Bonnie J. Bobula Smith and Barry D. Valentine.
Phylogenetic implications of grooming behavior of cockroaches (Insecta: Blattaria).
Psyche 92:369-386, 1985.

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PHYLOGENETIC IMPLICATIONS OF
GROOMING BEHAVIOR IN COCKROACHES
(INSECTA: BLATTARIA)*
Department of Zoology, The Ohio State University, Columbus, Ohio 43210-1293
The use of behavioral data for the investigation and delineation of evolutionary relationships has been increasingly heuristic (Evans, 1952; Speith, 1952; Alexander, 1962; etc.). In insects, grooming behavior seems particularly useful because it is a widespread and prominent part of their behavioral repertory. Comparative studies of several orders have been based on grooming behavior (Szy- manski, 1918; Heinz, 1949; Gangwere, 1958; Jander, 1966; Parish, 1972; Valentine, 1973; Valentine and Glorioso, 1979). Lipps (1973) provides an excellent review of grooming literature. The cockroaches are a diverse group with an extensive nontaxo- nomic literature. There are many descriptions of the general biology of the order (Gould and Deay, 1938; Roth and Willis, 1954, etc.) and of particular species (Qadri, 1938; Rau, 1940; Dow, 1955; Hes- lop and Ray, 1959, etc.). Roth and Willis (1954) and McKittrick (1964) summarize many such papers, especially on biology. Our taxonomy follows McKittrick (1964), and is summarized in Table 1. Unspecified grooming behavior of cockroaches is mentioned by Patton (1941) and Burkholder (1965). Others discuss grooming of particular body parts (Haber, 1920; Mote, Wilcox, and Davis, 1926; Roth and Willis, 1952 and 1954; and Eisner, 1961). A few authors are more detailed: Gangwere (1958), Yoshikawa (1958), Baton and Parley (1969), and Lipps (1973). The most complete description of roach grooming is by Turner (1913), who describes in excellent detail antennal, palpal, and leg cleaning using the mouth, and the use of a leg to rub the base of the antenna and dorsal surface of the abdomen, all in a roach he called Periplaneta orientalis, now placed in the genus Blatta.
*Manuscript received by the editor July 15, 1985.



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3.JU Psyche [VOI. 92
The above references give a very incomplete picture of roach grooming. Gangwere (1958) and Lipps (1973) discuss roaches from a generalized view, but the species are not named nor are their individual repertories described. No work investigates the order and tries to characterize grooming patterns within it, and no work des- cribes the complete repertory of even one species. Grooming behavior was recorded during 154 hours of observa- tions on 23 species representing 20 genera and four families of Blat- taria (see Table 1). The grooming movements performed by each species are listed in Tables 2 and 3. Terminology follows Valentine and Stouffer (in preparation). Since there are over 3,500 species of cockroaches, a few exceptions to the family patterns we present are to be expected.
Small and large species were maintained in 9 and 12 cm white cardboard medical specimen cups with clear plastic lids. Lightly crumpled paper provided cover, and bits of dog biscuits and small water-soaked cotton balls provided food and water. Cryptocercus punctulatus was maintained in a 9 cm cup containing pieces of the log in which it was discovered. This debris provided food and was lightly misted every other day.
Each common species was observed for at least four hours. The longer observation periods listed in Table 1 provided no additional behaviors. Monospecific groups of 5 to 7 individuals were observed for 10 minutes in the maintenance cup with the paper removed. Then, single roaches were observed for not less than 20 minutes. A new cup was used for each species. Species 20 mm long and larger were observed directly; those less than 15 mm were observed with a dissecting microscope. Observations were made at most hours of the day or night, either in artificial or existing natural light. In the cases of Blaberus craniifer and Cryptocercus punctulatus, the light was fitted with a red cellophane filter. After grooming behavior of groups and individuals had been recorded for at least four hours for a particular species, further grooming was elicited by dusting 3 to 5 roaches of each species with household flour and observing these individuals for an average of an additional 20 minutes.



