Diana E. Wheeler.
Behavior of the ant, Procryptocerus scabriusculus (Hymenoptera: Formicidae), with comparisons to other cephalotines.
Psyche 91:171-192, 1984.

Full text (searchable PDF, 1748K)
Durable link: http://psyche.entclub.org/91/91-171.html

The following unprocessed text is extracted from the PDF file, and is likely to be both incomplete and full of errors. Please consult the PDF file for the complete article.

PSYCHE
Vol. 91 1984 NO. 3-4
BEHAVIOR OF THE ANT, PROCRYPTOCERUS
SCA BRIUSCULUS (HY MENOPTERA: FORMICIDAE), WITH COMPARISONS TO OTHER CEPHALOTINES
Smithsonian Tropical Research Institute
Apartado 2072, Balboa, Republic of Panama and
*Museum of Comparative Zoology Laboratories Harvard University, 26 Oxford Street
Cambridge, Massachusetts 02 138
INTRODUCTION
Cephalotini is a well-defined tribe of Neotropical, arboreal ants of exceptional appearance, containing about 110 species in 4 genera (Kempf, 1973). Cephalotines can be distinguished from all other ants on the basis of the proventricular valves, which are sclerotized and shaped somewhat like the head of a mushroom (Emery, 1888; Kempf, 1951). The unusually thick exoskeleton bears generous sculpturing that can include numerous striations, ridges, and flanges, as well as protective spines. The four genera have an unusu- ally complete array of worker caste systems for such a small tribe. The genus Procrvptocerus, containing 28 species, is typically monomorphic. Eucrvpiocerus also has a monomorphic worker caste, but contains only 3 rare species. In Cephalotes, workers typi- cally have a wide size range, and in Zucrvptocerus, worker castes range from polymorphic to dimorphic and include the most highly modified soldier forms (Kempf, 195 1, 1973). *Address for correspondence
Manuscript received hj the eciilor Mu.\ 16, 1984



================================================================================

Psyche
[Vol. 91
The behavior of Cephalotes atratus (Corn, 1980) and Zacrvptoce- rus varians (Wilson, 1976; Cole, 1980) have been examined in detail. Both Wilson (1976) and Corn (1980) stressed the importance of studying the divergent genus Procr~ptocerus in order to factor out behaviors that are related to ecological peculiarities from those tied to the evolution of polymorphism within the tribe. Among cephalo- tines, Procrvptocerus appears, at least superficially, most similar to typical myrmicine ants because the head and thorax lack elaborate spines and flanges. Further, since the worker caste is monomorphic, and therefore less complex than in other cephalotines, it has been assumed to be the most primitive genus of the tribe. The species P. scabriusculus is found from Mexico to Venezuela (Kempf, 1972). It nests in dead wood, principally twigs, and forms polydomous, polygynous colonies. Here I present the results of a behavioral study on workers and queens of P. scabriusculus as a contribution towards understanding the biology of this species and the relationship between behavior and polymorphism within the Cephalotini.
METHODS
Nests of P. scabriusculus were collected in Escazu, near San Jose, Costa Rica. Three clusters of inhabited twigs were taken in late August, 1983, from Spondias purpurea. The colony observed in this study was extracted from 3 closely spaced dead twigs and presumed to be a major part of a single colony. It contained 6 queens, 62 workers, 10 worker pupae, 1 male pupa, 49 larvae, and 27 eggs. Both trophic and normal eggs were present. One additional colony was collected in a fig tree in November, 1982. The observation nest was a 100 X 15 mm plastic petri dish. A small test tube, containing water held back by a cotton plug, was placed in the center of the dish to provide moisture and a nest site. The petri dish fit easily on the stage of a dissecting microscope. Observations used for the ethogram were made over a period of 7 days. During this period, the colony was supplied with diluted honey and dead insects. The honey was quickly consumed by workers, but the insects were rarely touched. Occasionally, workers appeared to be drinking the body fluids of freshly killed insects. The colony was observed for a total of 20 hours, in 40 30-minute obser- vation periods. During each 30 minute period, the nest was scanned



