The Ants Chapter 13

CHAPTER 13. SYMBIOSES WITH OTHER ARTHROPODS

For more than a century it has been known that many species of insects and other arthropods live with ants and have developed a thriving symbiotic relationship with them. Most do so only occasionally, functioning as casual predators or temporary nest commensals. But a great many others are dependent on the ant society during part or all of their life cycles. These ant guests, commonly known as myrmecophiles, include a great variety of beetles, mites, collembolans, flies, and wasps, as well as less abundant representatives of a wide range of other insect groups (see Table 13-1). Myrmecophily is almost exclusively an invertebrate phenomenon. A respectable list of vertebrate species, including synbranch eels, frogs, lizards, snakes, birds, small and medium-sized mammals and even primates occasionally live with social insects or prey upon them. But very few are specialized for such an association (Myers, 1929, 1935; Hindwood, 1959; Scherba, 1965; Chew, 1979; Vogel and von Brockhusen-Holzer, 1984; Redford, 1987). The vast majority of obligate invertebrate symbionts are moreover arthropods, and it is among these organisms that the most striking adaptations for life with social insects have taken place. A number of these myrmecophiles make their homes in nests of the ants and enjoy all the social benefits of their hosts. Although the interlopers in some cases eat the brood, the ants treat the guests with astonishing tolerance: they not only admit the invading species to the nest, but often feed, groom and rear the guest larvae as if they were the ants' own young.

An ant colony possesses a complex system of communication (see Chapters 5 and 7) that enables it not only to carry out its collaborative activities in food gathering, brood care, and other social activities, but makes possible an instant recognition of nestmates and discrimination of foreigners. This identification and discrimination system functions like a social immune barrier: only colony members are allowed to enter the ant society, and alien individuals are harshly rejected. Nevertheless, by using various techniques, a considerable number of solitary arthropods have managed to penetrate ant nests. The fact that the ants treat many of these alien guests amicably suggests that the guests have broken the ants' communication and recognition code. In other words, they have attained the ability to “speak” the ants' language of mechanical and chemical cues.

History of myrmecophile studies
Before addressing this phenomenon in greater detail, it will be useful to review briefly the historical background of the study of myrmecophilous symbiosis. Erich Wasmann initiated the modern study of the subject. In 1894 and in subsequent publications he developed a classification that divides species into five behavioral categories, which reflect increasing levels of integration into the social system of their hosts:

1. Synechthrans. These arthropods are treated in a hostile manner by their hosts. They are predators for the most part, managing to stay alive by means of greater speed and agility or the use of defensive mechanisms such as repellent secretions and retraction beneath shell-like cuticular shields.

2. Synoeketes. These arthropods, which are also primarily scavengers and predators, are ignored by their hosts because they are either too swift or else very sluggish and apparently neutral in odor.

3. Symphiles. Also referred to occasionally as “true” guests, these symbionts are accepted to some extent by their hosts as though they were members of the colony.

4. Ectoparasites and endoparasites. These arthropods are conventional parasites. They live on the body surfaces of their hosts, or lick up their oily secretions, or bite through the exoskeleton and feed on their hemolymph, or penetrate the body itself.

5. Trophobionts. This category includes phytophagous homopterans, heteropterans, and lycaenid caterpillars that are not dependent on the social insects for food but instead supply their hosts with honeydew and nutritive glandular secretions. In exchange they receive protection from parasites and predators.

With the accumulation of more detailed information on the behavior of the symbionts in recent years, however, the Wasmannian classification has turned out to be considerably less than perfect. Many symbionts fit into more than one category. Symphiles, for instance, not only exist on the charity of their hosts, grooming and soliciting food from them, but also prey simultaneously on the hosts and their brood.

Several alternative schemes have been proposed to categorize the many life styles of myrmecophiles, by Delamare Deboutteville (1948), Paulian (1948), Akre and Rettenmeyer (1966), and Kistner (1979), respectively. In a more modern, ecological twist, Kistner distinguishes two major categories: (a) integrated species, “species which by their behavior and their hosts' behavior can be seen as incorporated into their hosts' social life”; and (b) non-integrated species, “species which are not integrated into the social life of their hosts but which are adapted to the nest as an ecological niche.”  Considering the complex diversity of myrmecophilous adaptations it is often difficult nevertheless to draw a clear distinction between “integrated” and “non-integrated” symbionts. Thus despite its considerable shortcomings, the original Wasmann nomenclature continues to be useful in labeling the majority of cases, and it is frequently employed as a kind of shorthand in the literature on social symbioses.

Diversity of myrmecophiles
The literature on myrmecophiles is enormous and growing each year, much of it consisting of incidental notes buried in taxonomic and ecological studies of selected genera and higher taxa. A very extensive review of solitary symbionts in insect societies was recently published by Kistner (1982). Much of the information on myrmecophiles is summarized in Table 13-1, which is based on the original table compiled by Wilson (1971), together with new information provided by Kistner's review and other publications.

Not surprisingly, the cumulative data reveal that certain taxa are much more preadapted for life as symbionts than others. The mites (Acarina), for example, are the foremost representatives among ectosymbiont species in terms of sheer numbers of individuals. Although there exist only a few quantitative faunistic investigations of symbionts in ant colonies, Rettenmeyer's study (1962a) of 150 colonies of army ants in Kansas and Panama is characteristic: he counted almost twice as many ectosymbiotic mites as all the other myrmecophiles taken together. Also, Kistner (1979) reports that he collected 3,288 mites from a single colony of the army ant Eciton burchellii. Mites find easy entry into nests either as scavengers that are too small and quiescent to be evicted by their hosts, or else as ectoparasites adapted for life on the body surface of the ants.

