evolution of polygynous obligate acacia-ants in western ......occupy swollen-thorn acacias that grow...

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EVOLUTION OF POLYGYNOUS OBLIGATE ACACIA-ANTS IN WESTERN MEXICO

BY DANIEL H. JANZEN*

Department of Biology, University of Chiicago, Chicago, Illinois, U.S.A.

INTRODUCTION

Central American obligate acacia-ants (Pseudomyrmex spp.) have either monogynous (single-queen) or polygynous (multiple-queen) colonies, depending on the species of ant. This study compares the two colony structures and discusses some of the ways in which such a difference influences the mutualistic interaction between ants and acacias. I also examine some of the selective pressures for the evolution of polygynous colonies from monogynous ones. Polygyny has not been previously recorded for obligate acacia-ants (but the Pseudomyrmex in Tachigalia is polygynous (Wheeler 1921)) and, as an ecological phenomenon, has received almost no attention. Ant and acacia obligatory mutualism has been discussed by Janzen (1966, 1967a, b, 1969, 1973), Hocking (1970) and Monod & Schmitt (1968), and is not the primary focus of this study.

Monogynous obligate acacia-ants

Over most of the geographic range of Central American swollen-thorn acacias (Acacia cornigera L., A. spaerocephala Schlecht & Cham., A. mayana Lundell, A. hindsii Benth., A. collinsii Safford, A. globulifera Safford, A. chiapensis Safford, A. allenii Janzen, A. melanoceras Beurling, and A. cookii Safford (Janzen 1973) the occupant ant colonies (Pseudomyrmex ferruginea F. Smith, P. belti Emery, and P. nigrocincta Emery plus at least three undescribed species) each has only one egg-laying queen and no auxiliary queens (Janzen 1966; 1967a, b, 1969; Beulig & Janzen 1969; and unpublished field notes). As P. ferruginea is the best-studied monogynous obligate acacia-ant (Janzen 1967a) I will use it as the representative monogynous species in the following discussions, but will note where its biology dramatically deviates from that of other monogynous species.

Colony foundation by monogynous obligate acacia-ants takes the following route. One or more newly fertilized queens find the young acacia. After numerous intra- and inter-specific aggressive encounters with other queens, some succeed in establishing exclusive ownership of a single swollen thorn. As each small colony grows, it gradually increases the number of thorns in its exclusive possession. Exclusive ownership and effective patrolling of the entire young acacia by the workers from one queen is first achieved when one of the colonies has 100-300 workers; a queen of P. ferruginea requires 9-12 months to produce a colony of this size (Janzen 1967a). Her workers kill the other workers and queens, and kill or drive away any new queens that attempt to establish a colony in the acacia at a later date. The colony may eventually expand to occupy as many as twenty swollen-thorn acacias but the usual number is one to five. Incorporation of new acacias into the colony occasionally involves intra- or inter-specific fights that

* Present address: Department of Zoology, The University of Michigan, Ann Arbor, Michigan 48104, U.S.A,

728 Evolution of acacia-ants in W. Mexico

annihilate the previous occupant of the acacia. No matter how large the colony, it does not accept additional queens. There is no queen supercedure, and if the queen dies, the colony dies.

Polygynous obligate acacia-ants Polygynous obligate acacia-ants are found in two restricted and ecologically very

different parts of the range of swollen-thorn acacias. Pseudomyrmex satanica Wheeler (Wheeler 1942) is polygynous and occupies Acacia melanoceras in the heavily shaded understorey of Panamanian and Canal Zone rain forests; the detailed biology of this interaction will be described in a later paper. Pseudomyrmex venefica Wheeler (Wheeler 1942) and at least five other undescribed species of polygynous obligate acacia-ants occupy swollen-thorn acacias that grow in regions with a very severe dry season but a substantial rainy season (1 0-1-5 m of rainfall during the rainy season). The vegetation of such sites is often called 'thorn forest'. For example, polygynous colonies are found in Acacia hindsii and A. collinsii at the northern end of their distribution on the west coast of Mexico, A. collinsii and A. cornigera on the Yucatan Peninsula, and A. collinsii in some of the small inland valleys in Guatemala and Honduras (cf. Janzen (1973) for details of the acacias' distributions). As I have worked most with Pseudomyrmex venefica, one of the two polygynous species in western Mexico, I will use it as the representative polygynous species in the following discussions, but will comment where its biology is known to deviate from that of other polygynous species from dry sites.

Briefly, colony foundation takes the following route. One or more newly fertilized queens find the young acacia. After numerous intra- and inter-specific aggressive encounters with other queens, some succeed in establishing exclusive ownership of a single swollen thorn. As the small colonies grow, their workers collectively patrol the surface of the acacia. While these workers are only mildly antagonistic to newly fertilized queens that find the acacia, they do not permit these queens to move into thorns already containing queens or brood. No one colony takes over the acacia at this time. A worker force of 100-300 P. venefica workers may therefore be produced in only 4-6 months. As the acacia grows, one of the queens eventually becomes its sole owner through the process of establishing daughter queens in progressively more of the new thorns than do the other queens. To do this, the colony accepts some of its daughter queens immediately after they have mated. An old colony may occupy many hundreds of swollen-thorn acacias and have tens of thousands of egg-laying queens; the loss of a physogastric queen is probably of little consequence to the colony. There is no fighting between merging colonies of the same species.

I assume throughout this study that polygynous species of obligate acacia-ants evolved from monogynous species of obligate acacia-ants. This assumption is supported by two observations. First, the many species of Pseudomyrmex that live in hollow twigs in tree crowns (and are not involved in a tight mutualism with a plant) appear to be almost exclusively monogynous. This statement is based on many years of collecting these species for taxonomic purposes. Monogynous obligate acacia-ants are most likely derived from these monogynous Pseudomyrmex (Janzen 1966). There is no reason to postulate that polygynous obligate acacia-ants had their origin in some now-extinct group of polygynous twig-inhabiting Pseudomyrmex. Second, for each polygynous species of obligate acacia-ant there is a morphologically similar monogynous species whose range abuts on the range of the polygynous species. In each of these cases the polygynous species occupies a habitat with a weather regime much drier than that normally

DANIEL H. JANZEN 729

occupied by the ant and acacia interaction, a habitat that is not occupied by the interaction except where there are polygynous species.

METHODS AND STUDY SITES

Data are gathered by dissecting large numbers of ant colonies in acacias of various ages and habitats. In small acacias, the colony is killed by putting the entire plant into a large cyanide bottle; large colonies are examined by aspirating worker ants from the main trunk until most of the colony has been collected, stripping the swollen thorns off the branches and putting them into large cyanide jars, and later dissecting each thorn. When there are large quantities of mixed brood and workers, they may be separated by air drying for several hours, stirring into water, and scooping off the floating workers. The pure samples can then be easily drained and oven-dried. A small acacia with 100- 300 thorns may be censused by two persons in about 2 h; a large tree with 5000 thorns may require five people working 3 days. When examining colony structure, great care was taken to ensure that 'colonies' were not just fragments of some much larger nearby colony; acacias occupied by the same colony may be as far as 3 m apart.

Special terms used in this study are defined as follows. A 'searching queen' is one that is newly fertilized and moving through the habitat in search of unoccupied swollen-thorn acacias. A 'founding queen' has entered a thorn and begun rearing a brood. The physogastric 'colony queens' are the egg-laying queens in the colony; they often have distended gasters (Plate la, b). A 'seedling acacia' usually has two to thirty swollen thorns and is 5-50 cm tall; it may be as much as 3 years old if the development of a protective ant colony has been delayed. For the purpose of this study, sucker sprouts from roots and old stumps are also termed seedling acacias.

Most of the generalizations on polygynous obligate acacia-ants in this paper are supported by field notes for an unpublished study of Pseudomyrmex venefica in the Pacific coastal lowlands between Mazatlan, State of Sinaloa to the Rio Balsas, State of Michoa- can, Mexico (September 1962 and 1963, June 1967, June-August 1968). Data were gathered on other polygynous species between 1962 and 1971 during the field work for a taxonomic study of Central American swollen-thorn acacias (Janzen 1973).