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Table 1.
Number of individuals and time spent observing each species CRYPTOCERCIDAE
Cryptocercus punctulatus Scudder 2
BLATTIDAE
Blattinae
Blatta orientalis Linnaeus 7
Periplaneta australasiae (Fabricius) 6
Periplaneta brunnea Burmeister 6
Periplaneta americana (Linnaeus) 6
BLATTELLIDAE
Plecopterinae
Supella longipalpa (Fabricius)
Blattellinae
Blattella germanica (Linnaeus)
Xestoblatta immaculata Hebard
Nyctiborinae
Nyctibora lutzi Rehn & Hebard
BLABERIDAE
Zetoborinae
Schultesia lampyridijormis Roth 12
Blaberinae
Eublaberus posticus (Erichson) 6
Archimandrite! tessellata Rehn 5
Byrsotria fumigata (Gubrin) 4
Blaberus craniifer Burmeister 4
Pycnoscelinae
Pycnoscelus indicus (Fabricius) 6
Pycnoscelus surinamensis (Linnaeus) 8
Diplopterinae
Diploptera punclata (Eschscholtz) 7
Panchlorinae
Panchlora nivea (Linnaeus) -30
Oxyhaloinae
Leucophaea maderae (Fabricius) 12
Nauphoeta cinerea (Olivier) 7
Jagrehnia madecassa (Saussure) 6
Gromphadorhina portentosa (Schaum) 6
Perisphaeriinae
Gyna sculpturata Shelford -24




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Psyche
CLEANING.
Involves chewing movements of the mouthparts. Antenna Clean: Two major modes of antenna cleaning were observed: Assisted and Unassisted. The Assisted mode is subdivided into three submodes: Bipedal, Contralateral, and Ipsilateral. 1. Assisted.
a) Bipedal: This movement was observed only in Periplaneta brunnea of the family Blattidae. Both forelegs simultaneously move upward and grasp one antenna as it and the head are bent down- ward. The head is then raised and the antenna pulled into the mouth by the crossed forelegs.
b) Contralateral: This movement was confined to and observed throughout the families Cryptocercidae, Blattidae, and Blattellidae. The antenna is deflected downward as the contralateral foreleg moves upward and contacts the antenna. The head is raised and the antenna is pulled into the mouth by the leg. c) Ipsilateral: Alternating with Unassisted, this movement was observed exclusively in the family Blaberidae. It resembles Contra- lateral except that the ipsilateral foreleg is used. 2. Unassisted.
Alternating with Ipsilateral, this method was observed exclu- sively in the Blaberidae. The antenna deflects into the mouth using its intrinsic musculature. There is no leg assistance, but the antenna may occasionally be trapped against the substrate. Once the antenna is in the mouth, two aspects of antenna cleaning are constant in all species: a single antenna is cleaned at a time, and in species assisting with the foreleg, the antenna is released by the leg as it is grasped by the mouthparts.
Palpus Clean: Palpal cleaning was observed in all species. The labial and maxillary palpi are cleaned similarly. A single palp is curled directly into the mouth from the normal resting position. Either the entire palp or only the tip is cleaned. Leg Clean: With three exceptions, all species clean all three legs. Cryptocercuspunctulatus performs no leg cleaning, and two species in the family Blaberidae, Pycnoscelus surinamensis and Leucophaea maderae, were never observed to clean the hindleg. 1. Foreleg Clean: A foreleg is raised and extended forward as the head turns to reach it. The body is supported in a normal resting position by the remaining five legs. The mouthparts contact the leg