Myrmecophilous mites are rivaled in diversity by staphylinid beetles, a family of approximately 28,000 species. Staphylinids, like acarines, are predisposed to life in ant and termite nests by virtue of their preference for moist, hidden environments and the role they commonly assume as generalized scavengers and predators. The greatest variety of staphylinid symbionts is found in colonies of the “true” army ants, that is, the dorylines and ecitonines (Seevers, 1965; Akre and Rettenmeyer, 1966; Kistner and Jacobson, 1975; Kistner, 1979). But they also commonly occur in nests of nonlegionary ant species. Kistner (1982) lists 19 staphylinid genera recorded from nests of attine ants, 17 genera found with Solenopsis fire ants, and approximately 15 genera known to occur in nests of formicine ants. Diversity aside, probably the most abundant insect guests of social insects in general and army ants in particular are phorid flies. When all species are combined, as many as 4000 adults occur in a single ecitonine army ant bivouac (Rettenmeyer and Akre, 1968).

Another safe generalization is that by far the greatest diversity of species of myrmecophiles, measured either per host species or per host colony, is found with species that form exceptionally large mature colonies. The ultimate in this trend is found in the great faunas of symbionts that live with ecitonine and doryline army ants, the meat ants of the genus Iridomyrmex, and the leafcutters of the genus Atta, the nests of which normally contain from hundreds of thousands to millions of inhabitants. An exceptional variety of guests has also been recorded from large colonies of Hypoclinea in tropical Asia and the north temperate species of the Formica rufa group. By contrast, very few symbionts are known from nests of species with the smallest mature colony sizes, including the great majority of ponerine, dacetine and leptothoracine ants.

This last rule of population size lends itself readily to theoretical explanation. The insect colony and its immediate environment can be thought of as an ecological island, partitioned into many microhabitats that symbiotic organisms are continuously attempting to colonize (Wilson, 1971; Hölldobler, 1972). In general, species with the largest mature colony size possess the greatest diversity of ecological niches and also enjoy the longest average span of mature colony life. The more diverse the microhabitats presented by the host colony, the greater the potential diversity of symbiont species. Furthermore, a long colony life increases the probability that symbiotic propagules will penetrate a given colony at some time or other. It is also true that if colony size is large, the equilibrial population size of its symbionts will be proportionately large and their species extinction rate (measured as the number of symbiont populations going extinct per colony per unit of time) will be correspondingly low. In general: large colony size enhances three factors--long colony life, high microhabitat diversity, and low symbiont extinction rates--that reinforce each other to produce a higher diversity and abundance of symbiotic species.

The evidence reviewed by Wilson (1971) and Kistner (1979, 1982) shows that many species are able to maintain a viable population size only under the protection of large colonies. The great majority of very specialized species are uncommon, and many are rare and local in distribution.

The guests of army ants: an extremely rich community
The species of mites associated with army ants, according to Rettenmeyer, can be conveniently divided into two main groups: those that live in the refuse piles or “kitchen middens” of the ants, and those that live on the bodies of the ants or within their bivouacs. The latter group, the only true myrmecophiles in this case, have finely apportioned the environment through amazing feats of specialization. Several of the extreme adaptations are illustrated in Figure 13-1. Of special interest are the Circocyllibanidae, which are phoretic on adult workers but occasionally ride on larvae, adult males and queens (Elzinga and Rettenmeyer, 1975). They appear to live primarily on certain parts of the host bodies such as the mandibles, head, thorax and gaster of adult workers. Of equal interest are the Coxequesomidae which are specialized to live on the antennae or coxae of their Eciton hosts. The most extraordinary adaptation of all, however, is exhibited by the macrochelid, Macrocheles rettenmeyeri, which is a true ectoparasite. This mite feeds on blood taken from the terminal membranous lobe (arolium) of the hind tarsus of large media workers of its exclusive host species, Eciton dulcium. In the process it allows its entire body to be used by the host ant as a substitute for the terminal segment of the foot. Rettenmeyer (1962a) described its behavior as follows: “The mite inserts its chelicerae into the membrane, but it is not known if the palpi assist in holding to the ant. Presumably the mite feeds in this position and may be considered a true ectoparasite rather than a strictly phoretic form. . . . Army ants characteristically form clusters by hooking their tarsal claws over the legs or other parts of the bodies of other workers. Temporary nests or bivouacs of Eciton dulcium crassinode may have clusters several inches in diameter hanging in cavities in the ground. In small laboratory nests, when a worker hooked the leg with the mite onto the nest or another worker, the hind legs of the mite usually served in place of the ant's tarsal claws. The hind legs of the mite were never seen in a straight position but were always curved. In all cases the entire hind legs of the mite served as claws, not just the mite's claws. No difference was noted in the behavior of the ant whether its own claws or the hind legs of the mite were hooked onto some support. When no other part of the ant's leg was touching any object, adequate support was provided by the mite's legs for at least five minutes.” A second species, M. dibanos, was observed to parasitize Eciton vagans in the same manner.

Many of the mites found with Neotropical army ants are endowed with particular holdfast mechanisms, such as modified claws, empodia, specialized ridges and teeth on their enlarged dorsa, and highly modified posterior idiosomas that adapt the mites to specific regions of the hosts' bodies (Elzinga, 1978).