P. ferruginea is the most widely distributed neotropical obligate acacia-ant. It ranges from the intersections of the Tropic of Cancer and the gulf coastal lowlands of eastern Mexico to the Pacific coast of Panama and Colombia. P. i*enefica, as with other polygynous species, has a very restricted distribution. It ranges from where the Rio Presidio crosses the Tropic of Cancer in the foothills north-east of Mazatlan, State of Siinaloa, south along the Pacific coastal plain and foothills to the Rio Balsas, State of Michoacan (about 450 miles). Over this range it occupies the northern tip of the ranges of both Acacia collinsii and A. hindsii (Janzen 1973). The two acacias occupied by Pseudomyrmex venefica seem to disappear from the habitat at their northern limit for the same reason that Acacia cornigera is absent from the eastern side of Mexico; the dry season becomes so severe that the acacia drops its leaves, leading to death of the ant colony (Janzen 1967a). A. hindsii disappears at the Mazatlan site mentioned previously; it is a prominent member of disturbed vegetation derived from the 'bosque tropical subdeciduo' described for this part of Mexico by Rzedowski & McVaugh (1966). The northernmost site for A. collinsii is slightly south of Uruapan, Michoacan (Gabriel Zamora site, see below). Pseudomyrmex venefica is sympatric (except in the drier parts of its range) with a slightly larger and red- dish undescribed species of polygynous obligate acacia-ant. P. venefica disappears


somewhere between Rio Balsas, and the town of Petatlan (State of Guerrero), which is about 80 miles south of Rio Balsas. To the north, the undescribed species disappears somewhere between the Gabriel Zamora site and Colima. In the Petatlan region and farther south, P. belti and P. ferruginea are common occupants of Acacia collinsii, A. hindsii, and A. cornigera. Pseudomyrmex belti is the monogynous species from which P. venefica appears to be derived; P. belti ranges south to Guanacaste Province, Costa Rica. The above-mentioned undescribed species appears to be derived from P. ferruginea. Throughout their ranges, Acacia hindsii and A. collinsii are each occupied by at least eight species of obligate acacia-ants.

There are two important study sites. (1) Gabriel Zamora. This site is on south-east-facing slopes (foothills of the Sierra

Madre del Sur) and along adjacent watercourses about 1 mile toward Uruapan from the town of Gabriel Zamora along the north side of Highway 37, Michoacan, Mexico. At 820 m elevation, this site has vegetation often called 'thorn-forest' and derived from frequent burning, grazing, and shifting cultivation of deciduous forest that was originally 10-20 m in height (the 'Tropical Semideciduous Forest' and 'Arid Tropical Scrub Forest' of Duellman (1965)). The permanent creek running through the study site is the major water supply for the town of Gabriel Zamora. A. collinsii is the only swollen-thorn acacia in the region and this site is the most northern record for the species (Janzen 1973). In the nearby swamps of the coastal lowlands, A. hindsii is the only swollen-thorn acacia. Here and at Gabriel Zamora, Pseudomyrmex venefica is the only obligate acacia-ant. A few miles to the south, in the Rio Balsas basin, there are no swollen-thorn acacias; here the general vegetation is desert-like and the valley receives only about 800 mm of rain (Duellman 1965). Somewhere to the north of Gabriel Zamora but south of Colima, the undescribed brown polygynous obligate acacia-ant has its southern distribution limit. The Gabriel Zamora site may be viewed as the southern end of the range of P. venefica, whose distribution is terminated by increasing dryness.

(2) Rio Palillo. This site is on the river banks of the Rio Palillo where it crosses High- way 46, about 15 miles east of San Blas, Nayarit. The vegetation varies from naturally disturbed riparian (and originally semi-evergreen) to brushy pastures, fields and 2- to 20-year-old fallow regeneration on gentle to steep slopes (the original hillside vegetation would have been low deciduous forest). Acacia hindsii is the only swollen-thorn acacia in this coastal plain site (30 m elevation) and it is occupied about equally by Pseudomyr- mex venefica and the undescribed brown polygynous obligate acacia-ant. Ecologically, the site is central to the distribution of both species. In wetter sites (along large rivers and in coastal swamps of Nayarit) the undescribed brown species often occupies most of the Acacia hindsii. In drier sites, such as in the foothills above Mazatlan, Pseudomyrmex venefica becomes the most common species; at the driest sites it is the only species (as at Gabriel Zamora).

CONTRAST OF MONOGYNOUS AND POLYGYNOUS COLONIES

Monogynous and polygynous obligate acacia-ants differ in many traits that are of importance in understanding the evolution of polygyny by obligate acacia-ants. These are listed in Table 1 and discussed in detail in the following sections.

1. Location and composition of mating swarms

When monogynous obligate acacia-ants' mating flights have been observed (Pseudo-

Journal of Animal Ecology Daniel H. Janzen, Plate I

_. * l |~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~.. . .

'NP

a

Polygynous acacia-ants from Rio Palillo, 4 July 1968. (a) Two physogastric queens from the same thorn, and cone-shaped plug of eggs from the end of the thorn without an entrance hole (the undescribed polygynous species of Pseudomyrmex). (b) A physogastric queen being helped through a thorn entrance by workers-the terminal two-thirds of the gaster are visible and the two sclerites are sternites (P. venefica). (c) A worker of P. venefica (dark, on left) stinging a worker of the undescribed species of polygynous acacia-ant, and being stung in return, during an inter-specific colony fight. (Photographs by D. H. Janzen.)

(Facing p. 730)


Table 1. Contrast of behaviour and ecology of a monogynous obligate acacia-ant (Pseudo- myrmex ferruginea) with a polygynous obligate acacia-ant (P. venefica) (these traits may be taken as representative of most monogynous and polygynous dry land species of arid habitats unless otherwise indicated in the text; those traits directly involving the acacia are

marked with an asterisk; see text for detailed discussion of this table)

P. ferruginea (monogynous) P. venefica (polygynous) (1) Mating occurs in a swarm far from the parent Mating occurs on acacia of the parent ant

acacia with the parent ant colony colony; males come from other colonies (2) All newly mated queens search for unoccu- Newly mated queens re-enter the thorn that

pied acacias produced them, or leave the acacia in search of unoccupied acacias

(3) All worker ants very antagonistic to all queens Worker ants mildly antagonistic or not except colony queen and virgins inside thorns antagonistic to queens outside or inside of own colony thorns

(4) Many searching queens find each seedling Few searching queens find each seedling acacia; severe intra- and inter-specific com- acacia; little intra- and inter-specific competition for thorns petition for thorns among searching queens

(5) One founding queen takes over the acacia All original founding queens are incorporated early in the life of the colony and remains the in the colony, though eventually the polygyn- colony queen nous colony is descended from one queen

(6) Colony is 9 months or older before it is large Colony may have enough workers to protect enough to protect the acacia from herbivores against herbivores in 3-5 months

(7) Queens are monomorphic Queens are polymorphic (8) Founding queens are very adept at cutting Founding queens are inept at making en-

entrance holes in unopened swollen thorns trance holes in unopened swollen thorns *(9) Polymorphic thorns on the acacia, with 75- Monomorphic thorns, with five to fifteen

200 worker ants in the large thorn containing worker ants in the thorns containing colony the colony queens queens

(10) Colony queens change thorns one to three Frequency of movement of colony queens times per year; colony reacts strongly unknown; no reaction by worker during

movement (11) Trails across ground must occasionally con- Trails across ground between shoots are very

nect auxiliary shoots with the shoot contain- rare; colony queens in all occupied acacias ing the colony queen

(12) Number of alates produced per colony queen Number of alates produced per colony queen per lifetime is high per lifetime is low

(13) Alate production starts in second year of Alate production starts in first year of colony colony life life

(14) Maximum colony size of 20-30 thousand Maximum colony size of many millions of workers workers

*(1 5) Patrolling effectiveness decreases as amount Patrolling effectiveness is not reduced by of foliage occupied by colony increases; the increasing the size of clump of acacias; colony colony rarely occupies more than ten adult may occupy hundreds of acacias acacias

*(1 6) Most new acacias produced by seed and seed Very few new acacias produced by seed, seed produced at early age comes mostly from older trees

(17) Intense intra-specific competition for acacias No aggressive intra-specific competition for between mature ant colonies acacias between mature ant colonies

myrmex ferruginea, P. belti, P. nigrocincta in Guanacaste Province, Costa Rica, P. ferruginea and P. belti in north-eastern Guatemala, P. ferruginea in the gulf coastal lowlands of Mexico), they occurred daily in all seasons before sunrise on the top of outstanding objects such as tall trees or telephone poles. Here, a few virgin queens and


males emerge from each of the many colonies in the area and contribute to the swarm. The virgin queens and males leave the colony sometime between midnight and about an hour before dawn.

