Diana E. Wheeler.
Behavior of the ant, Procryptocerus scabriusculus (Hymenoptera: Formicidae), with comparisons to other cephalotines.
Psyche 91(3-4):171-192, 1984.

This article at Hindawi Publishing: https://doi.org/10.1155/1984/65369
CEC's scan of this article: http://psyche.entclub.org/pdf/91/91-171.pdf, 1748K
This landing page: http://psyche.entclub.org/91/91-171.html

The following unprocessed text is extracted automatically 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 marked with colored paint and the acts of each recorded for 15.5 hours of the study. The most common acts in which queens partici- pated were soliciting liquid food from workers, soliciting liquid food from larvae, self-grooming movements, and being groomed by a worker (Table 2). For comparison, the average number of similar acts recorded for workers during the same 15.5 hour period is also shown in Table 2.
The 6 queens showed considerable variation in their rates of solic- iting liquid food. A chi-square test showed that pattern of queen behavior was significantly different from an even distribution for both soliciting food from workers (p<0.025) and soliciting food from larvae (p<0.005). The amount of food that queens were able to collect from workers and larvae could be directly associated with rank, the amount being an indication of resources convertible to Table 2.
Behavior of individual queens. Values given are actual numbers of acts in a category that were performed by each indiv,idual in 15.5 hours of observation. The average queen values are means of acts performed by the six queens. The value for average worker is the number of acts in a category performed by workers in 15.5 hours of observation divided by the number of workers (n=62). Queens solicited from larva by antcnnating and licking larvae around the mouth. Workers licked larvae as part of brood care and did not concentrate in the head region. Values of p for differences among queens were determined using a chi-squared test, a\. av.
Queen # 1 2 3 4 5 6 queen worker p
Solicit from worker 13 16
5 23 9
11
13 7 <.025
Solicit from 'lick larva 7
12
7 25
13 10
12 4 <.005
Self-groom 12 10
12 4 8
2
8 25 <.005
Groomedbyworker
26 39 40
35
43
31 36 15
ns




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

viable eggs. In soliciting, queen #4 clearly led all the rest, while queen #3 was the clear loser. The least demanding queens partici- pated in food exchange with workers at a rate similar to workers: such queens can be regarded as worker-like in their behavior (Table 2).
Occasionally. queens solicited from other queens (n=9). One queen would initiate the contact, but both would perform soliciting movements with their antennae. No food appeared to be exchanged during these bouts. The number of queen--queen contacts was not directly correlated with rank as determined by rates of queen- worker and queen-larvae exchanges. The sample size is so low, however, that it is premature to dismiss the possibility that rank is determined or maintained by such interactions. The relationship between grooming patterns and rank, if one exists, is not clear (Table 2). There were significant differences among queens in the amount of self-grooming indulged in (p<0.005, chi-squared test), but the difference in attention received from workers was not significant. Queens groomed themselves less than the average worker and were groomed by workers more often than workers groomed each other. No queen could be classed as worker- like in grooming behavior.
Viable and trophic eggs
Both normal, viable eggs and trophic eggs are found in P. scubri- usculus colonies. Viable eggs in P. sc~ub~~iusculu.~, those capable of embryogenesis, were large and cylindrical, measuring 1.32- 1.66 mm long. The shape is typical of Cephalotini. as well as other arboreal ants (Wheeler and Wheeler, 1954). Smaller, presumably trophic, eggs were highly variable in size (0.6- 1.2 mm). Trophic eggs were less cylindrical than viable eggs and had a milky, homogeneous appearance. Generally, ants consume trophic eggs immediately after they are laid (Wilson, 1971). Why P. scahriusculus should allow non-viable eggs to lie around is a puzzle. The relative capabilites of egg laying in workers and in queens is not known, since no egg laying was observed. In other cephalotines, workers are known to lay trophic eggs as well as viable, unfertilized eggs that develop as males. In Z. va~*k~n.~, minor workers lay trophic eggs (Wilson, 1976), and production of males by queenless colonies has been noted in C. utratus (Weber, 1957). 2. \wI-/'~/~.Y (Wilson, 1976) and Z. tnit7utux (personal observation).