================================================================================

19841 Wheeler - Behavior of Procrvptocerus 173 every 2 minutes. Therefore, if an act lasted 30 minutes, it would be recorded 15 times.
Most of the periods of observation fell between 0900 and 2300, but ants were also watched at 0200,0400, and 0600. The colony was exposed to light from dawn (0500) until room lights were turned off (2100-0200). Under these conditions, the colony was arrhythmic; no regular differences in activity levels or types of behaviors were noted. Pupal to adult molts took place at different times of day and night. Molting is strictly tied to the biological clock in many insects, and the fact the molting was irregular suggests that the colony was physiologically, as well as behaviorally, arrhythmic. The behavioral repertoire was analyzed using a FORTRAN pro- gram written by R. Fagen for catalogue analysis using a log normal fitting procedure developed by Bulmer (1974) (Fagen and Goldman, 1977; Fagen, 1978).
Colonies of Zacryptocerus minutus and Z. christopherseniwere collected in central Panama. Various observations are reported here for comparison with the biology of P. scabriusculus. RESULTS
CHA RA CTERIZA TION OF THE FEMA LE CASTES Two characteristics of the genus Procryptocerus are that the worker caste is monomorphic and that queens are slightly larger but very similar to workers (Kempf, 1951). The 2 female castes are compared graphically in Figure 1, in which head width is plotted against thoracic width. The size range of workers is so narrow that this caste can be considered monomorphic. Head widths of P. sca- briusculus workers ranged from 1.14- 1.36 mm, a difference of only 0.22 mm. This is trivial in comparison to Z. minutus (0.96-1.7 mm) and Z. christopherseni (1.42-2.66 mm), 2 species with distinct sol- diers. In C. atratus workers, head width across the occipital spines ranged from about 2-4.5 mm (Corn, 1980). Queens are morphologically similar to workers, but can be distin- guished from workers on the basis of a variety of quantitative as well as discrete differences. As shown in Fig. 1, queens can be dis- tinguished from workers on the basis of thoracic width. Other char- acters that are caste-specific are abdomen width and length, thoracic morphology, including wing scars, and the presence of ocelli.



================================================================================

174 Psyche
[Vol. 91
workers
queens
e . . .
. 0 . .
0 0 0 . .
thorax width (mm)
Fig. 1. Bivariate plot of morphological measurements lor workers and queens. Six of filled circles indicates, in order of increasing si~e. 1. 2. 3, 4. and 5 or more individuals. Workers: n=136. slope=0.74. correkition=0.$2. Queens: n=33. slope= 0.77. correlation=O.S9. Data are from two colonies. WORKERS
A total of 6823 behavioral acts were performed by workers and recorded over a period of 20 hours. These are presented by category in Table 1. Workers performed 31 types of acts, and, using the methods of Fagen and Goldman ( 1977), and Bulmer (1974), a true repertoire size of 3 1 was estimated. The range of the 95% confidence interval was less than 1 act. It must be emphasized that this level of accuracy applies only to the context in which the ants were observed. Undoubtedly, other behaviors would be expressed under other conditions, such as attack. Also, behaviors that are very rare or that are partially suppressed under laboratory conditions may not be recorded. Egg laying, for example, was not observed during this study. The following worker behaviors listed in Table 1 are treated in greater detail below: abdominal trophallaxis, transfer of liquid food (=regurgitation, oral trophallaxis), self-grooming, fate of infrabuccal pellets, excavating, and antenna1 tipping. In addi- tion, several behaviors not included in the ethogram are discussed: stridulation, defense, and miscellaneous leg movements.



================================================================================

Abdominal t~~ophal/a.~i.s
Both Wilson ( 1976) and Cole (1980) found that Z. variant exhi- bited a behavior rarely found in ants. abdominal trophallaxis. This behavior has not been observed in the only other cephalotine pre- viously studied, C. atratus (Corn, 1980). Here 1 report that P. scu- hriu.scu/u.s also exhibits abdominal trophallaxis. The behavior was observed primarily in individuals that had just emerged. Within hours after a worker eclosed and was able to walk, it initiated abdominal trophallaxis, licking the abdominal tip of a nestmate. Single contacts lasted as long as 30 minutes, and the same individual engaged in additional, shorter contacts over a period of several hours. Brief periods of abdominal trophallaxis between older workers and between a worker and a queen was also observed. These contacts were much shorter than the contacts involving cal- lows, generally less than 10 seconds and frequently only 1-2 seconds.
The function of this unusual ant behavior remains unknown. The fact that callows, newly molted individuals, seek out the substance is reminiscent of proctodeal feeding so well documented in lower ter- mites (Cleveland, 1926). Such behavior would be appropriate for transferring essential gut flora to newly ecdysed adults. Finally, it is a suspicious coincidence that cephalotines have two unusual charac- ters apparently associated with the digestive tract: the mushroom- shaped, sclerotized proventricular valves and abdominal trophal- laxis. Perhaps these ants have undiscovered dietary peculiarities. Outside the cephalotines, abdominal trophallaxis has been reported between the slavema king ant. Ha17mgo.t-enus a~~~e~-icanu.s, and its host species, Leptothora.~ amhiguus and L. longiM?inosu.s. Workers and queens of H. umericanus occasionally assume a stereo- typed posture, with the abdomen raised, and exude a droplet of fluid which is consumed by workers of the host species (Stuart, 1981). This unusual case of interspecific trophallaxis undoubtedly has an entirely different function than the type of abdominal tro- phallaxis described in cephalotines which occurs primarily between callow and fully pigmented workers.
Tran.sfe/* of liquid, food
Workers of P. .scahriu.scu/u.s exchange liquid food at moderately high rate in comparison other cephalotines. 15.9% of total acts per- formed by workers involved exchange (donating plus soliciting) of