The mating flights of P. venefica occur on the branches of the acacia occupied by the colony that produces the queens. The males emerge from the thorns from about 2 h after sunset until about midnight (between 26 June and 4 July 1968 this occurred every night at Rio Palillo from about 09.15 to 24.30 hours). Within a few minutes after leaving the thorns, the males fly off the branches with a buzzing flight and are blown downwind by even the very lightest breezes. Virgin queens emerge from the same branches within about 3 hours before sunrise (02.00 to 03.00 hours at Rio Palillo, from 05.30 to 08.00 hours at Gabriel Zamora). They walk only a few centimetres, sometimes buzzing their wings, and assume the same position on a leaf or thorn as does a virgin monogynous queen in the top of a tall tree: the abdomen is elevated and the genital chamber fully open. Presumably she is releasing sex pheromones. The males fly upwind to the acacia, run or buzz about on the foliage, and copulate as soon as they encounter a queen. Copulation lasts about 10 s and is with only one male (as with monogynous queens). Since the males have been flying about for several hours before the queens appear, it is unlikely that brother-sister matings are any more common than with the monogynous queen mating flights away from the parent ant colony. The large queens (Table 1, point 7) mate in a manner not obviously different from that of the small queens. There are no indications that virgin P. venefica queens ever fly away from the acacia containing their parent ant colony.

I assume that mating flights occur throughout the year, since there are young colonies of all ages in seedlings, and reproductive broods of P. venefica are present in mature colonies from May through January, which includes all climatic seasons.

Not all polygynous obligate acacia-ants mate on the acacia. At Rio Palillo, the undescribed brown species has early morning mating on top of emergent trees. I do not know whether the newly fertilized queens find their way back to their parent colonies, or the large polygynous colonies take in any queen; I suspect the former is the case. In addition to the observed mating swarms, hundreds of males of this species were observed buzzing around and on the foliage of acacias occupied by colonies about an hour before sunrise (Rio Palillo, July). Many attempted to copulate with workers. While no virgin queens were observed on the acacia (they had left the acacia earlier for the mating flight away in a nearby tree top), the activity suggests that on some days mating may take place on the acacia, as in the case of P. venefica.

2. Search behaviour of newly impregnated queens

Newly mated monogynous queens drop out of the treetop after mating. After reaching the ground, they start off in search of unoccupied acacias. Flying a little, a searching queen may walk many hundreds of metres and can live as long as 30 days without food or water.

Once mated, a queen of P. venefica immediately tries to go into the entrance hole of the nearest thorn. She is usually repelled by the guard worker just inside the entrance hole, but she is not persistently attacked as would have been the case were she in a monogynous colony. She then tries the entrance hole of the next thorn down the branch. She continues this behaviour until admitted to a thorn, or she leaves the tree. When admitted, the occupants do not resist her and it is likely to be the same thorn that she was reared in;


five newly mated queens have been observed to enter the thorns from which they were known to have emerged. During six mornings of observation in July at Rio Palillo, twenty of thirty-eight queens that I followed eventually gained entrance to a thorn on the same branch where they mated (the longest search time was 42 min and this queen tried at least 116 thorns). There were zero to three physogastric queens in these twenty thorns before they were entered by the newly mated queens. Not all newly mated queens re-enter a thorn in their own colony, since searching queens (of P. venefica) may also be found on acacia seedlings. The other eighteen of the thirty-eight queens mentioned above eventually left their parental colony by running down the acacia trunk or falling off.

The behaviour of searching queens causes most, if not all, of the physogastric queens in a mature colony to come from the brood reared in the branch that bears their thorns. This brood, in turn, is most likely to have been produced from eggs made by the queens in the thorns on that branch. The result is that the queen in the thorn that subtends a newly elongating branch will probably stock that branch with her daughter and grand- daughter queens, while only a small amount of brood may have been produced by queens in thorns on the branch that bears the new branch. If the newly elongating branch is the central axis of a newly established seedling, then this fortunate queen and her family are likely to take over the whole acacia tree during the years to come (see further discussion under point 5 of Table 1).

Since the mating flight of the undescribed brown species occurs away from the acacia, it is unlikely that its searching queens behave in this manner; in this species, searching queens may be more easily accepted into the thorns of their parental colony after mating, or may not.even have to locate their parental colony to be accepted.

From the viewpoint of the genotype represented by the polygynous colony, we may expect selection to favour mechanisms that result in the colony absorbing as many of its own searching queens as it needs for queen replacement and egg production; the re- mainder should be forced to leave in search of new seedlings. The trait of allowing only a newly mated queen to re-enter the thorn from which she came is probably one such mechanism. A second mechanism is that the searching queens eventually leave the parental colony even though they are only mildly molested by the worker ants. Once she has wandered off the branch where she was born, she probably has almost no chance of getting into the colony, and she is therefore wasting time and energy on the parent colony acacia. It is relevant that it is the workers that clean out the new green thorns and stock them with brood derived from eggs produced lower down the branch. These workers do not-allow searching queens to cut entrance holes in the new green thorns.

The mortality patterns of monogynous and polygynous searching queens are probably quite different. The only monogynous searching queens that have any chance of surviving are those that find unoccupied swollen-thorn acacias. A certain number of polygynous searching queens are guaranteed survival in the parent colony; on the average, this should be the number of old queens that die per day plus about one-third of the daily increase in total acacia thorns available to the colony (based on the figure that there is about one-third of a physogastric queen for every thorn on a large acacia, Table 2). On the other hand, one may wish to view those queens which stay with the parent colony as merely extensions of their mothers' ovaries and therefore qualitatively different from the queens which start new colonies. It should be noted that the worker force is so efficient at preventing entrance by the wrong searching queens that it is unlikely that she could ever evolve a mechanism whereby she could enter a monogynous colony or polygynous thorn at will. We may also add that while it would momentarily increase the fitness of

Q

Table 2. Density offounding and colony queens of Pseudomyrmex venefica in swollen-thorn acacias of various ages

Number of Age of Number Number Number Number Number trees in trees of of of of of

Sample sample (height) queens thorns queens/thorn workers/shoot queens/shoot Gabriel Zamora, 10 June 1968 145 1-2 months 121 522 0-23 0*79 0-83

Unoccupied sucker shoots (16 cm)? New cornfield

Gabriel Zamora, 8 June 1968 14 1-6 months 4 57 007 0 57 0-29 Unoccupied sucker shoots (15 cm) Rocky hillside

Rio Palillo, 24 June 1968 81 1-2 months 123 348 0 35 0-65 1-52 Unoccupied sucker shoots (33 cm) New cornfield

Gabriel Zamora, 10 June 1968 76 1-2 months 90 517 0-17 37 1-18 Occupied sucker shoots* (20 cm)? New cornfield

Rio Palillo, 9 July 1968 6 12-15 months 97 293 033 548 16-16 Occupied sucker shoots-t (55 cm) Old cornfield

Gabriel Zamora, 16 June 1968 11 18-30 months 474 1894 0-25 2238 431[ Occupied sucker shootsl (65 cm) Rocky hillside

Tree III 1 5 years 619 2323 0-27 35 520 619 26-5 miles S.W. El Palmito,** (3 5 cm) Sinaloa, Mexico. 13 July 1968 Isolated tree (Total count)

Tree I 1 10 years 1478 4362 0-34 117 658 1478 Gabriel Zamora, 17 June 1968 (3-5 m) Isolated tree (Total count)

Tree IV 1 25 years 3934 10,868 0-36 180 409 3934 23-5 miles S.W. El Palmito,** (5 m) Sinaloa, Mexico. 5 June 1968 Isolated tree (estimate based on 10% of the tree crown)

* These shoots had 10-50 workers on their surface when undisturbed. t These shoots had 20-100 workers on their surface when undisturbed. I When undisturbed, these eleven acacias had 61-877 workers on their surface at mid-day (x = 286). ? The difference in height of occupied and unoccupied shoots in this field is due to protection by the ants and is highly significantly

different (P> 0-001, t-test). The occupied shoots were along the edge of the field and occupation provided by immigration from nearby uncut large acacias.

** Along Mexico Highway 40.


a foreign searching queen if she could be accepted by a colony, such behaviour by her colony would then lower her fitness through the admission of many other foreign searching queens.

3. Antagonism by worker ants to queens

In monogynous colonies, the worker ants viciously attack any male or queen except their own colony queen and their own virgin queens before they leave the thorns. Attack occurs even when a virgin queen or male has just left the thorn in which it was reared and is running along a branch before flying off the acacia in the early morning. There is no reason to believe that a newly mated monogynous queen is immune from attack by her parent colony. There are no auxiliary queens. If a searching queen in a monogynous colony happens to enter an empty thorn on an occupied acacia, she is pulled out by her antennae and eventually killed or chased off the acacia even when the colony occupies several acacias. If they can hold on to them, the workers kill all reproductives that they attack.