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

184 Psyche [vo~. 91
Can a comparison of behaviors within the Cephalotini contribute to an understanding of the phylogeny within the tribe or of the evolution of morphological worker castes'? Including the behavioral data reported here, information is available for the three major genera of cephalotines: Procr\'ptocerus, Cephalotes, and Zacrvp- torei-LLS. It is now possible to compare and integrate behavioral with morphological data in considering phylogenetic relationships among cephalotines.
Only behavioral characters that do not occur in all members of a group can be useful in constructing alternative paths of evolution. Six such characters known for three species of cephalotines are listed in Table 3. First. I will use these characters to illustrate overall behavioral similarities between species. Then, the polarity (ancestral vs. derived state) of these characters will be surmised and used to construct behavioral cladograms (Fig. 2). Finally, the evolutionary relationships suggested by the cladogram can be used to re-examine our assumptions about the evolution within the cephalotines and their diverse morphological worker castes. P. .scahriu.s~~ulus has been characterized as morphologically diver- gent (Kempf, 195 1 ), quite discrepant (Kempf, 1973), and primitive (Corn, 1976; Wilson, 1976). In its behavior, however, it shares a remarkable number of traits with the advanced species, Z. varians (Table 3). Table 3 indicates that P. scabriusculus and 2. wriuns share four of the six discrete behavioral characters listed, two of Table 3.
Con~parison of behavioral characters among three cephalotine species, representing the three ma-lor genera. The six behaviors that are listed may have phylo- genetic significance. An asterisk (*) indicates which behavioral state is considered derived. Note that Pt~oi~rvpm,i~t.~.'i ~.-uht~~iifici~l~i.s and Zu('r\'ploceru.\ vuriut~s share our characters, v,'hile Z. \,uriaii.\ and Cfiulo/i"i utrutus share two. P. .\i'abrii/.s-cu/us and C'. aiming share none of the six behavioral states. Abbreviations given are used in Figure 2.
Cep/iti/oie.\ Za<.r\'pl oi,eru\ Procrvpioreru.\ Abdominal trophallaxis (at) no (yes* yes*) Adult transport (car)
yes (no* no*)
Infrabuccal pellets
no* (yes yes)
1-3) trophic eggs
no* (yes yes)
Stridulate (str)
(no* no*) yes
Abdominal self-groom (ag) (no* no*) yes




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

19841 Wheeler - Behavior of' Procr.~y)iocerus 185 which are primitive. 2. varians and C. atratus share only two char- acters, while P. s~~ahriusculus and C. atratus share none. P. scahri- usculus and C. atratus are both considered relatively primitive, but behaviorally they are primitive in different ways. On the basis of morphological characters, Brown (1973) felt that all cephalotine genera besides Procr.~piocerus could be lumped. Kernpf (1973) maintained the distinction betwen the genus Cepha- Iota and Zucrvptocerus. The behavioral data show that C. atratus is divergent from both P. scahriusculu.~ and 2. varians and therefore support the generic distinctions proposed by Kempf (1973). The probable polarity (ancestral vs. derived state) of each of the characters in Table 3 can be assessed by outgroup comparisons with other ants. The closest relatives of the Cephalotini are, unfortu- Fig. 2. Cladograms for 4 synapomorphic characters in 3 species of cephalotines: Proct-vploceru'i ficubriusculu.~, Cepuhlolefi uirulu.s, and Zui~rvploi'erus variant. The ancestral cephalotine is assumed to have had the following profile: -at (abdominal trophallaxis). +ag (abdominal grooming), +str (stridulation), +car (adult transport =carrying nestmate).