Mites, being much smaller than their hosts, function primarily as ectoparasites or scavengers within the army ant nests. Many of the insects, on the other hand, either scavenge or obtain part of their nutriment by licking the oily secretions of the bodies of the hosts, a specialized behavior referred to by Wheeler and a few other authors as “strigilation.” The nutritive value of strigilation is open to some question, at least in the case of the ecitophiles. Both Rettenmeyer and Akre have suggested that it also serves to transfer the host odor to the parasites. This hypothesis received support from the recent finding by Vander Meer and Wojcik (1982) that the scarabaeid beetle Myrmecaphodius excavaticollis acquires colony specific cuticular hydrocarbons from its Solenopsis hosts. Other insects feed on the booty brought in by the army ant host workers, or else prey on the hosts themselves, especially the defenseless larvae and pupae. As illustrated in Figure 13-1, the insect guests vary greatly in size and in the positions they take on the bodies of the host workers. They also vary in the locations they prefer within the bivouac as a whole and the ant columns during colony emigrations and raids.

A typically instructive case of positional specialization is provided by the aleocharine staphylinid Tetradonia marginalis. Akre and Rettenmeyer (1966) note Tetradonia marginalis “is the most common staphylinid found in refuse deposits of Eciton burchellii and in the emigrations. Sometimes more than 100 individuals can be found in a single large deposit of this host. Many of these myrmecophiles do not run along the emigration columns but apparently fly from one colony to another. Tetradonia marginalis was the species most frequently attacking uninjured, active workers as well as injured workers of both Eciton burchellii and Eciton hamatum along edges of columns and near bivouacs [Figure 13-2]. The staphylinids were not seen to attack workers running along in the middle of raid or emigration columns or those running quickly along the edges.”

During recent field work in La Selva, Costa Rica, we were able to confirm some of the observations of Akre and Rettenmeyer. We were especially intrigued by the beetles' spatial positions at the end of the emigration columns and the hunting techniques they employed while there. For an hour late in the evening of March 28, 1985, we watched as a large part of the emigration column of Eciton hamatum crossed a forest path. At the very end of the column, with no more than 100 stragglers on that portion of the trail, we spotted ten or more of Tetradonia marginalis running swiftly along the trail, abdomen curled up over the thorax. Most were attacking Eciton media workers, and one was attacking a major. All of the victims were slow and partly disabled, unable to walk swiftly. We speculated that they had fallen back due to injuries or sickness, and had been singled out by the beetles for attack. The staphylinids circled around, seizing the legs or tips of the abdomens, in the latter case seeming to bite the anal region of the ant. Some dragged their victims swiftly along the trail by a leg and even those appearing to bite the anal region started off in this manner within a few minutes. In one instance two beetles attacked an ant together, running along with it in a coordinated fashion. One staphylinid flew off when we tried to capture it.

Akre and Rettenmeyer (1966) made a distinction between “generalized” species of symbiotic staphylinids, having the typical appearance of most Staphylinidae and with no obvious modifications for life with ants, and “specialized” species, which include mimetic forms (to be described later in this chapter). The specialized staphylinids are distinguished by the possession of rigid abdomens that are held in a single position (Figure 13-3). Paradoxically, these insects are also less common than the nonmimetic forms in the host colonies. Akre and Rettenmeyer compiled an impressive list of consistent behavioral differences between the two kinds of species, which we have reproduced in Table 13-2. These data reveal a gradually increasing degree of behavioral integration with the host society, which may constitute the most obvious of the evolutionary pathways along which progress in symbiosis can be measured. The two kinds of species can be reasonably interpreted as progressive stages in an adaptation to the host ants and their way of life.

The ant colony as an ecosystem
In more general terms, the concept of an insect colony as an ecological island, or, to use a slightly more precise language, a partially isolated ecosystem, can be extended to gain a better understanding of certain aspects of the biology of the symbionts. The ant colony and its surroundings is richly structured into many diverse microhabitats, such as the foraging trunk routes, refuse areas, peripheral nest chambers and guard nests, storage chambers, brood chambers with separate areas for pupae, larvae and eggs, queen chambers, and the bodies of adult and immature inhabitants of the nest. These microhabitats are occupied by a diversity of symbionts, which show special adaptations to each of the niches in turn.

The body of the host ants. The bodies of ants are occupied internally by a diversity of endoparasites, including nematodes (Gösswald, 1938b), termatodes (Hohorst and Lämmler, 1962; Schneider and Hohorst, 1971) and cestodes (Muir, 1954; Plateaux, 1972; Buschinger, 1973b). This form of parasitism can affect the individual host's morphology (Gösswald, 1938; Kutter, 1958), metabolism (Kloft, 1949) and behavior (Hohorst and Graefe, 1961), but it usually has little impact on the social behavior of the host ants. We will therefore not discuss this subject in greater detail.

One endoparasite, however, deserves special mention, namely the tachinid fly Strongygaster globula (formerly called Tamiclea globula), whose larvae develop as endoparasites inside the gaster of colony founding queens of Lasius niger and Lasius alienus (Gösswald, 1950). The behavior of the infected queens is not noticeably affected, except that they cease to lay eggs. When the last instar larva of the parasite leaves the host's abdomen through the cloaca, it quickly pupates and is groomed and tended by the host ants as if it were a member of the ants' own brood (Figure 13-4). In contrast, the fly imago is not treated amicably by the ant and has to leave the incipient ant nest quickly. The ant queens infected with Strongygaster die after the parasites leave the nest.