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at any point and clean it by slowly chewing from the point of con- tact to the end of the tarsus.
2. Midleg Clean: As the ipsilateral foreleg is raised and the head turned backward, a midleg is raised and extended forward under the body and raised foreleg. The body is supported by the ipsilateral hindleg positioned slightly farther forward than usual, the three opposite legs, and sometimes by the side of the abdomen. 3. Hindleg Clean: This movement resembles Midleg Clean. The foreleg is raised, followed closely by the midleg as the head dips down and back, and the hindleg swings forward underneath the raised fore- and midlegs. The tip of the abdomen is curled laterally toward the head, and the body is supported in a fourpoint stance by the curled abdomen and the three legs of the opposite side. If only the tibia1 apex or tarsus is cleaned, the midleg may remain in contact with the substrate.
Certain features are common to all leg cleaning in all species. The leg is usually raised from the substrate, and is always held ventrally. Movement of the leg relative to the head is always posterior, back and forth movement in the mouth did not occur. Cleaning may begin at any level from coxa to tarsus, and once begun continues from point of contact to the end of the tarsal claws. The leg or parts of the leg may be cleaned once or several times in succession. There is no set order for legs to be cleaned, and leg cleaning may be interspersed with grooming of other body parts. Body Clean: Grooming the body with the mouthparts has only two modes in roaches.
1. Sternum Clean: Sternal cleaning is well-distributed through- out the families and genera (see Table 2). The body is slightly raised by extension of the legs, and the forelegs are widely spaced. The head bends down under the body until the mouthparts reach the coxae of the forelegs. These and the area between them are cleaned. Similar cleaning of the sternal and coxal area of the meso- and metathorax did not occur.
2. Pronotum or Wing Edge Clean: This is a much rarer move- ment than Sternum Clean, and was observed infrequently in only six species (see Table 2). The head is turned to the side and either the edge of the pronotum or the wing base just behind it is cleaned. RUBBING.
Involves progressive contact of body parts with other parts, or rarely, with the substrate.




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Table 2.
Cleaning Movements of Roaches
u
CRY PTOCERCIDAE
Cryptocercus punctulatus C x
BLATTlDAE
Blatia orienzalis C x x x x
Periplaneta australasiae C x x x x
Periplaneta brunnea B,C x x x x
Periplaneta americana C x x x x
BLATTELLIDAE
Supella longipalpa C x x x x
Blattella germanica C x x x x
Xestoblatta immaculata C x x x x
Nyctibora luizi C x x x x
BLABERIDAE
Schultesia lampyridiformis
Eublaberus posticus
Archimandrite! tessellata
Byrsotria fumigates
Blaberus craniifer
Pycnoscelus indicus
Pycnoscelus surinamensis
Diploptera punctata
Panchlora nivea
Leucophaea maderae
Nauphoeta cinerea
Jagrehnia madecassa
Gromphadorhina portentosa
Gyna sculpturata
u x x x x
U.1 x x x x
U.1 x x x x
u x x x x
U x x
U.1 x x x x
U.1 x x x
I x x x x
U.1 x x x x
I x x x
I x x x x
I x x x x
I x x x x
u x x x x
Note: U - unassisted
C - assisted -contralateral
I - assisted - ipsilateral
B - assisted - bilateral
'indicates movements performed only after application of flour