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

186 Psyche [vo~. 91
nately, not known. Therefore, cephalotines are compared with other myrmicines, when that information is available, as well as with other subfamilies. Two important behaviors, abdominal trophal- laxis and stridulation (see Table 3), were discussed in detail above. Adult transport, in which one adult carries another, occurs widely in ants, and is especially well developed and stereotyped in the Myrmi- cinae and the Formicinae (Wilson, 197 1; Moglich and Holldobler, 1974). Therefore, the expression of this behavior is considered the primitive condition in the Myrmicinae and its loss the derived state. Behavioral Claciograms
Cladograms provide a useful device for examining possible ways different sets of characters could have evolved. 1 will assume that the three species, P. scabriusculus, C. arrarus, and Z. varians, are monophyletic, sensu Hennig (1966); no species is an ancestor of either of the others. 1 also assume that the three species involved are representative of their genera. Recognizing that this second assump- tion may be premature, I stress that more species need to be studied, especially in the diverse genus Zacrvptocerus. The most useful characters in constructing cladograms are those that are synapomorphic, derived traits that are shared. There are three ways that three species could have evolved such that two now share an advanced trait. The simplest is that the two species share a common ancestor that possessed the character. The second and third ways require two steps. First, the two species could have evolved the trait independently. Secondly, all three species could have acquired the trait from a common ancestor, and one species subsequently lost it.
There are four synapomorphic characters in Table 3. Abdominal trophallaxis and absence of adult transport are shared by Z. varians and P. .scahnu.sculus while absence of stridulation and of abdominal self-grooming are shared by Z. varians and C. arratus. Of the three possible cladograms using these four traits (Figure 2), two appear equally plausible. In both cladogram A and B, two of the four synapomorphies require two steps to generate the appropriate dis- tribution of characters. Two steps means independent derivation of the characters, or common derivation and secondary loss. The third cladogram, C, can be rejected as unlikely by parsimony since all four synapomorphies require two steps to produce the appropriate pattern.




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

When the relative importance of characters is considered, clado- gram A gains plausibility over B. The ability to stridulate has rarely been lost in the Myrmicinae (Markl, 1973). Therefore, a single loss (cladogram A) can be considered more likely than a double one (cladogram B). Similarly, abdominal grooming movements occur in almost all ants (Wilson, 1962; Parish, 1972); loss is probably a rare evolutionary event. The appropriate pattern of abdominal groom- ing is derived most parsimoniously in cladogram A. Adult transport (carrying) on the other hand is a character expressed to widely varying degrees among the ants. Nestmate carrying, used primarily during emigration to new nest sites, may be relatively easy to lose if. it becomes unnecessary ecologically. The adult transport character then does not lend strong support to either cladogram. Finally, the appropriate pattern for abdominal trophallaxis is derived most par- simoniously in cladogram B. In cladogram A, Cephalotes loses this character secondarily. Since intraspecific abdominal trophallaxis rarely occurs in ants, and is poorly understood, the difficulty or ease of its subsequent loss cannot be evaluated. In summary, on the basis of a character by character evaluation, cladogram A is more plausible.
/t~~p//"c*utionsfbr the Evolution of' Worker Polymo17>/7ist?7 Monomorphism is the ancestral state of the worker caste in most ants and probably represents the ancestral state of the Cephalotini as well. In myrmicines, a few cases of secondary monomorphism are known in species with workers that are minute in comparison to the queen (Wilson, 1953, 1971 ). If worker monomorphism is accepted as the ancestral state in the Cephalotini, then cladogram A provides the most parsimonious derivation of the pattern of worker poly- morphism. Cladogram B implies that the morphological worker caste systems characteristic of Zac/-.~y->tocerus and Cephalotes evolved independently. According to cladogram A, the tendency to express morphological diversity within the worker caste evolved once. Cephalotes maintained a weak bimodality in the size fre- quency distribution over a wide size range (Corn, 1980), while the Zacr.~y->/oce~u~ line intensified that bimodality, a trend which led to the completely dimorphic worker caste of some species, If worker monomorphism is ancestral and Procrvptoce~x.~ repre- sents a relict state, it follows that, in the Cephalotini, soldiers must