================================================================================

176 Psyche [vo~. 91
'I-iihlc 1 .
tjcha\ioitil repertoire of PI.ocI~,I.~KHIJ~~~.\ muhriii.\culii.s. Number of acts and relative frequencies observed in 20 hours. Acts Workers
Queens
Sell-groom
iintenniie iind legs 1945( .2851) 75( .2517) ithdomcn and legs 86( .0126) 2( ,0070)
lick iihd~~~liriiil tip 16( .0023)
Antcnniil tipping 48( ,0070)
Ahdomini11 trophitllii~i~
eiillow licks worker
worker licks worker
worker licks queen
Solicit kind or donate liquid food
with worhcr
with queen
Solicit from Iiir\ ac
Inl'riihuccal pellets
extrude
help nestmiite extrude
Cil rl'!
Allogroom
w orker
queen
Fat
egg
lim a or pupil
unidentified brood
hone!,
l.ick
egg
lariii
pupa
lick molting pupil
new emergent
Manipulate. can\. drag
egg
larva
pupa
callow
l.ick wall of nest 60( .0088)




================================================================================

19841
Wheeler - Behavior of' Prucryptocerus
Table 1. (continued)
--
Acts Workers Queens
Debris
carry. manipulate 178( .0261)
lick I I( .0016)
Total number of acts 6823 1 .OOOO) 298( 1 .OOOO) food with another adult ant. Since donating and begging are com- bined, the number must be halved to be compared to the "regurgita- tion with" category reported in other behavioral repertoires. This figure (8.0%) is higher than in C. atratus, where donating made up about less than 2% of worker acts (Corn, 1980). It is much lower than the relative frequency of exchange found in Z. varians by both Wilson (1976) and Cole (1980), 22.8% and 21.3% respectively, as the rate of regurgitation in minor workers. Z. varians soldiers have a more limited repertoire than minor workers and devote over 40% of their behavioral acts to exchange of liquid food (Wilson, 1976; Cole, 1980).
The relative frequency of exchanging liquid food in P. scahriuscu- lus is moderately high in comparison to other myrmicine ants. Pogon~rmex badius lacks the behavior entirely (Wilson and Fagen, 1974). In Orectognathus versicolor, an advanced dacetine, relative frequency of oral trophallaxis is low, between 1 and 2%, in all worker size classes (Carlin, 1981). Leptothorax curvispinosis (5- 10%) and L. du/oticus (4-6%) (Wilson and Fagen, 1974; Wilson, 1975), have relative frequencies similar to P. scabriusculus. Self grooming
A notable feature of self-grooming in P. scabriusculus, compared to that of other cephalotines studied, is that abdominal self- grooming movements are performed. In workers, about 4% of all self-grooming acts involved abdominal grooming with the fore- or hind legs. The abdomen was tucked under somewhat to facilitate complete coverage. In addition, in about 1% of self-grooming acts, the abdomen was bent forward between the legs and the tip licked. Self-grooming of the abdomen has never been observed in either C. atratus or Z. varians (Wilson, 1976; Cole, 1980; Corn, 1980). The