The bodies of immature and adult army ants, as noted earlier, provide special microhabitats for a diversity of ectosymbionts. The same is true for nonlegionary ant species. Probably the best known examples are species of the antennophorid mite genus Antennophorus, which live with formicine ants of the genera Lasius and Acanthomyops (Janet, 1897b; Wasmann, 1902; Karawajew, 1906; Wheeler, 1910b). The mites ride on the bodies of the ants, shifting their positions when two or more are present on the same ant so as to produce a balanced load. When three mites are present, two ride on either side of the gaster, and the third on the lower surface of the head (Figure 13-5). When four are present two position themselves on either side of the abdomen and head, respectively. The workers first try to remove the mites from their bodies, but seem to give up after several unsuccessful attempts.

The Antennophorus live on food regurgitated by the ant hosts, either imbibing it as it passes between workers or soliciting it directly by stroking the mouthparts of workers with the long, antennal-like forelegs. In the latter case the mites evidently imitate the tactile signals used by the ants themselves. It has even been observed that mites attached to the gaster of one worker are able to solicit food from another. The mites prefer to mount newly eclosed workers. This habit confers a distinct advantage: young workers usually stay inside the nest, and they are attractive to older workers who frequently feed them by regurgitation, affording the mites plenty of opportunity to participate in the trophallaxis.

A remarkable analogy to Antennophorus in its ectosymbiotic adaptations has been discovered by K. Hölldobler (1928) in the phorid fly Metopina formicomendicula, which lives in nests of the thief ant Solenopsis fugax. The Metopina adult mounts thief ant workers and rapidly strokes the head and mouthparts of the ant with its forelegs. The worker usually responds by slightly raising her head, opening her mandibles, and regurgitating a droplet of food, which is then rapidly imbibed by the fly (Figure 13-6). The ants occasionally attack the phorids when they move through the nest, but they rarely succeed because the flies are too swift and elusive. When resting the Metopina frequently ride on the queen, where they are usually ignored by the workers. Karl Hölldobler (1951) categorized Metopina as a “synoekete of the evasive type.”

Trails and kitchen middens. Many guests of army ants, and especially the staphylinid beetles, regularly accompany raiding columns, where they prey on the captured booty of their hosts or on the host ants themselves. These myrmecophilous scavengers and predators, as exemplified by Tetradonia marginalis, often bring up the “rear guard” of the raiding columns, sprinting deftly along each twist and turn of the newly vacated trails. It has been known for a long time that guests of army ants can orient by the odor trails without further cues provided by the hosts. Since army ants frequently change the location of their bivouacs, it is important for the myrmecophiles to be able to follow the emigration trails. Akre and Rettenmeyer (1968) investigated this phenomenon systematically by exposing a large variety of guests of ecitonine army ants to natural odor trails laid over the floor of the laboratory arena. They found that nearly all of the species tested, including a haphazardly chosen sample of Staphylinidae, Histeridae, Limulodidae, Phoridae, Thysanura, and Diplopoda, were able to orient accurately by means of the trails alone. However, some myrmecophiles did better than others. For example, the staphylinids Ecitomorpha, Ecitophya, and Vatesus, which regularly accompany ant columns in close formation, followed experimental trails readily and accurately, whereas phorid flies, which under natural conditions exhibit a kind of meandering movement along emigration trails, deviated more frequently from the experimental trails. Other species, such as histerid beetles, which normally ride on host ants or booty in ant columns, did relatively poorly in the trail-following tests.

In some instances the guests were more sensitive to trail pheromones than the ants themselves. In choice tests the symbionts preferred trails laid by their own host species to those of other army ants, and sometimes they were repelled by the trails of the wrong species. However, a few instances were recorded in which the ecitophiles were less specific in their response. Interestingly, the behavior was partly correlated with the myrmecophiles' acceptance of several host species in nature. None of the symbionts showed an ability to distinguish the trails of its own host colony in competition with trails laid by other colonies belonging to the same species.

Trail following may also be a means by which parasites locate the host colony. Kistner (1979) observed a limuloid beetle Mimocetes as it flew into a raiding column of Dorylus, then zigzagged from one side to another for about 10 cm, and finally entered the thick swarm of driver ants. The cockroach Attaphila fungicola lives with the fungus growing ant Atta texana, the workers of which depend strongly on odor trails for orientation during foraging expeditions and colony emigrations. Moser (1964) demonstrated that Attaphila fungicola follows the trail pheromone of its host ants, which he extracted directly from the poison gland of the workers and laid arbitrarily along selected routes in the laboratory. This experiment substantiates an earlier observation by Bolivar (1905) of Attaphila schuppi following trails of Acromyrmex in the field in Brazil. Moser also noted that the cockroaches do not depend solely on the ability to disperse from nest to nest, because individuals have been observed riding on the backs of Atta texana queens during the nuptial flights of these ants. The myrmecophilous cricket Myrmecophila manni probably also disperses along the foraging trails of its host, the mound-building ant Formica obscuripes. Henderson and Akre (1986a,b) recently observed a total of 63 crickets, including both sexes and all nymphal instars, on foraging trails of Formica obscuripes more than 20 meters distant from the nests. During June and July these insects were seen running on the trails nearly every evening from dusk to almost midnight.