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

188 Psyche [vol. 91
be the primitive caste and minor workers the novel caste. In Pro- cryptocer;/.s, workers closely resemble the queen as do soldiers in Zacr,~y?toceru.s and large workers in Cephalotes. Advanced cepalo- tines appear to have added smaller workers to their worker caste systems. Soldiers of Zacr.17>toceru.s fulfill the first of two criteria proposed in Wilson (1980) for a primitive caste: they resemble the workers of the less modified, monomorphic members of the same tribe (e.g. Proi'r.~plucer~~s). Zuc~-.ly>tocerus soldiers do not meet the second criterion. that the primitive caste perform the generalized services of a colony. Wilson (in press) has discovered that Pheidole soldiers can be induced to express behavior typical of a minor worker's repertoire; morphological specialization does not preclude behavioral flexibility. This discovery uncouples morphological and behavioral specialization and may relax the need for a primitive caste meeting the second criterion of generalized behavior. Ecological similarity between species can contribute significantly to similarities in behavioral traits. Cole has demonstrated that two species of ecologically similar but phylogenetically distant species of ants. Z. varian.s (Myrmicinae) and Colohopis sp. (Formicinae) exhibit convergence of qualitative behavioral traits as well as of quantitative aspects of their repertoires. Both species inhabit hollow twigs of a variety of plants that represent dry habitats (Smith, 1923; Kenipf. 1958; Cole. 1982).
Z. \+ariam and P. .s~-ab~-iu.s~-ulu^ are also ecologically similar. Both nest in hollow. dry twigs. and the ants themselves are of similar size. In Z. variant, minor workers measure 3.6-4.7 mm and soldiers 5.9-6.3 mm in total length (Kempf, 1958). The size of P. scabriuscu- 1u.s workers falls between the two castes of Z. varians, with workers measuring 4.6-5.2 mm in total length. The colony size of both spe- cies is also small, not exceeding several hundred workers. In addi- tion, Z. variant is known to be nocturnal, and P. scabriusculus is believed to be nocturnal of crepuscular (Snelling, 1968). C. atratus, in contrast. is a large ant (8-14 mm total length), nesting in spacious cavities in living wood. Colony size is extremely large compared to other cephalotines. with about 12,000 workers in a mature colony. They forage diurnally. Corn (1976) suggests that many of the differences between C. atratus and Z. varians might be based on the differences in nest site. Use of infrabuccal pellets as



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

19841 Wheeler - Behavior of Procrvptocerus 189 food and high rates of regurgitation are adaptations to dry condi- tions (Wilson, 1976; Cole, 1980), and would not be necessary in C. atratus which nests in moist tree cavities (Corn, 1976). The relatively wide nest chambers of C. atratus may have provided an environ- ment in which the primitive behavior of carrying nestmates was possible, and ultimately, retained (Corn, 1976). The lack of both infrabuccal pellets and abdominal trophallaxis may be indicative of an entirely different diet in C. atratus than either P. scahriusculu.s or Z. varians.
In summary, some of the behavioral similarities between P. sca- briusculus and Z. varians, and the apparent divergence of C. atratus, may be based in ecology rather than phylogeny. Behavioral conver- gence of P. .s~~abriusculu.s and Z. varians would lend further support to cladogram A.
P. .scahriu.sculus is a cephalotine with multiple queens and a monomorphic worker caste. Differences in the behavior among individual queens suggest that queens are not equal in reproductive status. Newly emerged P. scahriusculus workers indulge in pro- longed periods of abdominal trophallaxis. Abdominal trophallaxis has been reported previously in Z. varians, an advanced cephalotine with a dimorphic worker caste. Cladograms based on behavioral characters support a phylogenetic scheme in which the divergence of Procrvptocerus occurred prior to the divergence of Cephalotes. Within the Cephalotini, the minor workers, rather than soldiers, appear to be the novel worker caste.
I would like to thank all the Eberhards for encouraging me to work in Costa Rica and for making this study not only possible but pure pleasure. L. Freed helped me locate, and provided transporta- tion to cephalotine habitats in Panama. I thank N. F. Carlin, D. S. Gladstein, and R. M. Fagen for guiding the analysis of the reper- toire and W. P. Maddison for enlightening discussions of cladistics. N. F. Carlin, B. Holldobler, W. P. Maddison, and E. 0. Wilson provided constructive comments on earlier versions of the manus- cript. Funds were provided by a Smithsonian Postdoctoral Fellow- ship and NSF Grant #PCM-8301763.




