequencydistributions under each hypothesis in experiments 1 and 2 (Sokal & Rohlf 1995).We analyzed the frequency distribution of new fecal piles according to thefollowing three classification criteria: data set (actual vs. expected data), treatment(treatments 1–4 and A–D), location (original or new sites). For each comparisonwe constructed three-dimensional contingency tables comprising two rows(observed and expected data set), four columns (treatments), and two tiers(locations). Zero values in the cells were replaced with 0.5 (Haberman 1978). Themodel is

ln ffijk ¼ l þ ai þ bj þ ck þ abij þ acik þ bcjk þ abcijk ð1Þ

where ffijk represents the expected frequency of new fecal piles for the cellcorresponding to row i, column j and tier k; l is the mean of the log values of theexpected frequencies; a, b and c represent the effect of �data set�, �treatments� and�locations� respectively, and ab, ac, bc and abc represent the pair-wise and three-way interactions of variables.

If the interactions involving a (ab, ac and abc) are not significant, theobserved and expected frequency distributions can be regarded as homogeneous.

Fig. 2: The procedure for the bioassay using ether-extracted feces. The letters A–D refer to the fourdifferent treatments


Alternatively if the interactions involving a are significant, the observed andexpected frequency distributions are significantly different, indicating that theactual data are different from the expected (hypothesized) ones. In order toassess the effect of the interactions involving a (ab, ac and abc), we made theunsaturated model which did not include the interactions involving a (ab, acand abc), and check the change in likelihood ratio chi-square value. Thestatistical analyses were performed using the SPSS Statistical Package Version11.5 (SPSS Japan Inc., Tokyo, Japan).

Results

Feces Deposition Patterns

On all occasions (n ¼ 213), the fecal piles were observed inside the nests. Thefecal piles were mostly concentrated at one site near one nest entrance (87.8%),sometimes at one site in the middle of the nest (8.9%) or at two sites near bothentrances (3.3%).

In the eight nests with a single foundress female, the first deposition of fecesoccurred 6.9 ± 1.46 h (�xx ± SE, n ¼ 8) after beginning nest construction. Thetime from the beginning of nest foundation to the first defecation was significantlylonger than the intervals from one defecation to the next after the initialdefecation (Fig. 3) (anova: F3,28 ¼ 6.46, p < 0.01, Fisher’s protected leastsignificant difference (PLSD): p < 0.01). This suggests that defecation issuppressed during the nest foundation, presumably owing to nest constructionactivities. Thus it was interpreted that a foundress uses tactile stimuli to fix thedefecation site at one site near one nest entrance once it has roughly constructedthe nest.

Fig. 3: The average time (h) from the beginning of nest foundation to the first defecation (1st) and theaverage intervals from one defecation to the next after the first defecation (2nd, 3rd, 4th) with SE bar


Manipulation Experiments

Experiment 1

When the fecal piles had been moved to a new site in the middle of the nestinterior or exterior (treatment 1 and 2), the new fecal piles were found near thenew site in 89.7 and 96.9% of the cases respectively (Table 1). By contrast, whenthe fecal piles had been removed from the original site (treatment 3), the mitescontinued to defecate at the original site in 73.3% of the cases, and near anotherentrance in the remaining cases (26.7%). Because, it could be judged that themites also selected another entrance (with the same structure) by tactile stimuliin the latter case, the data was included in the data of original site in the loglinear analysis (Table 1). When the fecal piles had not been removed (treatment4), the mites continued in 100% of the cases to defecate at the original site(Table 1).

When we used expected values from hypothesis 1, the unsaturated log-linearmodel without the interactions involving a (ab, ac and abc) did not fit to our data(likelihood ratio: v2 ¼ 131.54, df ¼ 7, p < 0.0001), thus the interaction involvinga is significant. This indicates that the observed distributions differ from thoseexpected under hypothesis 1, i.e. that mites do not defecate in the original sitewhen the fecal piles have been moved. By contrast, when we used expected valuesfrom hypothesis 2, the unsaturated log-linear model without the interactionsinvolving a (ab, ac and abc) did fit our data (likelihood ratio: v2 ¼ 2.33, df ¼ 7,p ¼ 0.939). This gave best fit to our data among all possible unsaturated models.This indicates that the observed and expected frequency distributions werehomogeneous, i.e. that mites switch defecation sites when the location of the fecalpiles changed.

Table 1: Observed and expected cell numbers of three-dimensional contingency table inexperiment 1

Data set (a)

Treatment (b)Location of newfecal piles (c)

Actualdata

Expected if mites donot use odor cues

Expected if mitesuse odor

Treatment 1 Original site 3 29 0New site 26 0 29




In treatment 3, the data of near another entrance was included in the data of originalsite. Zero values in the cells were replaced with 0.5, when log-linear analyses wereperformed.


Experiment 2

When the ether-extracted material had been placed at a new site in the middleof the nest exterior (treatment A), the new fecal piles were found near the new sitein 93.3% of the cases (Table 2). By contrast when the material extracted indistilled water and pure ether, respectively, or fecal piles washed by ether had beenplaced at a new site in the middle of the nest exterior (treatment B, C, and D), themites continued to defecate at the original site in, 90.0, 100, and 83.3% of thecases, respectively, and at a new site in the remaining cases.

When we used expected values from hypothesis 1, the unsaturated log-linearmodel without the interactions involving a (ab, ac and abc) did not fit to our data(likelihood ratio: v2 ¼ 70.73, df ¼ 7, p < 0.0001), thus the interaction involvinga is significant. This indicates that the observed distributions differ from thoseexpected under hypothesis 1, i.e. that mites do not defecate at the original sitewhen ether-extracted material had been placed elsewhere. By contrast, when weused expected values from hypothesis 2, the unsaturated log-linear model withoutthe interactions involving a (ab, ac and abc) did fit our data (likelihood ratio:v2 ¼ 7.89, df ¼ 7, p ¼ 0.342). This gave the best fit to our data among all possibleunsaturated models. This indicates that the observed and expected frequencydistributions were homogeneous, i.e. that mites switch defecation sites whenether-extracted material had been placed at a new site.