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Antenna-Foreleg Rub: This movement was performed by all spe- cies observed except C. punetulatus. The basal segments of the antenna not reached by the mouthparts during Antenna Clean are groomed by rubbing. The base of the antenna is caught in the crook of the tibio-femoral joint, and the foreleg very deliberately and slowly moves down in a scraping motion. This movement is often followed by Foreleg Clean, but is not consistently combined with Antenna Clean.
Head-Foreleg Rub: Two forms were observed (see Table 3). 1. Eye-Rub: This movement was observed in all species but C. punctulatus. The foreleg is raised and the area of the tibio-femoral joint contacts the eye just below the antenna1 base. The leg moves straight down in a short, sharp rub reaching most of the eye surface. 2. Low Face Rub: This movement was observed in all species. It is similar to Eye Rub, yet distinct. The area of the head contacted is restricted to the lateral mouth region.
Prothorax-Foreleg Rub: Individuals of a single species, Supella longipalpa, raise a foreleg so that the femur contacts the lateral margin of the prothorax and performs a quick series of two to five posterior strokes.
Abdomen-Hindleg Rub: This movement is well-distributed throughout the families. Only two blaberid species, Archimandrita tessellata and Gromphadorhina portentosa, were not observed to perform some type of abdomen rub. Dr. Louis M. Roth, in a most useful review of this manuscript, informs us that some other blaber- ids omit abdomen or wing rubs. He points out that the bodies of Laxta females are often solidly caked with dirt, and the tegmina of Therea nuptialis have small setae which retain debris and make the insects less conspicuous.
A hindleg is used to rub the dorsal, ventral, and/or lateral sur- faces of the abdomen. The movement is always unilateral: an insect may alternate sides rapidly, but only one hindleg ever touches the body at one time. The direction of the rub is posteriad. Often, but not consistently, abdomen rubbing is followed by hindleg cleaning. Cercus-Hindleg Rub: Cercus rubbing is present in most of the species observed (Table 2). Cereus-Hindleg Rub is a separate and elaborate movement quite distinct from abdomen rubbing. The ipsilateral hindleg rubs any part of the cercus; at times, only the very tip. The abdomen may or may not be curled toward the rubbing leg.



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,
Table 3. Rubbing and positioning movements of roaches CRYPTOCERCIDAE
Cryptocercus punctulatus
BLATTIDAE
Blatta orientalis
Periplaneta australasiae
Periplaneta brunnea
Periplaneta americana
BLATTELLIDAE
Supella longipalpa
Blattella germanica
Xestoblatta immacula~a
Nyctibora lutzi
BLABERIDAE
Schultesia lampyridiformis
Eublaberus posticus
Archimandrita tessellata
Byrsotria furnigata
Blaberus cranifer
Pycnoscelus indicus
Pycnoscelus surinarnesis
Diploptera punctata
Panchlora nivea
Leucophaea maderae
Nauphoeta cinerea
Jagrehnia madecassa
Gromphadorhina portentosa
Gyna sculpturata
x x x x x x x x
x x X X X x
x x X X X
* x X X * *




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Some individuals of the more primitive species spend up to two minutes engaged solely in this grooming movement. Abdomen-Substrate Rub: Two of the smaller species (length less than 15 mm), Blattella germanica and Diploptera punctata, were observed to occasionally twist the abdomen sideways and drag the edge and part of the dorsal surface against the substrate. The wings are maintained in their normal position or raised a bit, resulting in only the abdomen contacting the substrate. Hindleg-Hindleg Rub: Individuals of only two species, S. longi- palpa and Schultesia lampyridiformis, place one hindleg slightly further under the body than normal and rub it several times from tibia to tarsus with rapid strokes of the tarsus of the opposite hind- leg. Often the movement is reversed, and the other hindleg is rubbed similarly.
Wing-Hindleg Rub: A few individuals of three species, S. longi- palpa, Nyctibora lutzi, and L. maderae, rub the dorsal surface of the closed wings with the tarsus of a hindleg, while the abdomen is in its normal resting position beneath the wings. This movement was always performed while Abdomen-Hindleg Rub was in progress. Wing-Abdomen Rub: Several species in the families Blattellidae and Blaberidae (see Table 2) rub the underside of the closed wings vigorously and elaborately with the abdomen. There are four sepa- rate techniques. First, the abdomen may be rubbed from side to side in its normal position below the wings. Second, the abdomen may be flexed strongly, concave to the substrate, and the wings rubbed with only the central bent portion (of the abdomen). Third, the abdomen may be flexed strongly, convex to the substrate, and the tip of the abdomen rubbed in a circular or lateral motion against the underside of the wings. Finally the abdomen may be twisted so that only the lateral edge contacts the wings. When performed, these movements were almost always of longer duration than other grooming, and were usually performed between, or even during periods of extensive locomotion.
Wing Flip: In Blaberidae, a period of wing flipping was some- times observed in conjunction with Wing-Abdomen Rub. The flip- ping could also be performed alone. Bouts last two to five minutes, with wings either flipped vertically or horizontally.