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

Psyche
[Vol. 91
BRANDA~, C. R. F.
1978.
Division of labor within the worker caste of Formica perpiloxu Wheeler (Hymenoptera: Formicidae). Psyche 85: 229-237. 1983.
Sequential ethograms along colony development of Odontot~iuvhus a//;- nix Guerin (Hymenoptera, Formicidae, Ponerinae). Insectes Soc. 30: 193-203.
BROWN, W. L.
1973.
A comparison of the Hylean and Congo-West African rain forest fauna. In Tropical Forest Ecosystems: a comparative review. B. J. Meggers, E. S. Ayensu and W. D. Duckworth, Eds. Smithsonian Institution Press, Washington, pp. 161 - 185.
BCLMER. M. G.
1974.
On fitting the Poisson lognormal distribution to species-abundance data. Biometrics 30: 101 - 1 10.
CARLIN. N. F.
1981.
Polymorphism and division of labor in the dacetine ant 0rci'tognuthu.s vers/'(~u/or (Hymenoptera: Formicidae). Psyche 88: 23 1-244. CLEVELAND. L. R.
Symbiosis among animals with special reference to termites and their intestinal flagellates. Q. Rev. Biol. 1: 5 1-60. Repertoire convergence in two mangrove ants, Zacrj*ptoreru.s varianx and Cut1ipot1otu.s (Colobopsis) sp. Insectes Soc. 27: 265-275. The guild of sawgrass-inhabiting ants in the Florida Keys. Psyche 89: 35 1-356.
The ecology and behavior of Cephalotes uiralux, a Neotropical ant (Hymenoptera: Formicidae). Ph.D. Dissertation. Harvard University. Polymorphism and polyethism in the Neotropical ant Cephulotesatratu.~ (L.). Insectes SOC. 27: 29-42.
CREIGHT~N. W. S.
1963.
Further studies on the habits of Crvptoceru,~ texunux Santschi (Hymen- optera: Formicidae). Psyche 70: 133- 143. 1967. Studies on free colonies of Cr,~*ptoceru.s texunu.~ Santschi (Hymenoptera: Formicidae). Psyche 74: 34-4 1.
CREIGHTON W. S. AND R. E. GREGG.
1954. Studies on the habits and distribution of Crvptocerus texanus Santschi (Hymenoptera: Formicidae). Psyche 61: 41 -57. CREIGHTON, W. S. AND W. L. NUTTING.
1965. The habits and distribution of Cr,vptocerus rowheri Wheeler. Psyche 72: 59-64.
EISNER, T. AND G. M. HAW.
1962. The infrabuccal pocket of a formicine ant: a social filtration device. Psyche 69: 107- 1 16.