In more general terms, the concept of an insect colony as an ecological island, or, to use a slightly more precise language, a partially isolated ecosystem, can be extended to gain a better understanding of certain aspects of the biology of the symbionts. The ant colony and its surroundings is richly structured into many diverse microhabitats, such as the foraging trunk routes, refuse areas, peripheral nest chambers and guard nests, storage chambers, brood chambers with separate areas for pupae, larvae and eggs, queen chambers, and the bodies of adult and immature inhabitants of the nest. These microhabitats are occupied by a diversity of symbionts, which show special adaptations to each of the niches in turn.

The body of the host ants. The bodies of ants are occupied internally by a diversity of endoparasites, including nematodes (Gösswald, 1938b), termatodes (Hohorst and Lämmler, 1962; Schneider and Hohorst, 1971) and cestodes (Muir, 1954; Plateaux, 1972; Buschinger, 1973b). This form of parasitism can affect the individual host's morphology (Gösswald, 1938; Kutter, 1958), metabolism (Kloft, 1949) and behavior (Hohorst and Graefe, 1961), but it usually has little impact on the social behavior of the host ants. We will therefore not discuss this subject in greater detail.

One endoparasite, however, deserves special mention, namely the tachinid fly Strongygaster globula (formerly called Tamiclea globula), whose larvae develop as endoparasites inside the gaster of colony founding queens of Lasius niger and Lasius alienus (Gösswald, 1950). The behavior of the infected queens is not noticeably affected, except that they cease to lay eggs. When the last instar larva of the parasite leaves the host's abdomen through the cloaca, it quickly pupates and is groomed and tended by the host ants as if it were a member of the ants' own brood (Figure 13-4). In contrast, the fly imago is not treated amicably by the ant and has to leave the incipient ant nest quickly. The ant queens infected with Strongygaster die after the parasites leave the nest.

The bodies of immature and adult army ants, as noted earlier, provide special microhabitats for a diversity of ectosymbionts. The same is true for nonlegionary ant species. Probably the best known examples are species of the antennophorid mite genus Antennophorus, which live with formicine ants of the genera Lasius and Acanthomyops (Janet, 1897b; Wasmann, 1902; Karawajew, 1906; Wheeler, 1910b). The mites ride on the bodies of the ants, shifting their positions when two or more are present on the same ant so as to produce a balanced load. When three mites are present, two ride on either side of the gaster, and the third on the lower surface of the head (Figure 13-5). When four are present two position themselves on either side of the abdomen and head, respectively. The workers first try to remove the mites from their bodies, but seem to give up after several unsuccessful attempts.

The Antennophorus live on food regurgitated by the ant hosts, either imbibing it as it passes between workers or soliciting it directly by stroking the mouthparts of workers with the long, antennal-like forelegs. In the latter case the mites evidently imitate the tactile signals used by the ants themselves. It has even been observed that mites attached to the gaster of one worker are able to solicit food from another. The mites prefer to mount newly eclosed workers. This habit confers a distinct advantage: young workers usually stay inside the nest, and they are attractive to older workers who frequently feed them by regurgitation, affording the mites plenty of opportunity to participate in the trophallaxis.

A remarkable analogy to Antennophorus in its ectosymbiotic adaptations has been discovered by K. Hölldobler (1928) in the phorid fly Metopina formicomendicula, which lives in nests of the thief ant Solenopsis fugax. The Metopina adult mounts thief ant workers and rapidly strokes the head and mouthparts of the ant with its forelegs. The worker usually responds by slightly raising her head, opening her mandibles, and regurgitating a droplet of food, which is then rapidly imbibed by the fly (Figure 13-6). The ants occasionally attack the phorids when they move through the nest, but they rarely succeed because the flies are too swift and elusive. When resting the Metopina frequently ride on the queen, where they are usually ignored by the workers. Karl Hölldobler (1951) categorized Metopina as a “synoekete of the evasive type.”

Trails and kitchen middens. Many guests of army ants, and especially the staphylinid beetles, regularly accompany raiding columns, where they prey on the captured booty of their hosts or on the host ants themselves. These myrmecophilous scavengers and predators, as exemplified by Tetradonia marginalis, often bring up the “rear guard” of the raiding columns, sprinting deftly along each twist and turn of the newly vacated trails. It has been known for a long time that guests of army ants can orient by the odor trails without further cues provided by the hosts. Since army ants frequently change the location of their bivouacs, it is important for the myrmecophiles to be able to follow the emigration trails. Akre and Rettenmeyer (1968) investigated this phenomenon systematically by exposing a large variety of guests of ecitonine army ants to natural odor trails laid over the floor of the laboratory arena. They found that nearly all of the species tested, including a haphazardly chosen sample of Staphylinidae, Histeridae, Limulodidae, Phoridae, Thysanura, and Diplopoda, were able to orient accurately by means of the trails alone. However, some myrmecophiles did better than others. For example, the staphylinids Ecitomorpha, Ecitophya, and Vatesus, which regularly accompany ant columns in close formation, followed experimental trails readily and accurately, whereas phorid flies, which under natural conditions exhibit a kind of meandering movement along emigration trails, deviated more frequently from the experimental trails. Other species, such as histerid beetles, which normally ride on host ants or booty in ant columns, did relatively poorly in the trail-following tests.