================================================================================

178 Psyche [vo~. 91
fact that P. scahriusculus was able to perform this maneuver dem- onstrates that the loss of abdominal grooming in other cephalotines was not related to the inflexibility conferred by heavy armor. Of greater significance, the ability to autogroom the abdomen, espe- cially the tip, casts doubt on a suggestion made by Wilson (1976) and echoed by Cole (1980) that the acquisition of abdominal tro- phallaxis by cephalotines was tied to loss of maneuverability. Fate of infrahuccal pellets
P. scahriusculus workers regurgitated infrabuccal pellets and the action frequently attracted the interest of a nestmate. However, ants never ate the pellets or offered them to larvae, as has been observed in Z. varians (Wilson, 1976; Cole, 1980). As soon as a pellet was regurgitated, a worker would leave the brood area and drop the pellet onto the floor of the petri dish. Regurgitation of infrabuccal pellets was never observed in C. atratus (Corn, 1976). Excavation
Usually several workers were at the rear of the nest tube digging at the damp cotton with their legs and mandibles. Presumably this behavior would be homologous to excavating the blind end of a tunnel in a twig nest.
Antenna1 tipping
A stretching behavior dubbed antenna1 tipping by Wilson and Fagen (1974) was frequently observed. This behavior has been noted in many ant species, including Leptothorax cwvispinosis, L. duloti- cus (Wilson, 1975), Formica perpilosa (Brandao, 1978), Colobopsis sp. (Cole, 1980), C. atratus (Corn, 1980) and Z. varians (Wilson, 1976; Cole, 1980). In P. scabriusculus, the first pair of legs were extended forward and the rear 2 pairs extended backwards. The body was elevated due to the leg extension and the abdomen drooped slightly. The position of the head was more variable. Some- times it was raised and sometimes it was tucked under the body. The impression was one of rigidity, and the body sometimes trembled slightly or the antennae vibrated.
Stridulation
Both workers and queens stridulated when physically trapped or restrained. This behavior does not appear in the behavioral reper-



================================================================================

toire (Table 1) since it was produced only when ants were held and not under the standard conditions for observation. When an ant was provoked into stridulating, nearby nestmates did not obviously alter their behavior. The stridulatory file is located on the neck of the gaster where it inserts into the post-petiole. The presence and use of a stridulatory organ in Procryptoce/-us is remarkable as it is found in no other genus of cephalotines. The absence of a stridulatory organ in the Myrmicinae is unusual; Markl 1973). in a survey of stridulatory structures in ants, found that 83% of myrmicine genera had them. So, it is intriguing first. that most cephalotines have lost the file and second, that Procr,~-ptocerus has retained the structure. Markl (1973) found the stridulatory organ in all 7 species of Procryptocerus he examined. Four subfamilies of ants have stridulatory organs: the Notho- myrmeciinae, the Pseudomyrmicinae. the Ponerinae and the Myr- micinae (Sharp. 1893: Haskins and Enzmann, 1938: Markl. 1973; Taylor, 1978). The stidulatory organ is always found on the same pair of segments: the file is located on abdominal segment IV and the scraper on segment 111. In view of the apparent evolutionary stability of the stridulatory organ's position. its presence in Procryp- tocerus can be regarded as a reliable primitive character. The ability to stridulate is common in ants, but the role of stridu- lation in communication has been demonstrated in only two cases. Markl (1965) showed that stridulation serves as a distress signal in A ttu cephalotes. Buried workers stridulate and nest mates respond by digging in the vicinity of the sound. Markl and Holldobler (1978) have shown that in Novoniessor, stridulatory signals function as a mechanism for modulating responses to other stimuli. For example, food retrieving behavior was enhanced when chemical recruitment stimuli were received concurrently with stridulator~r signals. Nova- messor stridulates spontaneously, without the provocation of physi- cal restraint.
Neither of these proven roles of stridulation applies directly to P. s~~uhr/'u.scul~~~. Digging is not an appropriate rescue response in an arboreal nest. and the fact that P. .scabriuscul~~s does not stridulate spontaneously, without restraint. argues against an analogy with No\~~t~e.s.sor. A third possibility is that stridulatory vibrations deter predators. This phenomenon has been documented in insects other than ants (see Masters, 1979).