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

Wheeler - Behavior 9 f Procr-1ptoceru.s
EMIIKY, C.
1888.
Uber den sogenannten Kaumagen einiger Ameisen. Z. wiss. Zool. 46: 378-4 12.
FAGI:N. R. M.
1978.
Repertoire analysis. In QuuniIrutive Ethology. P. W. Colgan, Ed. John Wiley and Sons, New York.
FAGI:~. R. M. AND R. N. GOLDMAN.
1977.
Behavioral catalogue analysis method. Anim. Behav. 25: 261 -274. FAKISII. D. .J.
1972.
The evolutionary implications of qualitative variation in the grooming behaviour of the Hymenoptera (Insecta). Anim. Behav. 20: 662--676. HASKINS. C. P. AND E. V. ENZ.MANN.
1938.
On the occurrence of certain sociological and physiological features in the Formicidae. Ann. N. Y. Acad. Sci. 37: 97- 162. HENMG. W.
1966.
Phylogenetic systematics. University of Illinois Press, Urbana, Illinois. H~~l.i.D0~1.l~~. B. AND E. 0. WII.SON.
1977.
The number of ant queens: An important trait in evolution. Naturwiss. 64: 8-15.
KIMPI. W.
1951.
A taxonomic study on the ant tribe Cephalotini. Rev. Entomol. 22: -244.
1958.
New studies of the ant tribe Cephalotini (Hym. Formicidae). Studia. Entomol. 1: 1176.
1972.
Catalogo abreviado das formigas das regiao Neotropical (Hymenoptera: Formicidae). Studia Ent. 15: 3-344.
1973.
A new Zucr.~.pioceru.'i from Braril, with remarks on the generic classifica- tion of the tribe Cephalotini (Hymenoptera: Formicidae). Studia Ent. 16: 449-462.
LIM~NGI, J.
1977.
Variacion de tamafios en la poblacion de Zacr\~ptoceru.spu.sIllu'i en 10s llanos vene7olanos. Smithsonian Tropical Research Institute. Exxon Student Reports.
MAKKI,. H.
1965.
Stridulation in leaf-cutting ants. Science 149: 1392-1393. 1973.
The evolution of stridulatory communication in ants. Proc. 7th Congr. IUSSI. London: 258-265.
MARKL, H. AND B. H~LLDOHI.ER.
1978. Recruitment and food-retrieving in Novomessor (Formicidae, Hymen- optera). I I. Vibration signals Behav. Ecol. Sociobiol. 4: 183-2 16. MASTERS. W. M.
1979.
Insect disturbance stridulation: its defensive role. Behav. Ecol. Socio- biol. 5: 187-200.
~~OGLIC'II. M. AND B. H~I.I.D~BI.ER.
1974. Social carrying behavior and division of labor in ants. Psyche 81: 2 19-236.




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

Psyche [Vol. 91
SHARP. D.
1893.
On stridulation in ants. Trans. Entomol. Soc. Lond. 1893, p. 199-213. SMITH. M. R.
1923. Two new Mississippi ants of the subgenus Colobopsis. Psyche 30: 82-88. ~NK~.I.ING. R.
1968. Taxonomic notes on some mexican cephalotine ants (Hymenoptera: Formicidae). 1. A. Co. Mus. Contrib. Sci. 132: 1-10. ST[-ART. R. J.
1981. Abdominal trophallaxis in the slave-making ant, Harpagoxenua anieri- wiu.s (Hymenoptera: Formicidae). Psyche 88: 33 1-333. T.AvI.~R. R. W.
1978.
Noihom~~rt?ie~~ia macrop: A living ant fossil. Science 201: 979-985. TRAMH.I.~. J. F. A.
1982. Population structure and social organization in primitive ant Arnhlyo- pone pul/ipe'i (Hymenoptera: Formicidae). Psyche 89: 65-80. WI:HI-.R. N. A.
1957. The nest of an anomalous colony of the arboreal ant Cephalotes airam. Psyche 64: 60-69.
Wll1:l:l.l:~. G. C. AND J. WIII~I-.I,~~R. The ant larvae of the myrmicine tribes Cataulacini and Cephalotini. J. Wash. Acad. Sci. 44: 149- 157.
0.
The origin and evolution of polymorphism in ants. Q. Rev. Biol. 28: 136 156.
Behavior of Ducdon arniigerum (Latreille), with a classification of self- grooming movements in ants. Bull. Mus. Comp. Zool. (Harvard) 127: 40 1 -422.
The Inseci Socieiies. Belknap Press of Harvard University Press, Carn- bridge. Mass.
Aversive behavior and competition within colonies of the ant Lepio- thorax curvispinosu.~. Ann. Entomol. Soc. Am. 67: 777-780. L~iothorax duloiit~ux and the beginnings of slavery in ants. Evolution 29: 108- 1 19.
A social ethogram of the Neotropical arboreal ant Zacrypiocerus varians (Fr. Smith). Anim. Behav. 24: 354-363.
Caste and division of labor in leaf-cutter ants (Hymenoptera: Formici- dae: Aiia). 1. The overall pattern in A. 'iexden.~. Behav. Ecol. Sociobiol. 7: 143- 156.
The relation between caste ratios and division of labor in the ant genus Ph~idol~ (Hymenoptera: Formicidae. Behav. Ecol. Sociobiol. (in press). 0. AND R. M. FAGEN
On the estimation of total repertoire size in ants. N. Y. Entomol. Soc. 82:



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