In some instances the guests were more sensitive to trail pheromones than the ants themselves. In choice tests the symbionts preferred trails laid by their own host species to those of other army ants, and sometimes they were repelled by the trails of the wrong species. However, a few instances were recorded in which the ecitophiles were less specific in their response. Interestingly, the behavior was partly correlated with the myrmecophiles' acceptance of several host species in nature. None of the symbionts showed an ability to distinguish the trails of its own host colony in competition with trails laid by other colonies belonging to the same species.

Trail following may also be a means by which parasites locate the host colony. Kistner (1979) observed a limuloid beetle Mimocetes as it flew into a raiding column of Dorylus, then zigzagged from one side to another for about 10 cm, and finally entered the thick swarm of driver ants. The cockroach Attaphila fungicola lives with the fungus growing ant Atta texana, the workers of which depend strongly on odor trails for orientation during foraging expeditions and colony emigrations. Moser (1964) demonstrated that Attaphila fungicola follows the trail pheromone of its host ants, which he extracted directly from the poison gland of the workers and laid arbitrarily along selected routes in the laboratory. This experiment substantiates an earlier observation by Bolivar (1905) of Attaphila schuppi following trails of Acromyrmex in the field in Brazil. Moser also noted that the cockroaches do not depend solely on the ability to disperse from nest to nest, because individuals have been observed riding on the backs of Atta texana queens during the nuptial flights of these ants. The myrmecophilous cricket Myrmecophila manni probably also disperses along the foraging trails of its host, the mound-building ant Formica obscuripes. Henderson and Akre (1986a,b) recently observed a total of 63 crickets, including both sexes and all nymphal instars, on foraging trails of Formica obscuripes more than 20 meters distant from the nests. During June and July these insects were seen running on the trails nearly every evening from dusk to almost midnight.

It is well known that caterpillars of the lycaenid Maculinea teleius change from phytophagous to myrmecophilous habits after casting the skin of the third larval instar. It was previously assumed that the myrmecophilous stage is carried by its host ants, Myrmica rubra, into the host nest, where the Maculinea larvae prey on the ant brood (Malicky, 1969). However, Schroth and Maschwitz (1984) recently found that fourth instar larvae of Maculinea teleius actively move into the host ants' nest, thus confirming an earlier observation by Chapman (1919). In laboratory experiments Schroth and Maschwitz demonstrated that the lycaenid larvae follow trail pheromones of their host ants when searching for the nests.

Trails and ant paths not only serve as orientation cues, they also inadvertently create a diversity of ecological niches within which the symbionts specialize. The Eciton army ants and their attending ecitophiles provide some of the most striking examples of modes of adaptive radiation. Another, wholly unexpected case involves the adult females of three nymphalid butterfly species, Mechanitis isthmia, M. doryssus, and Melinaea imitata, which regularly follow raiding swarms of the army ant Eciton burchellii. Ray and Andrews (1980) found that these butterflies feed on bird droppings in the swarm vicinity. Many species of birds, mostly in the antbird family Formicariidae, deposit droppings as they follow raiding swarms of Eciton burchellii to feed on insects flushed from the leaf litter by the ants (Willis and Oniki, 1978). Thus, army ant swarms provide an indirect yet reliable and relatively rich source of nutrients in the form of bird droppings. Although no experimental proof has yet been attempted, it is most likely that odors associated with the swarms may allow the butterflies to orient to the general vicinity of the droppings.

The trails and paths of nonlegionary ant species also harbor a diversity of myrmecophiles. One of the most fascinating examples is the nitidulid beetle Amphotis marginata, the “highwaymen” of the local ant world (Figure 13-7). These beetles occupy shelters along the foraging trails of the formicine ant Lasius fuliginosus during the day. At night they patrol the trails and successfully stop and obtain food from ants returning to the nest. Ants that are heavily laden with food are easily deceived by the beetles' simple solicitation behavior. The Amphotis adult induces an ant to regurgitate food droplets by using its short antennae to trap the ant's labia and rapidly drum on its head (Plate 16). Soon after the beetle begins to feed, however, the ant seems to realize it has been tricked and attacks the beetle. The beetle then is able to defend itself simply by retracting its appendages and flattening itself on the ground. With the aid of special setae on its legs it firmly attaches its lower body surface to the ground. The ant is then unable to lift the beetle or turn it over (Hölldobler, 1968, unpublished observations). This mechanism appears to give the beetle nearly complete protection. A somewhat similar parasitic pattern is exhibited by the calliphorid fly genus Bengalia. This paleotropical form has been reported to steal prey and larvae from columns of doryline driver ants and trails of a large number of nonlegionary ant genera (Bequaert, 1922; Maschwitz and Schönegge, 1980).