The workers in a mature colony of P. venefica or other polygynous species are only mildly aggressive to reproductives of their own species. During a mating flight on an acacia occupied by P. venefica, the fast-moving males are ignored or only occasionally bitten and dragged about. Virgin queen P. venefica may be bitten and dragged a few millimetres, especially when standing still while releasing sex pheromones; however, the workers are not persistent in their attack and do not sting these females. Copulating pairs are treated in the same manner. Newly mated queens may be chased on the acacia occupied by their parental colony, but not persistently. If caught, they are usually released after being dragged about. If searching queens are taken from the surface of seedling acacias and placed on acacias occupied by the same polygynous species, they are treated slightly more aggressively than searching queens of the colony occupying the acacia, and sometimes may be killed. However, these searching queens never successfully enter a thorn, owing to the guard worker blocking their passage through the thorn entrance.

If a physogastric monogynous queen is dissected out of her thorn and placed on the surface of her own acacia, she is not attacked and is rapidly dragged back into a thorn (though she may have much difficulty getting through the thorn entrance). When the same experiment (Plate lb) is done with physogastric queens of polygynous colonies from the same or different acacias, the workers usually react similarly (and see point 5, Table 1). On some occasions the workers attempt to drag these queens into particular thorns and there may be competition among the workers for a queen (on first sight this may appear to be an attack). A worker may also pick up a queen and drop her off the acacia. It is possible, however, that there is some aggression toward polygynous queens; polygynous physogastric queens often lack part or all of one or more legs or antennae. This mutila- tion may be caused by attack when a queen is leaving an old thorn and moving up the branch in search of a new one, or it may occur inadvertently when workers are trying to drag a queen into a thorn.

On young acacias, the workers chase searching queens with about the same intensity as they do on mature polygynous colonies. This happens in spite of the fact that at this time the young founding queens are not necessarily related and the worker force may be of mixed descent. Here, it is the founding queen in each thorn (or their workers in the thorns) that prevent further addition of unrelated queens to the colony as the young acacia produces new thorns.

When any queen of one polygynous species is placed on an acacia occupied by the


other polygynous species, the workers attack and kill her just as would the workers from a mnonogynous colony.

4. Intra-specific queen competition for thorns on seedlings

When there is a high density of adult monogynous colonies (e.g. more than five to ten per hectare), far more searching queens find nearby seedlings than there are thorns for them to occupy. The result is a substantial delay in colony foundation, since a young founding queen is likely to lose her brood when she leaves the thorn in search of food. While she is gone, another searching queen of any species is likely to enter the thorn, refuse entry to the original owner, and start her own colony after neglecting or discarding the previous brood (this interaction is eliminated once the first worker ant is produced, as it guards the entrance). Monogynous queens are adept at locating seedling acacias, and are commonly found in the thorns of seedling acacias many hundreds of metres from mature monogynous colonies.

With polygynous species, it is commonplace for most unoccupied seedlings to have only a small fraction of the thorns occupied by founding queens of any species. Many thorns even lack holes. This is the case even when there are hundreds of adult acacias in the immediate vicinity. For example, a cluster of 40-100 cm tall Acacia hindsii unoccupied seedlings (sucker shoots) had 306 thorns yet only nine of these contained founding queens of Pseudomyrmex venefica (2 January 1965, 4 miles north-east of the intersection of Highways 15 and 40, Sinaloa, Mexico). This cluster was only 40 m from a huge clump of Acacia hindsii that was producing hundreds of new queens each day. Further, this was the end of the rainy season and therefore during the previous five months, conditions had been ideal for queens that were searching for seedling acacias. A nearby unoccupied clump of seedling acacias had 162 thorns yet had no founding queens (there was one searching queen on the foliage). Such data were recorded repeatedly; Table 2 gives further information on the contents of the unoccupied shoots.

In a habitat with a high density of monogynous mature colonies, a seedling acacia may have as many as fifty searching queens on it by mid-morning (the record is 222 queens of Pseudomyrmex belti on a 40-cm unoccupied seedling near Playa Coco, Guana- caste Province, Costa Rica, 20 June 1965). However, polygynous searching queens are only occasionally found on seedling acacias. Some of the queens are absorbed by the mature colonies, and this may account in part for the fact that only a small number of searching queens find any given seedling acacia. However, it is probably also due to poor searching ability of the queens. The latter hypothesis is supported by the observation that seedlings with a few searching queens may be found within 3-10 m of clumps of acacias that daily produce hundreds of newly mated queens. However, founding and searching queens of P. venefica have been found on seedling Acacia hindsii many hundreds of metres from any adult A. hindsii.

Two important conclusions arise from these differences between monogynous and polygynous species. First, although a monogynous queen has possession of a thorn she has little chance of establishing a colony if there is a high density of mature colonies in the area. In this case there is also little chance of the seedling becoming occupied. In contrast, a polygynous founding queen is much more likely to survive until she loses through competition for the acacia crown (see point 5 in Table 1). Second, monogynous species appear to have a density-dependent population regulation mechanism operating. With polygynous species there appears to be no reduction in the rate of establishment of new colonies as the density of mature colonies increases, at least at the densities


observed in nature. With this in mind, it is not obvious why the riparian vegetation in the coastal lowlands of Nayarit, Mexico, is not a pure stand of A. hindsii.

A third outcome is that in areas with polygynous ant species, unoccupied seedling acacias tend to have a much larger and more diverse fauna of animals living in the thorns that lack founding queens than is the case in habitats with monogynous acacia-ants. These animals also persist longer in the development of the polygynous colony than they do in a monogynous colony. It is commonplace to find a large sapling A. hindsii with five to twenty young colonies of Pseudomyrmex venefica but the other thorns containing ant colonies of Camponotus, Paracryptocerus, Pseudomyrmex gracilis Guer. and P. nigropilosa Emery, and various beetles, spiders, microlepidoptera larvae, and bees (Hylaeus spp.).

5. Ontogeny of colony ownership

The monogynous founding queen that first produces a large worker force (100-300 workers) monopolizes the whole tree. Her workers kill or evict the other queens and their workers from the older thorns and occupy the new green thorns. Rapid production of aggressive workers will benefit both the queen and the acacia. Once established the colony remains monogynous. I have dissected hundreds of colonies of P. ferruginea throughout Central America and never found any which had two or more colony queens. I have dissected at least 100 colonies of P. belti and P. nigrocincta from Costa Rica to lowland Mexico; all have had only one colony queen.

As the P. venefica founding queens develop their colonies, each contributes workers to the overall patrolling force on the acacia (there is never more than one founding queen in a thorn at this stage in colony development). These workers intermingle freely on the acacia surface and show no sign of aggression towards other workers or to the queens in the thorns. As mentioned earlier, their mild attack of searching queens, plus their refusal to allow these queens to enter the thorns, restricts the initial number of founding queens in the colony to the number that enter before a patrolling force has developed (in Was- mann's (1910) terminology, the original colony is formed by 'primary pleometrosis', while the mature colony is formed through 'secondary pleometrosis'; Wilson (1963) observes that such 'claustral colony founding' is known for a number of ant species, and Waloff (1957) has shown that the fitness of individual queens may be higher in groups than on their own).

Eventually, the lineage of one of the founding queens occupies the entire tree through the following process. From the axil of one of the swollen thorns on the seedling acacia, a vertical shoot develops. As it grows, it bears new swollen thorns which are usually taken over by workers coming from the swollen thorn at the base of the new branch. These workers carry eggs from their queen's thorn to these new thorns, and eventually this brood produces alate queens. Some of these queens re-enter the thorn when they have mated. Through the medium of her daughter queens, the queen in the thorn located at the base of the branch that becomes the central axis of the acacia should therefore eventually be responsible for all the brood in the adult acacia. It should be emphasized that even a single founding queen of a polygynous species can establish a colony if the seedling is growing in a site where the acacia survives long enough for the queen to do the job herself.

When a seedling acacia is occupied by young colonies of two polygynous species, their workers fight inter-specifically for the acacia just as do the workers of monogynous colonies.


The speed and smoothness with which the colony changes from several lineages to one lineage depends on several variables. If one founding queen develops a large worker force well before the others do, she will quickly take over the colony since her workers will occupy the new thorns on the central axis (and on the other new branches) irrespective of the location of her thorn on the acacia. At the opposite extreme, if the acacia is growing in full sunlight, it may have a very bushy lifeform and each queen will remain in control of one or more large branches until one branch finally becomes the central axis of the tree. A third complication is provided by the merger of two large polygynous colonies. Here, two colonies come in contact through the growth of seedlings or sucker shoots in the vegetation between two large clumps of acacia. Since there is no aggression between the workers (point 17 of Table 1), it may be many years before one lineage occupies the entire cluster of acacias, if it ever does.

Once a polygynous colony becomes well established, the number of colony queens increases in proportion to the amount of foliage in the cluster of acacias. The mature acacias described in Table 2 have an average of 0 27-0 36 physogastric (colony) queens per undamaged thorn. Even using 0 27 colony queens per thorn as a minimum figure, a colony of P. venefica may easily contain 300 000 colony queens; it is easy to find a clump of acacias with 100 times the amount of foliage as was in the crown of tree IV in Table 2.