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Prior to discussion of specific grooming movements, several gen- eralized comments can be made regarding all species observed. Except for Abdomen-Substrate Rub observed in two species, grooming in roaches is restricted to cleaning, or rubbing one body part with another. Other orthopteroids are known to utilize droplets of fluid in grooming (Allard, 1929). Though some individuals observed in this study placed droplets of clear fluid from the mouth onto the substrate, none utilized the droplet in grooming. Though isolated grooming movements are often interspersed with periods of general activity, the most extensive and complete bouts are nearly always preceded by periods of relative quiet lasting two to seven minutes. No set sequence of grooming movements is discern- ible in any individual or species. Any combination or sequence of movements is possible, including repetitions of a particular move- ment, Larger species (> 45 mm) display a strong tendency to per- form all grooming movements less frequently than the smaller species.
Generally, the use of flour as a stimulus has its greatest effect in simply increasing the frequency of movements in the next grooming bout. However, some species perform movements in the presence of flour which are not observed in its absence. Such movements are noted in Table 2 by an asterisk. Movements that are most consist- ently affected are basal antenna1 rubbing, abdomen rubbing, wing- abdomen rubbing, and wing flipping.
An overall inhibiting factor is the presence of barometric low pressure. In advance of fronts and when under low pressure cells, all species exhibit a tendency to remain relatively quiet. With a single exception, all species quickly became habituated to sunlight and artificial light. Grooming activity is readily performed at any hour of the day or night, even in bright light. Blaberus craniifer presents the single exception. In this species, the only grooming performed in daylight or lamplight was antenna and palp cleaning. Whether or not dusted with flour, when exposed to light the animal cleaned only the antennae and palpi, then arranged itself with the head, antennae, and legs drawn under the pronoturn and wings, and sat unmoving until darkness fell or it was placed in a dark environment. During dark hours, the animal could be heard moving vigorously around the cup. On numerous occasions, the



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appearance of the roach's body the next day clearly indicated that leg cleaning and abdomen, cercus, and basal antenna rubbing had been performed. Using a red filter, two additional movements were observed: Foreleg and Pronotum Clean. Unfortunately, the single specimen died before a complete repertory was observed. Ordinal Patterns.
The most striking characteristic of grooming in the order Blatta- ria is the remarkable stereotypy of the movements. In grooming a particular structure, one method usually suffices for all species. Despite varied habitats as living in loose sand, or flowers, or in bird nests (Roth, 1973), roaches groom legs, palpi, head, and abdomen in the same way.
Stereotyped methods and modes of grooming may be explained by considering the generalized anatomy of the group and the natural habitats of the species. The cockroaches are a very ancient order little changed in morphology since their time of dominance in the Carboniferous Period. Fossil and contemporary roaches are ana- tomically very similar. Since extant species are not substantially different in external morphology from either ancestral species or each other, there has been little or no pressure to evolve new groom- ing patterns to deal with specialized anatomical constraints. Also, roaches are cosmopolitan in their distribution and superficially diverse in their habitats. Unlike interstitial Diplura (Valentine and Glorioso, 1979), none of these habitats places undue physical restric- tions on the animals. Roach habitats are cryptic, but none confines a species exclusively to cramped quarters, therefore there is no evi- dence for selection favoring open-ended and complex repertories like those of Diplura.
Familial Patterns.
Discussion of familial trends in grooming behavior lends greatest insight into roach phylogenetic relationships. Some differences exist at other taxomonic levels (Bobula, MS), but these are either incon- sistent or based on small sample sizes.
The grooming movement most useful in interpreting blattarian phylogeny is Antenna Clean. Other movements form less clear pat- terns among groups and hence offer no aid in clarifying general phylogenetic relationships.
Based on trends in Antenna Clean, consistent familial differences exist between the families with generalized reproductive behaviors



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(Crypt ocercidae, Blattidae, Blat tellidae) and the more specialized