A diversity of insect predators settles near ant trails and preys on the ants. They employ an astonishing repertory of hunting techniques to capture their prey without being attacked or killed by the usually very aggressive ants. Some of the most specialized predators occur among the Hemiptera (Jordan, 1937). One remarkable hunting technique is employed by the reduviid bug Acanthaspis concinnula (Mühlenberg and Maschwitz, 1976). This species lives near the nests of the fire ant Solenopsis geminata. The bug captures Solenopsis workers, immobilizes them by injecting poison, and then sucks out the hemolymph. Then it places the shriveled corpses on its back. The accumulated shield of dead victims provides an excellent disguise and even attracts other ant workers, which approach to inspect their freshly killed nestmates. A similar “shielding behavior” has been described in some hunting spiders (Oliveira and Sazima, 1984). A wholly different method is employed by the reduviid bug Ptilocerus ochraceus (Figure 13-8) of Java, which feeds to a large extent on the dolichoderine ant Hypoclinea biturberculata, an extremely abundant ant in southeastern Asia (Jacobson, 1911). The predators take up a position in or near an ant path and offer an intoxicating attractant secreted from trichome glands on the underside of the bug's abdomen. On encountering a Hypoclinea worker the bug presents the trichomes by raising the front of the body, simultaneously lifting up its front legs, “. . . folding them in such a manner that the tarsi nearly meet below the head. The ant at once proceeds to lick the trichomes, pulling all the while at the tuft of hairs, as if milking the creature, and by this manipulation the body of the bug is continually moved up and down. At this stage of the proceedings the bug does not yet attack the ant; it only takes the head and thorax of its victim between its front legs, as if to make sure of it; very often the point of the bug's beak is put behind the ant's head, where it is joined to the body, without, however, doing any injury to the ant. It is surprising to see how the bug can restrain its murderous intention as if it was knowing that the right moment had not yet arrived. After the ant has indulged in licking the tuft of hair for some minutes the exudation commences to exercise its paralyzing effect. That this is only brought about by the substance which the ants extract from the trichomes, and not by some thrust from the bug, is proved by the fact, that a great number of ants, after having licked for some time the secretion from the trichomes, leave the bug to retire to some distance. But very soon they are overtaken by the paralysis, even if they have not been touched at all by the bug's proboscis. In this way a much larger number of ants is destroyed than actually serves as food to the bugs, and one must wonder at the great profligacy of the ants, which enables them to stand such a heavy draft on the population of one community. As soon as the ant shows signs of paralysis by curling itself up and drawing in its legs, the bug at once seizes it with its front legs, and very soon it is pierced and sucked dry” (Jacobson, 1911).

A similar waylaying technique is employed by larvae of the carabid beetles Sphallomorpha colymbetoides and Sphallomorpha nitiduloides, which prey on the Australian meat ants Iridomyrmex purpureus, also a dolichoderine species. Moore (1974) discovered that the beetle larvae dig burrows near the nests and paths of the meat ants and wait for passing Iridomyrmex workers. When an ant approaches, the larva lunges at her, grasping the ant's legs and holding her for one or two minutes. The struggling ant soon relaxes, apparently in a state of paralysis. Moore speculates that the larva might apply toxic secretions, possibly from its maxillary glands. This, however, has not yet been tested experimentally. Once the prey is motionless, the larva sucks out the hemolymph of the ant and then discards the shriveled corpse. Often several Sphallomorpha burrows are found grouped together. Moore believes that the aggregation improves the predators' hunting success, because captured meat ants discharge an alarm pheromone that attracts other ants from nearby.

A similar ecological niche near ant nests or ant paths is occupied by ant lions, which are members of the order Neuroptera. The larvae of these insects build funnel-shaped pit traps in loose soil, where they wait on the bottom for ants to slip and fall down to them (Wheeler, 1930). However, the ant lion larvae are not exclusively predators on ants. Of 222 prey of the species Myrmeleon immaculatus identified by Heinrich and Heinrich (1984), only 36 percent were ants.

Yet another, very different technique exploiting trails and kitchen middens is employed by the European staphylinid beetle Pella funesta (Hölldobler et al., 1981). In early spring the adult beetles deposit eggs near the kitchen middens of the formicine ant Lasius fuliginosus. The larvae develop in the refuse pile and pupate sometime during May to July. In July or August the adult beetles eclose. The young adult beetles then apparently emigrate, as indicated by a short phase of high diurnal locomotory and flight activity. After this period the beetles hunt the ants near the Lasius fuliginosus nest during the night, while remaining hidden in convenient shelters during the day. The Pella adults overwinter in dormancy inside the Lasius nest. At the end of the winter they enter a second diurnal activity phase during which mating takes place. After reproduction the beetles die, normally a few weeks before the new adult beetle generation ecloses in June.

The larvae of Pella funesta are as closely associated with the ants as the adults. They are found almost exclusively near or in the kitchen middens of the Lasius fuliginosus nest, where they subsist primarily on dead ants. While feeding, the larvae always attempt to stay out of sight, either by remaining entirely beneath the booty and devouring it from below, or by crawling inside the bodies of their victims. Occasionally two to four larvae feast on the same corpse. When the beetles become overly crowded, however, they attack and cannibalize each other (Figure 13-9).