In a large and mature polygynous colony, there are two ways for a new thorn to obtain a colony queen. As the branch lengthens, eggs are carried into the new thorn from older thorns with queens. As described earlier, some of these may produce queens that, once mated, return to the thorn. On the other hand, a colony queen may leave an ageing thorn and emigrate up the branch to a newer thorn. To investigate the process of colonization at the new thorn, physogastric P. venefica queens were dissected out of thorns from other parts of the acacia and then released on marked thorns that were 1-2 months old (Gabriel Zamora, 11 June 1968). The queens were licked by nearby workers, never attacked, and often picked up and dragged into the thorn entrance if they did not get there immediately under their own power. These thorns were opened 5 days later and the queens examined. More than 7500 of them were still in the thorn that they had entered and were apparently very healthy. The maximum number of physogastric queens that entered a thorn and remained for 5 days was twenty-five and twenty-two. In both of these experiments the colony queens were brought from the other side of an old highway, so they were certainly from a different genetic lineage. The longest involved placing eleven physogastric queens in one thorn on 27 June (Rio Palillo, with the undescribed brown species of polygynous obligate acacia-ant) and 13 days later this thorn contained nine physogastric queens.

These experiments not only suggest that workers are not antagonistic to more than one queen per thorn, but that the queens are not strongly antagonistic to each other. This conclusion is the opposite from that often reached with other polygynous species of ants (e.g. Camponottis (Holldobler 1962)). However, on a long-term basis, some process must be evening out the distribution of queens among the thorns. For example, the 901 physogastric queens in branch 'G' of tree I in Table 3 were distributed such that 817, forty, and one thorns had one, two, and four colony queens in them respectively. There were also 1597 queenless brood thorns which presumably had room for a colony queen as well (this distribution of queens per thorn is significantly different from random at P>0-005, % = 127-43). It is probable that a queen normally immigrates to a queenless brood thorn as the acacia grows.

When a seedling or sucker shoot grows up near a mature polygynous colony, it is

Table 3. Percentage of Pseudomyrmex venefica founding (tree 1-11) and colony (tree I of Table 2) queens that were large, medium and small (all queens (n) in each tree or branch were recorded ('G' in tree I refers to the pooled sample of all branches not examined individually); C assignment to size categories was done by eye in thefield; 'large' and 'medium' should probably be pooled as they are nearly indistinguishable, >

representing the upper and lower halves of the large mhorph distributions in Fig. 2(b-e)) m

Tree number I Tree number Branch

Queen size 1 2 3 4 5 6 7 8 9 10 11 1 A B C D E F 'G' I z Large 21% 45% 30% 38% 0 59% 6% 24% 28% 27% 6% 31%o 26% 23% 35% 50% 100% 15% 35% 33% N Medium 50%o 33% 27% 31% 0 22% 24% 35%/ 14% 12% 6% 24%O 47% 61% 53% 36% 0 58% 44% 47% Z Small 29% 22% 43% 31% 100% 19%/o 70% 41%o 58% 61% 88% 45% 27% 17% 12% 14% 0 26% 22% 20% n 34 73 33 58 3 37 34 17 127 41 17 474 116 173 121 101 1 65 901 1478


occupied much as is a new branch within the mature acacia. To examine the progression of colony queen establishment, eight heavily occupied sucker shoots (from stumps of mature occupied acacias cut 1 month before) were dissected at Gabriel Zamora (7 June 1968). The terminal five thorns (youngest) had four physogastric queens out of forty thorns and the basal thorns (oldest) had thirty physogastric queens in forty thorns. In the middle of the sucker shoots, forty thorns chosen at random had ten physogastric queens. There was brood in every thorn. This time-dependent pattern of occupation by colony queens can be observed in any long branch in the crown of a mature acacia.

6. Speed of colony growth

Even when there is no competition between queens to hinder colony development (see point 4 of Table 1), a monogynous queen requires at least 9 months to produce a colony of 100-300 workers, the size at which effective patrolling of the acacia begins. This period can be lengthened indefinitely when competition between queens is intense, though it is generally cut short by death of the unprotected acacia.

Since each queen contributes some workers, the patrolling worker force in a polygynous species attains this size in about 2-8 months, depending on the number of queens in the acacia seedling and its general health. On the average, after 9 months these workers will be more effective at patrolling the acacia than will be an equal number of workers in a monogynous colony of the same age. This is because the older workers are more aggressive, and a higher proportion of the workers are old in the polygynous colony. As the colony continues to grow, the rate at which it is capable of adding workers is greater than in a monogynous colony, owing to the large number of queens.

The rate of production of young colonies has probably been of paramount importance in the evolution of polygyny in colony founding. The drier the acacia's habitat (longer and/or more intense the dry seasons), the more rapidly must a patrolling force become established if the acacia is to grow a crown large enough to survive the dry season and to feed the ant colony during that period of low productivity. Incidentally, inter-specific competition between young polygynous colonies will delay the establishment of a protective worker force, just as does inter- and intra-specific competition among monogynous species. This circumstance may also hinder the development of multiple-species com- munities of polygynous acacia-ants.

7. Queen polymorphism The queens of any given monogynous species vary little in size at any one site, and

show no indication of morphological polymorphism. Queens of any one colony of Pseudomyrmex venefica are clearly dimorphic in thorax

width (Fig. 1). The same pattern was seen in head width, but is not recorded here. There is no suggestion that this is related to some queens carrying out worker ant r6les, and should not be equated with the production of ergatoid queens in lower ants (cf. Wilson 1953). However, I had the distinct impression that the smaller searching queens were more successful at re-entering the thorns near where they mated than were the large searching queens. This impression is supported at Gabriel Zamora by comparing the ratio of small to large alate queens (6:143, Fig. lb) with the ratio for de-alate queens from the same colony (14:192, Fig. Ic). At the site of tree III (Table 2), the change is even more impres- sive; the same ratios are 14:98 and 25:57 (cf. Fig. Id and Fig. le) and are significantly different (X2 = 1013). Further, small physogastric queens that are removed from their thorns (point 5, Table 1) pass through the entrances of their new thorn more rapidly than


20- (n) 20 (b)

16 - 16

14~~~~~~~~~~~~~~~ _

4)C, 12 4605 0560647207607 082084 909609127

o~~~~~~~~~~~~~

E y z

z 4 ~~~~~~~~~~~4-

0 496 0532 07568 08604 00720 00756 07 92 0828 0864 09 0936 0 972

40 (c) 20

(d)