Discussion

In this study, we have shown that mites settle their defecation site(s) at onlyone site inside the nest, and that waste management is maintained by followingtwo simple rules: First, mites defecate near the nest entrances if no volatilechemical cues are available, and secondly, when chemical cues are availablefrom feces deposited previously, they defecate at this site. The observations on

Table 2: Observed and expected cell numbers of three-dimensional contingency table inexperiment 2

Data set (a)

Treatment (b)Location of newfecal piles (c)

Actualdata

Expected if mites donot use odor cues

Expected if mitesuse odor

Treatment A Original site 2 30 0New site 28 0 30

Treatment B Original site 27 30 30New site 3 0 0

Treatment C Original site 30 30 30New site 0 0 0

Treatment D Original site 25 30 30New site 5 0 0

Zero values in the cells were replaced with 0.5, when log-linear analyses were performed.


defecation patterns show that mites defecate close to entrances in the absenceof chemical cues, whereas the fact that females switched defecation sites inresponse to the experimental manipulations shows that when odor cues areavailable these are used. According to these rules, a foundress who does nothave access to chemical cues fixes the defecation site by tactile stimuli just afterconstructing the framework of her nest. Thereafter, the foundress as well asindividuals that join the nest later deposit their feces at the fixed site based onodor cues.

This begs the question why not only tactile stimuli are used. There are severalpossible adaptive reasons for using volatile chemical cues from feces rather thantactile cues. The nest has a simple structure much like a tunnel, and it has twosimilar-shaped entrances. If the entrance structure is the only tactile cue by whichto recognize the defecation site, there will inevitably be two defecation sites.Because nests are often extended continuously at either end, double defecationsites may disturb nest extension. Furthermore, as mites suck the sap of the hostplant juice, their feces are watery. Touching watery feces is very dangerous formites, because they can easily become trapped by the feces, and die. Therefore, ifthe mites always tend to defecate at the �entrances� using only by tactile cues, theymay face several difficulties. Thus, we believe that by using chemical cues,defecation at the site where feces have been already deposited is an appropriatesolution to this problem.

Nest sanitation is closely related to the development of sociality in mites(Donze & Guerin 1994; Saito 1995; Saito 1997), so any differences in themechanism of waste management between closely related species should offeruseful information about the evolution of sociality in mites. S. miscanthi is amember of the celarius species group Ehara in which there are three social andfour subsocial species (including two new species under description, Saito et al.,unpubl. data). All species of this species group are characterized by group livingin web-nests and the behavior that all individuals within a nest defecate at one ortwo specified places near the entrances of their nests (Saito 1983). However, it isknown that there are several differences in nest size, group size, defense behaviorand detailed defecation patterns (Saito & Takahashi 1982; Saito 1997; Mori2000). Schizotetranychus miscanthi has the most developed sociality showing thelargest colonies, greatest overlap between generations in a nest, cooperative nestfoundation, and cooperative bi-parental care (Saito 1995, 1997). In relation to theevolution of sociality, future studies on whether the proximate mechanism ofwaste management identified in this species is common to the species of this groupshould be greatly interesting.

We found that the mites use volatile chemical cues from feces to recognizethe defecation site. In mammals, reptiles, amphibians and insects, wastes arecommonly used as information, for example, to recognize the defecation site,territory, aggression or dominance behaviours, or sexual advertisement (e.g.Wilson 1975; Rosell & Sundsdal 2001; Lee & Waldman 2002; Zenuto & Fanjul2002). In social insects feces are not used as sources of information, but rathercomplex chemical compounds (Detrain et al. 1999). In spider mites, there is a


possibility that fecal odor is used not only to recognize the defecation site but alsoto get other information. If mites leave their original nests for some reason, theymust construct new nests or enter other nest shelters nearby. Indeed, we oftenobserved several foundresses in a nest just founded. Unless females dispersetogether to found new nests jointly, they may use odor cues from feces to locateother females or nests. The chemicals from feces possibly play an important rolein such a group formation process.

However, it is also known that some predators or parasitoids use olfactorycues from the feces of their prey to search for prey (Mattiacci & Dicke 1995;Meiners et al. 2000; Schaffner & Muller 2001). There is also a possibility that theodor from spider mite’s feces is used by predators to search for prey in micro-scale, because predator mites are known to locate spider mites using olfactorycues produced by the infested plants in macro-scale (Sabelis & Baan 1983; Dick1998). The relationship between predator behavior and prey feces is also worthstudying in the future.

Acknowledgements

We thank Drs Eisuke Hasegawa, Hideshi Naka, Junji Takabayashi, Kotaro Mori, TeruhikoYoshihara, and Yutaka Watanuki for their valuable suggestions and help. We also appreciate theefforts of Dr A. R. Chittenden who kindly reviewed the manuscript. This work was supported byResearch Fellowships of the Japan Society for the Promotion of Science for Young Scientists, and byGrants-in-Aid (nos. 13575021 and 13440227) for Scientific Researches from JSPS.

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Received: September 25, 2002

Resubmitted: March 6, 2003

Initial acceptance: March 18, 2003

Final acceptance: April 30, 2003 (L. Sundstrom)


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Rules for Nest Sanitation in a Social Spider Mite, Schizotetranychus miscanthi Saito (Acari: Tetranychidae)