================================================================================

Psyche
[Vol. 91
Defense
P. .s(~ut71+iusculuf, relies almost exclusively on its thick exoskeleton, with cephalic scrobes to shield the antennae, to discourage enemies and predators. In response to real or supposed threats (other ants, freshly killed flies, seeds, flowers, pollen, etc.), workers lowered their heads, contacted the object, and pushed. The workers also nipped as best they could with their small, blunt mandibles. P. .scahriusculu^ was ineffective in coping with enemy ants in the open. One colony in a petri dish took 12 hours to clip the legs off a P.sem/o177.1~nw.~ sp. worker placed in the nest. Presumably bulldoz- ing would be more effective inside a twig nest in preventing tres- passers from entering and nipping would be more effective where the enemy could be pinned against the walls of the narrow passageways.
Leg movements
Another behavior not included in the repertoire is miscellaneous leg movement. When ants were inactive, standing quietly in posi- tion, often 1, 2, or, rarely, 3 of their legs might be moving. Most of the movement was made by the tibia and tarsus, which were swung as a unit, while the femur stayed in place. Often, the femur was flexed and also participated in the movement. About 60% of the time the movement involved one of the rear legs, 30% a middle leg, and 10% a front leg. The behavior was observed in queens as well as workers.
QUEENS
Number of' queens
P. .scabriu.sculu.s has multiple queens. The colony observed in this study contained, at the time of collection, 6 dealate queens and 62 workers (8.8% queens). After the study was terminated, the colony was preserved in alcohol. Subsequent dissection showed that all 6 queens had fully developed ovaries. In addition, 3 queens (#I, #4, and #6) contained at least one egg large enough to fall in the size range of viable eggs. Two fragments of other colonies contained 4 queens with 40 workers (9.1 %) and 1 queen with 17 workers (5.5%). A large colony collected in November, 1982, contained 72 workers with 27 queens (27%). In this colony, many of the queens had unex- panded, crumpled wings indicating that they had been produced within the colony and were not primary, founding queens.



================================================================================

19841 Wheeler - Behavior uf Procrvptocerus 18 I In ants, polygyny evolves under special ecological conditions, such as short-lived nest sites (Holldobler and Wilson, 1977). There- fore, it is not a reliable indicator of major phylogenetic trends within a group. Apparent polygyny (the presence of multiple dealate queens) is scattered throughout the advanced genus Zacrvptocerus. In Z. texanus, Creighton and Gregg (1954) (see also Creighton, 1963; Creighton, 1967) found colonies and colony fragments con- taining 0- 14.7% queens. In Z. christopherseni, I found 13 dealate queens in a single colony containing over 4,000 workers and sol- diers. In contrast, 7. rowheri (Creighton and Nutting, 1965), Z. pu.sillus (Limongi, 1977), Z. varians (Wilson, 1976), Z. minutus (personal observation), as well as Cephalotes atratus (Corn, 1980) and Eucrvptocerus placidus (Corn, 1976) are apparently mono- gynous.
Behavior of queens
Queens performed a total of 298 acts in 9 categories over a period of 20 hours (Table 1). When data were fitted to a lognormal Poisson distribution (Fagen and Goldman, 1977), the true repertoire size of queens in a laboratory nest was estimated to be 11, with a 95% confidence interval of 23, types of acts. The entire repertoire of queens, with the exception of self- grooming, was devoted to eating. Queens solicited and received food not only from workers but also from larvae. Queens used antenna1 soliciting movements and licked larvae vigorously around the mouth to demand food. This behavior is similar to that described for queens of Leptothorax curvispinosus, which solicit labial gland secretions from larvae (Wilson, 1974).
Most of the queens' infrequent behaviors, shown in Table 1, were probably associated with behavioral sequences leading up to demanding food from workers or larvae. For example, grooming of workers preceded solicitation movements with the antennae. Man- ipulation of larvae, moving them into a better position, was a pre- lude to solicitation behavior.
P. sc'abriusculus queens, which performed acts in 9 behavioral categories, were more versatile than queens of Z. varians. In 2. varians, queens performed only 3 acts: self-grooming, regurgitating with minor workers, and laying eggs (Wilson, 1976; Cole, 1980). Outside the Cephalotini, 5 repertoires of queens are available. Repertoire size ranges from 5 in Colobopsis sp. (Cole, 1980) and



================================================================================

182 Psyche [vo~. 91
Lej3tothom.i- cur\~i.sj~inosus (Wilson and Fagen, 1974) to 8 in Orec- tognuthus versicolor (Carlin, 1981), 9 in the slavemaking species, Leplofhorax ^uSoticus (Wilson and Fagen, 1974), and 16 in the primitive ponerine, Atublyopone pa1lipe.s (Traniello, 1982). In respect to other ant species, then, the repertoire size of P. scabrius- culus queens appears to be average. In comparison to the queen of 2. vurians, however, the queen of P. sc+abr/'u.scu/u.s is much less behaviorally specialized.
Variation in behu\tior of' inc/i\iic/ual queens To determine if there were differences in the behavior of individ- ual queens that might reflect reproductive dominance, queens were