36- 16-

32 = 12

28~~~~~~~~~~~~2 C z~~~~~~~~~~~~~~~~~~~C 0~~~~~~~~~~~~~

~~~~~~ 20~~~~~~~~~~~~~-

xE -7 m ..=003 m ag 5 m 0684 072 075 0792e 028. 0864-aat

z~~~~~~~~~~

24

4~~~~~~~~~~~~~~

Thorax w0dt (m,range-672-0- mm) Thoraxmorph:n=192,x7= 0- wid th 792 = 0-(m

0584 mm, tree I of Table 2). (b ) Alat e (virgin) queens from inside thorns (smallm

mop:n = 6,, x = 07484 mm, S.D. = 00265 mm, range 07004-0776 mm; large morph: n=13 n=9,x= 08726 mm, S.D. = 00323 mm, range 08009592-84 mm, tree II of Table 2). ()D-lt

(e eaae(reproducing) queens from inside thorns (small morph: n = 14, x = 0724 8 mm, SD 0..=0029 mm, range, 0672-07562 mm; large morph: n = 192, x = 08840 mm, S.D. = 02 m

0-025 mm, range 0 808-0 916 mm, tree 1II of Table 2).


do large physogastric queens. No polymorphism is evident in the workers of P. venefica (Fig. la).

It is tempting to postulate that the large queens have higher searching and founding ability than the small queens when forced out of the colony after mating. To test this, the proportion of small and large queens in seedlings versus a nearby mature tree is compared in Table 3; these proportions clearly do not differ in the hypothesized direction as 45%O of the queens are small in the seedlings and 20% are small in the mature colony (these queens were graded to size by eye and the 'small' category undoubtedly contains a few with the lower tail of the 'large' size distribution in Fig. 1 a, b). This does not, however, adequately test the hypothesis as these seedlings were only 10-40 m from mature acacias. A much more satisfactory test would be to compare the ratios in seedlings many hundreds of metres from mature acacias with the ratios in mature colonies.

Not all polygynous queens are polymorphic. The undescribed brown species sympatric with P. venefica is monomorphic. Interestingly, the queens of Viticicola tessmani Stitz, an African pseudomyrmecine that apparently has a strongly mutualistic interaction with a rainforest vine (Bequaert 1922; Wheeler 1922), have as great a variation in size as Pseudomyrmex venefica; however, an adequate sample is not available to determine whether they are polymorphic.

8. Queen ability to cut entrance holes in thorns

Monogynous searching queens are very adept at cutting entrance holes in new green thorns. When green thorns are in short supply, they will even cut entrances in partly to totally seasoned thorns. If chased away from the task by a potential predator, they will return to work within a few minutes.

Searching queens of P. venefica and other polygynous species are often found standing inactive on the surface of seedling acacias that have a founding queen in every open thorn, yet have numerous green thorns with partly finished entrance holes; when chased away from partially completed entrances, polygynous searching queens often do not return to the task. I have no detailed time records, but it is my impression that a polygynous queen is much slower than a monogynous one at cutting an entrance hole. It is also possible that the small P. venefica searching queens are less competent than the large ones at cutting entrance holes. The low ability of polygynous queens to enter the thorns may be related to the low number of founding queens per seedling as compared with seedlings exposed to monogynous queens.

9. Thorn polymorphism

Acacias occupied by monogynous species have two distinct types of swollen thorns, which differ in size and shape. The majority of the thorns are comparatively small and are widely spaced along the lateral branches and central axis (type-A thorns (Janzen 1967a, 1973)). However, a few branches are greatly shortened and bear a few much larger and much stronger thorns (type-B thorns). For example, seventeen type-B thorns from one Acacia hindsii near Retalhuleu, Guatemala (19 June 1967), had an average volume of 4 9 cc (S.D. = 13, range 2-1-9-6) while fifty type-A thorns from the same tree had an average volume of 1-7 cc (S.D. = 0.5, range 0-6-1 8). The same measurements for an adult A. hindsii 27 miles east of Guatemala City (15 June 1967) are 5-7 cc (n = 11, S.D. = 0 9, range 3-3-8- 1) and 1'8 cc (n = 50, S.D. = 0-6, range 0'6-2' 1) respectively. In a mature colony, the colony queen is in one of the large thorns and is accompanied by seventy-five


to as many as 200 workers. Many of these workers remain in the thorn even if the tree is very violently disturbed. Type-B thorns are quite impervious to attack by birds seeking out larvae, while type-A thorns are frequently split (Janzen 1969). Since the colony will not accept a new queen if the colony queen is killed, and since a new colony cannot get started in the acacia until the workers of the old queenless colony have died (4-6 months), there is strong selection for the acacia to produce type-B thorns for the colony queen. Adjacent to the queen thorn there may be as many as three large thorns, each containing 500-2000 eggs. There are usually 4000-5000 in a Pseudomyrmex ferruginea colony of about 10 000 workers during the rainy season.

In regions where swollen-thorn acacias are occupied only by polygynous species, the acacias lack type-B thorns. There is some intra-acacia variation in thorn size in such regions, but all thorns are of the size and shape normally called type-A thorns. For example, ninety-nine thorns chosen at random from the 4281 thorns of an Acacia hindsii at Rio Palillo (4 July 1968) had an average volume of 09 cc (S.D. = 0 3, range 0-4-1-5). The same measurements for 121 thorns chosen at random from the 2823 thorns of tree III (Table 2) are 1-4 cc (S.D. = 0 3, range 0A4-2 1). While predation on ant brood by birds occurs with polygynous colonies, the loss of some colony queens is probably of little more importance to the acacia than is the loss of the brood. Associated with this, thorns containing colony queens have no more workers (five to fifteen) in them than do queen- free thorns with brood. When the acacia is severely disturbed, workers leave thorns with physogastric queens as readily as queen-free brood thorns.

The queen thorn of a monogynous species may have as many as 2000 eggs and almost never has larvae or other brood; it never contains alates. Queen thorns of polygynous species may contain up to 300 eggs but usually contain fewer. For example, in tree IV in Table 2, the nine thorns with eggs had 10-115 eggs each (average of sixty-four eggs per thorn); of the estimated 3934 physogastric queens in this tree, 40.900 had eggs in their thorns. This yields a conservative estimate of 102 976 eggs in the standing crop in a colony with at least 180 409 workers. This ratio is quite similar to that estimated earlier for a monogynous colony. Queen thorns of polygynous colonies contain some brood of all ages and may even contain a few newly emerged males.

The change from polymorphic to monomorphic thorns may easily occur within one widely distributed species of acacia. For example, A. hindsii ranges from Nicaragua to slightly north (and inland) of Mazatlan, Sinaloa, Mexico (Janzen 1973). Throughout that portion of its range occupied by Pseudomyrmex v,enefica, it has monomorphic thorns. From the Petatlan region (north of Acapulco) south through Guatemala it is strongly polymorphic for thorn type and occupied by monogynous obligate acacia-ants. The same change occurs in Acacia collinsii over the same relative portions of its geographic range.

10. Movements of the queen within the acacia crown

One to three times each year the monogynous colony queen ceases egg production for a short time (so that the very large gaster shrinks somewhat) and then moves to a younger type B thorn. This relocation is necessary so that she is always in a strong thorn (thorn walls begin to weaken with weathering at about 1I- years of age). There may also be selective value in the queen remaining centrally located in the acacia crown as it moves upward with tree growth. When the colony queen moves between thorns, almost the entire worker force patrols the surface of the acacia; the surface of the main branches may be completely covered with ants. The queen is covered with ants as she moves from


the old thorn to a new thorn, the entrance of which has already been somewhat enlarged by the workers.

I do not know how frequently polygynous colony queens move. It must be at least once every 2 years, because they are rarely found in thorns older than 2 years. Since physogastric polygynous colony queens are not as enlarged as are monogynous colony queens, they leave and enter new thorns with relative ease. They run rapidly up the branch and into a thorn five to fifteen thorns farther up the branch. The workers do not appear to resist her entry. However, she may be going to a thorn that was originally provisioned with her eggs by her workers. There is no obvious change in the behaviour of the workers on the surface of the acacia when the queen changes thorns. Occasionally a worker chases her, as though she were chasing a searching queen.

11. Connections between the shoots occupied by one colony

The acacias occupied by a large monogynous colony are occasionally connected by trails across the ground and vegetation during the warmest hours of the day. Eggs (and sometimes brood) are carried from the acacia containing the colony queen to the other acacias; this movement probably transfers pheromones from the colony queen to these queen-free colony fragments. The colony fragment in an acacia lacking a queen can maintain its social structure for 2-6 months without contact with the colony queen, but eventually its structure degenerates (patrolling effectiveness declines, sexual brood becomes nearly all male, etc.). If the acacias are close enough to have touching branches, there is generally a free and continuous traffic of ants between the acacias.

There is a continuous exchange of workers wherever there is branch contact among a clump of acacias occupied by a polygynous colony. However, since there are colony queens in almost every thorn, there is no need for egg or pheromone transfer between acacias. Trails between the widely spaced acacias occupied by a polygynous colony are very rare. They are formed only on the very hottest days, and therefore may be only for the purpose of distributing the nectar among the acacias. When an acacia is cut down, the colony readily forms a trail to a nearby living acacia and eventually the brood and queens move into one (just as with monogynous species). Where there is a new seedling or sucker shoot near an occupied acacia, the colony forms a trail to this plant, and colony queens as well as brood move into it. Since a polygynous colony may eventually be competitively eliminated through contact with another colony, there should be selection for a colony to minimize its contact with other colonies even if there is no aggression between workers which are derived from different queen lineages (point 17, Table 1).

12. Alate production

A large monogynous obligate acacia ant colony may produce as many as ten males and ten virgin queens per day (and therefore, per colony queen); such a colony has a standing crop of 50-200 alate queens in it when dissected.

A large polygynous colony probably produces far more than ten queens per day. For example, tree III (Table 2) had 1907 alate queens and 2420 males in it at the time of collection; there is no reason to believe this to be other than the normal standing crop. Since tree III had 619 colony queens, there were 3-08 alate queens per colony queen. Tree I (Table 2) had 901 alate queens and 542 males. There were 1478 colony queens in this tree and only 061 alate queens per colony queen. Given this low standing crop per colony queen, the number produced per day per colony queen may be less than in a monogynous colony. Even in this case though, if the colony is old and of one queen's


lineage, then there are many more produced per original queen per day than is the case in a monogynous colony.

13. Age at first reproduction by the ant colony

A monogynous colony produces the first males when it has 1000 to 1500 workers (and is about 15-24 months old) and the first queens when it has about 2000 workers. Alates are not produced in large numbers until there are at least 5000 workers in the colony (3-4 years of age).

Males first appear in a new polygynous colony when it has 100-500 workers, and the first alate females when it has 200-500 workers. The rate of alate production rises steadily and by the time there are 2000 workers in the colony (9-12 months old), there are reproductive adults or pupae in almost every thorn.

A colony queen in a young polygynous colony responds to two opposing selective forces in respect to age at first reproduction. Since the other colony queens are producing workers, any one queen can produce reproductives and only produce enough workers to gather food for the reproductive brood. However, the more she responds to this parasitic option, the less will be her chances of gaining ownership of the growing acacia; this ownership requires workers that can occupy the new thorns as they appear. At a different level, the more of the colony queens that begin to divert their resources to production of reproductives, the slower will grow the total worker force on the acacia (though this may not matter once the acacia has enough workers to ensure its survival to old age). This picture is further confounded by selection favouring the following behaviour. If a colony queen could assess whether she is losing the contest for the entire tree, we might expect that, when losing, she would shift to producing mostly reproductives.

The situation described will be highly variable and depend on the number of queens involved in starting the colony. For example, a 75-cm-tall A. hindsii with forty-six thorns (2 January 1965, 4 miles north-east of the intersection of Highways 15 and 40, Sinaloa, Mexico) contained one very physogastic queen and four founding queens that did not yet have brood. There were twenty-three thorns with brood in them and a total of 152 worker ants; eight thorns had alate virgin queens (nineteen queens in total) and two had males (two males in total). This single physogastric queen had started a substantial colony and reproduced at a far smaller colony size than could any monogynous queen. Incidentally, a more normal circumstance would have been for five to ten queens to have developed in about the same manner as did the single queen, leading to a much larger worker force on the acacia at the time of first production of alates.

14. Size of colony

A monogynous obligate acacia-ant colony rarely contains more than 20 000 workers though in very exceptional circumstances one may contain as many as 30 000 workers.

Polygynous colonies may contain almost an infinite number of workers, depending on the definition of 'colony'. An old and isolated clump of 100-200 acacias may have an average of 18 000 workers per acacia, as it is easy to find a clump with 100 times the volume of tree IV in Table 2. This means that the clump may contain 1 8-3-6 million workers. Exceptionally large clumps may cover several acres and have several thousand acacias; these are without doubt the largest ant colonies in the world. Colonies from widely separated areas do not fight when placed together (point 17, Table 1) (antagonism between workers is a common field test used by myrmecologists to determine if two groups of ants belong to the same colony). In a certain sense, we may regard the entire range of Pseudo-


myrmex venefica as occupied by the same ant colony. However defined, it appears that a polygynous ant colony that is derived from the lineage of only one colony queen should be able to grow as large as the resources permit. This size is set by how large a stand of acacia can grow in the face of competition with other plants.

15. Patrolling effectiveness versus number of acacias occupied by a colony

The larger the clump of adjacent acacias occupied by a monogynous colony, the less efficiently the marginal acacias are patrolled. When the number of shoots in a clump gets greater than, for example, ten 2-m-tall acacias or three to four large acacias, patrolling efficiency falls so low that further plants are not added to the clump because the peri- pheral plants are so heavily damaged by insects that they do not grow. I assume that the failure of the monogynous colony to protect an ever-increasing number of acacias is due to the inability of a single queen to produce eggs and/or pheromones at an ever-increasing rate.

As suggested in the previous section, the patrolling efficiency of polygynous colonies does not appear to be related to the number of acacias occupied by the colony. With a physogastric queen in a third of the thorns, the size of the patrolling worker force should be a simple function of the amount of food produced by the acacia clump. This means that the only limitation to the size of an acacia clump is the rate at which other species of trees grow high enough to shade out the acacias.

The population of acacias occupied by monogynous species tends to be made up of a large number of individual adult plants scattered through the habitat, with occasional clusters of two to ten adult plants. On the contrary, the population of acacias occupied by polygynous species tends to be constituted of large clumps along river and swamp edges where dense thickets are formed through extensive root sprouts, and of rare scattered clumps and old single adults on hillsides. While the total biomass of swollen- thorn acacias may be about the same in both cases if averaged over a large region, it is clear that there are many more genetically distinct individuals in the acacia population occupied by monogynous queens than in that population occupied by polygynous queens.

16. Method of reproduction

In vegetation that is neither influenced by modern agricultural techniques nor heavily grazed by cattle, nearly all acacias occupied by monogynous species are produced from seed. Seedlings commonly appear in new disturbed areas such as road shoulders, aband- oned fields, and dam sites; many of these become reproducing adults though cutting takes a heavy toll. Small clumps of acacias may occur through sprouts from lateral roots, but are not large for reasons given in the previous section. Since these clumps are not large, they do not deflect succession and thus it is unlikely that there will be much further reproduction from these sprouts from roots. However, if the vegetation is repeatedly cleared by cutting with a machete and/or heavily grazed or less frequently cleared by fire, much of the reproduction will be from root and stump sprouts. Seedlings do not do well under such a land-use regime, apparently owing to a lack of food reserves to replace the crown when it has been removed. Most adult acacias occupied by a monogynous colony simply grow up, set seed for several years, and then drop out as the local plant succession progresses.

Acacias occupied by polygynous colonies reproduce mostly by root sprouts and produce dense thickets that can delay succession for many years (cf. Fig. 4 in Janzen (1967b)). The normal pattern is for the first (oldest) acacia to root-sprout frequently and the mor-


phology of the clump is one or two large acacias (each as much as 50 years old) surrounded by smaller saplings of various sizes and ages. The old acacias in the clump produce very large seed crops as well as sucker shoots, but seedlings are rare in the surrounding habitat as compared with habitats of acacias occupied by monogynous colonies. I have been left with the impression that acacias occupied by polygynous colonies rarely become established, but once established they last a very long time. The oldest Acacia hindsii stump examined in the northern end of the distribution had over 100 annual growth rings (45 cm diameter stump, 8 m tall, 8-9 m diameter crown); if we can assume continuous occupation by an ant colony, then the ant colony may be this old as well. The maximum age of monogynous obligate acacia-ant colonies is probably 15-20 years.

The drier the site, the longer a clump of acacias occupied by a polygynous species appears to persist; in completely deciduous thorn forest in the northern part of the range of Pseudomyrmex venefica, the acacias are often canopy members of climax vegetation. In this case they live much longer than do acacias occupied by monogynous species in deciduous forest. The effect of the ants on clumping by the acacias is particularly striking if one species is observed over a wide geographic range. Acacia hindsii is clumped where occupied by Pseudomyrmex venefica, yet occurs as single plants where occupied by monogynous species to the south (Chiapas, Mexico, Guatemala and Honduras). In short, a contrast of monogynous with polygynous ant-acacia interactions is a contrast of a less iteroparous organism with a very iteroparous organism.

17. Competition between colonies

The workers of monogynous colonies of all ages fight with any other colony for possession of a swollen-thorn acacia. The winning colony kills the colony queen of the loser, and discards some of the loser's brood. In general, the colony with the most workers wins in intra-specific fights; the workers fight in pairs and in most cases, both members die from stings and dismemberment. Such fights most commonly occur when two occupied acacias grow into contact with each other, when a colony discovers another acacia nearby that has a weak colony, or when an acacia dies and the colony is then hard-pressed to find another acacia. A reliable test of ownership of an acacia is to put a small branch from it into the crown of a nearby acacia; if the invading workers fight, there are two colonies (and dissection of the acacias will yield two colony queens).

The workers of a polygynous colony do not fight with those of another conspecific colony, even when one acacia is moved as far as 10 miles before being placed in the crown of another. When two large trees are clearly owned by different conspecific polygynous colonies (e.g., from opposite sides of a river) and one is cut and placed in the crown of the other, the workers, brood and queens will usually have moved into the growing tree within two months. In this case there may be an average of one to two physogastric queens per thorn rather than the usual 0-2-0A4. When two conspecific colonies come in contact through having their clumps of acacias expand, they simply merge. If one colony has a substantially higher growth rate than the other, it is conceivable that one colony may eventually come to occupy the entire patch; this should, however, require many years. On an inter-specific basis, mature colonies of polygynous species fight as intensely as do monogynous conspecific colonies (Plate 1c).

CONCLUSIONS

The largest ant colonies in the world appear to have been generated by a simple ecological-


behavioural process. Cooperation among conspecific non-sibling founding queens maximizes the rate of colony growth and hence the rate of increase of protection of the acacia in a very harsh habitat. However, this co-operation results in a polygynous colony in which the workers of no one queen can recognize the workers of the other queens with sufficient accuracy to take over forcibly the newly established acacia. Eventual purity of the colony occurs therefore through scramble competition based on the growth rate of each sub-colony and fortuitous aspects of the sub-colony's position in the acacia. Since the acacia lives in a habitat where succession proceeds slowly, the growing colony comes to occupy a cluster of trees old enough (large enough) to support an immense colony of ants before the acacia disappears through successional changes. We may note in passing that the Beltian bodies and extra-floral nectar produced by one clump of acacias constitutes one of the largest bodies of food reliably available to any insect in a small area.

Of the many questions left unanswered by this study, one of the more important is why does the winning queen take over the acacia through queen production rather than just worker production, i.e. why does she remain polygynous once established? Part of the answer probably lies in the idea that reproducing a daughter queen in a thorn is a more secure form of thorn possession than just brood placed there by workers. A second aspect of the answer lies in the idea that as the acacia foliage volume increases rapidly with addition of sucker shoots to the clump, a single colony queen cannot produce eggs rapidly enough to keep the new thorns stocked with workers, yet stay small enough to live in a thorn and move from thorn to thorn as the thorns age and drop off the tree.

Just as a phenotype that maximizes individual seedling fitness may not maximize parent tree fitness, and vice versa, the newly mated queen's perception of the selective picture may be different from that of the parent colony. In a harsh habitat such as the one occupied by polygynous species, the newly mated queen has almost no chance of establishing a colony on her own. Even if she can find a seedling acacia and become a founding queen, she still has the problem of competing with the other queens for the acacia. On the other hand, she is assured of at least some reproduction if she can re-enter a thorn on her mother's acacia. That this option has the highest fitness for her is suggested by the observation that she always tries to get back into the acacia after mating. That this option does not always have the highest fitness for the parent colony is suggested by the observation that only a small fraction of the newly mated queens are allowed re-entry by the system. When she fails at entering her mother's acacia, two processes favour her striking off on her own in search of a seedling acacia (if these two processes were not present, then her best strategy would be to continue to attempt entry until death).

(1) If she succeeds in establishing her own colony, her fitness is enormous compared to what it would have been had she joined the thousands of queens in her mother's colony.

(2) The rarer the behaviour of attempting to found a colony on one's own becomes, the more intensely will such behaviour be selected for, owing to the increased probability of being the owner of a newly established acacia. However, there is a lower limit to this process. The population of acacia ants will go locally extinct if on the average not enough searching queens find the young acacia to get a colony going; on rare occasions a single queen may get a colony going on her own, but this must be a very rare event or the system would shift from polygynous to monogynous.

There is another area of balancing selection between the individual queen and the


colony. Since each colony contains many queens, a particular queen would appear to have the option of becoming a total parasite on the system by producing nothing but alates. The picture is somewhat different at different stages in colony development. If one of the founding queens does this in a young acacia, she lowers her own fitness in two ways. She lowers the probability that the acacia will survive at all and that her workers will be the ones eventually to own the acacia. As the acacia becomes established and the colony gets large, turning to production of only reproductives might cut off the food flow to the thorn (we do not know if workers feed only their parent queen) and will definitely lower the chance of her lineage taking over a branch, as she will have no way of occupying the new thorns as they appear. Associated with this would be the selective pressure favouring a worker behaviour whereby workers allow only those newly mated queens that they have raised back into their thorns.

Though as yet poorly documented, there are some areas in Guatemala, Honduras and Yucatan where monogynous and polygynous species appear to coexist in the same habitat. This may be a simple result of recent human disturbance having blurred the distinction between the harsher habitats occupied by polygynous species and those occupied by monogynous species of obligate acacia-ants. On the other hand, it is reason- able to expect some habitats where the two life-forms can co-exist, much as annual and perennial plants with similar life forms can coexist in some habitats. The sympatry of Pseudomyrmex venefica and the undescribed polygynous obligate acacia-ant in western Mexico is a mild case of this. The undescribed species is less polygynous than P. venefica and does not have polymorphic queens; it is not surprising in this context to find that they coexist only in the moister habitats within the range of P. venefica.

ACKNOWLEDGMENTS

This study was supported by NSF GB-5206, GB-7819, GB-7805 and GB-25189, and the University of Kansas. M. Beulig, N. Fashing, J. Gladstone, D. Kamm, L. Keeler and J. Vandervelt aided in data gathering and analysis. C. R. Carroll, C. M. Pond, C. W. Rettenmeyer and G. B. Williamson offered constructive criticism of the manuscript.

SUMMARY

(1) The colony and population traits of monogynous obligate acacia-ants (Pseudo- myrmex ferruginea and others) and polygynous obligate acacia-ants (P. venefica and others) are found to differ on many qualitative points (Table 1).

(2) Polygynous obligate acacia-ant colonies are probably the largest in the world, with respect to both the number of queens and workers. They appear to be evolutionarily derived from monogynous species as the product of environments where it is necessary for the founding queen ants to cooperate in colony foundation if the acacia is to survive. They remain polygynous as a result of the way that one queen (and her reproductive offspring) eventually takes over the entire tree, which in turn can grow very large because of the slow rate at which it is eliminated in succession; a polygynous colony is probably the only colony life form that can successfully occupy such a large acacia.

(3) Other outstanding traits of polygynous species, such as greatly reduced aggression between conspecific unrelated workers and queens, polymorphic queens, and mating on the parent acacia may be viewed as (necessary?) by-products of a polygynous interaction.

R


(4) The acacias respond evolutionarily to a polygynous ant colony through loss of polymorphism of the swollen thorns, increased perenniality, and increased size of clumps derived originally from one plant.

REFERENCES

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(Received 11 December 1972)

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Issue Table of ContentsJournal of Animal Ecology, Vol. 42, No. 3 (Oct., 1973), pp. 495-829The Dynamics of a Population of Leptopterna dolabrata (Heteroptera: Miridae) in Relation to its Food Resources [pp.495-507]Air Flow, Evaporation and Mineral Accumulation in Mounds of Macrotermes subhyalinus (Rambur) [pp.509-520]A Re-Interpretation of Gause's Population Experiments by Means of Simulation [pp.521-530]The Distribution of Pholidoptera griseoaptera (Degeer) (Orthoptera: Tettigoniidae) in England and Wales Related to Accumulated Temperatures [pp.531-537]The Factors Influencing the Selection of Food by the House Martin (Delichon urbica (L.)) [pp.539-564]The Population Dynamics and Host Plant Interactions of Strophingia ericae (Curt.) (Homoptera: Psylloidea) [pp.565-583]Activity of the Sea-Shore Bristle-Tail (Petrobius maritimus (Leach)) (Thysanura) at Low Temperatures [pp.585-598]Larval Settling Behaviour of the Acorn Barnacle (Balanus pacificus Pilsbry) and its Relation to Distribution [pp.599-609]The Analysis of Intra-Generation Change in Animal Populations [pp.611-622]Conditions of Co-Existence in Sympatric Breeding Populations of Acrocephalus Warblers [pp.623-635]The Prey and Predators of Phaenocora typhlops (Vejdovsky) (Turbellaria: Neorhabdocoela) Living in a Small Pond [pp.637-643]The Food of Grey-Faced Petrels (Pterodroma macroptera gouldi (Hutton)), with Special Reference to Diurnal Vertical Migration of their Prey [pp.645-662]Convergence of Population Biology and Adult Behaviour in Two Sympatric Butterflies, Neominois ridingsii (Papilionoidea: Nymphalidae) and Amblyscirtes simius (Hesperioidea: Hesperiidae) [pp.663-672]The Energy Relations of the Polychaete Neanthes (= Nereis) virens (Sars) [pp.673-692]Stability in Insect Host-Parasite Models [pp.693-726]Evolution of Polygynous Obligate Acacia-Ants in Western Mexico [pp.727-750]Low-Altitude Migration and Diurnal Flight Periodicity; the Importance of Plusia gamma L. (Lepidoptera: Plusiidae) [pp.751-760]Observations on the Density of Queens in Natural Colonies of Myrmica rubra L. (Hymenoptera: Formicidae) [pp.761-771]The Population Structure of Maniola jurtina (Lepidoptera: Satyridae): The Sex-Ratio Control [pp.773-778]Mortality of Sceliphron assimile Dahlbom (Sphecidae) Caused by the Eulophid Melittobia chalybii Ashmead [pp.779-784]The Effectiveness of the Coccinellid Beetle, Adalia bipunctata (L.), as a Predator of the Lime Aphid, Eucallipterus tiliae L. [pp.785-802]Distribution, Density, and Dispersion of Two Species of Atta (Hymenoptera: Formicidae) in Guanacaste Province, Costa Rica [pp.803-817]Reviewsuntitled [p.819]untitled [pp.819-820]untitled [p.821]untitled [pp.821-822]untitled [pp.822-824]untitled [pp.824-825]untitled [pp.825-827]untitled [p.827]untitled [pp.827-828]Short Notices [pp.828-829]

Erratum [p.829]Back Matter

evolution of polygynous obligate acacia-ants in western ......occupy swollen-thorn acacias that grow...

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