When ants encounter the Pella larvae they usually attack them. Almost invariably the larvae raise their abdominal tips towards the heads of the ants in a defensive maneuver. Pella larvae possess a complex tergal gland near the abdominal tip, which may secrete appeasement or diversion substances. At least the ants respond to the movement by stopping their attack and palpating the abdominal tip of the larva. In most cases this brief interruption is sufficient to allow the larva to escape. In general, Pella larvae are able to come into close contact with workers of Lasius fuliginosus without being attacked, and this is especially the case when the temperature is relatively low (14-17°C). Under these circumstances larvae have been observed licking the cuticle of live ants, including even the mandibles and mouthparts. Tracer experiments with radioactive labeled food did not, however, indicate that the larvae are able to solicit regurgitation from the ants. Their main food source seems to be dead ants and nest debris. They can easily be raised in the laboratory entirely apart from living ants, provided they are given a regular diet of freshly killed ants. The genus Pella was originally combined with Zyras and Myrmedon, but raised to full generic rank by Kistner (1972). Wasmann (1886, 1920, 1925, 1930) reported that all species he had studied, including cognata, funesta, humeralis, laticollis, lugens, and similis, live with Lasius fuliginosus. Of these, only 'humeralis uses alternate hosts, in this case species of the Formica rufa'' group. According to Wasmann all Pella species prey on ants, concentrating especially on disabled adults. In addition Wasmann observed that the beetles are active primarily during the night. In a more recent study Kolbe (1971) failed to find predatory behavior in P. humeralis and concluded that this species primarily feeds on dead ants. Similar observations were made with Pella japonicus, which lives with Lasius spathepus (Yasumatsu, 1937; Kistner, 1972). Kistner also observed that these beetles “ate small insects that are being transported by the ants.” However, he could not see the Pella eating live ants or fighting any of the ants on the trail. Hölldobler et al. (1981) confirmed that adult Pella funesta, Pella laticollis and P. humeralis live as scavengers, feeding on dead or disabled ants and debris discarded by the ants. However, they also observed that these beetles, in concert with Wasmann's claim, act as very effective predators on the ants. In the field and laboratory Pella beetles were seen hunting Lasius fuliginosus. The beetles chased after individual ants and pursued them for distances of up to six centimeters. When a beetle made a rear approach, it attempted to mount the ant and insert its head between the victim's head and thorax (Figure 13-7). When attacked the ant usually reacted by stopping abruptly and pressing the femurs rapidly and tightly against its body. Often this reaction threw the beetle off the back of the ant, allowing the ant to escape. Of 178 beetle onslaughts on Lasius fuliginosus workers observed during a period of 3 hours, only nine were successful. The beetles partially decapitated their victims, at least to the extent of severing their esophagus and nerve cord. Occasionally two or three beetles were seen chasing an ant. Once the ant was caught by a beetle the other beetles joined in subduing and killing it. Although individual Pella often tried to drag the prey away from the others, all the members of the pack usually ended up feeding on it simultaneously. No aggression among the beetles was observed on such occasions. When the beetles were starved for several days, they occasionally chased each other, even jumping on one another's backs, but they never engaged in cannibalism.

When foraging on the ants' garbage dumps or running along the ants' trails, Pella adults frequently encounter ants and are attacked by them. How do the beetles manage to escape their aggressive hosts? Usually they run around with their abdomens curved slightly upwards. When encountering an ant, the beetles flex the abdomen even more strongly. This is a typical and frequently described behavior of many staphylinid myrmecophiles and is commonly considered a defensive response. It has been suggested that during abdominal flexing the beetles discharge secretions from their tergal gland (Jordan, 1913; Kistner and Blum, 1971). The gland is located between the sixth and seventh abdominal tergites and is unique to the subfamily Aleocharinae, to which most myrmecophilous and termitophilous staphylinids belong (Jordan, 1913; Pasteels, 1968). The chemical composition of the tergal gland secretions of several species has been investigated and found to be extraordinarily diverse (Blum et al., 1971; Brand et al., 1973a; Kolbe and Proske, 1973; Hölldobler et al., 1981). Kistner and Blum (1971) suggested that Pella japonicus and possibly also Pella comes, both of which live with Lasius spathepus, produce citronellal in their tergal glands. This substance is also a major compound of the mandibular gland secretions produced by the host ants, for which it functions as an alarm pheromone. Pella japonicus tergal gland contents have not yet been chemically identified. Because irritated beetles seemed to smell like the ants' mandibular gland secretions, Kistner and Blum speculated that Pella japonicus produce citronellal in the tergal glands and thereby mimic the alarm pheromone of their host ants. They suggested that in this way the beetles can “cause the ants to reverse their direction, a reaction which allows the myrmecophiles to escape.” However, the investigations by Hölldobler et al. (1981) of the defensive strategy employed by the European Pella towards their host ants Lasius fuliginosus lead to a different interpretation. When irritated mechanically, Pella laticollis discharges a pungent brownish secretion from its tergal gland. A chemical analysis of the secretions did not reveal any resemblances to the mandibular gland secretions of the host ants. Furthermore, the beetles never employed the tergal gland secretions when they were attacking ants. They did so only when severely attacked themselves--and in particular when the ants seized their appendages. Ants contaminated with tergal gland secretions in these episodes usually displayed an aversive reaction, releasing the grip on the beetles and grooming and wiping their mouthparts and antennae on the substrate. But the beetles then had to escape quickly, because other ants nearby became alerted and rapidly converged on the scene, apparently in response to the alarm pheromones of their nestmates.

Although Hölldobler and his collaborators could not find any resemblance of the bulk of Pella tergal gland secretions to the mandibular gland secretions of Lasius fuliginosus, it is noteworthy that the Pella secretions did contain undecane, a hydrocarbon commonly found in the Dufour's glands of formicine ants and considered to be an alarm pheromone in Lasius fuliginosus (Dumpert, 1972). Even with this element, however, isolated tergal gland contents of P. laticollis elicited a repellent reaction rather than an alarm response in Lasius fuliginosus. Apparently the repellent effect of the quinones, the major components of the tergal gland secretions, is stronger than the attractant effect of undecane. When the ants' antennae were directly contaminated with the beetles' tergal gland secretions, they hung almost motionless, and the ants were disoriented for several minutes. Hence it is unlikely that the beetle uses its powerful repellent defensive system each time it makes a “routine” encounter with its host ants. Hölldobler and his co-workers concluded that in such situations the beetles rely on an appeasing or diverting defensive strategy, with the repellent defense being employed only as a last resort.

In early spring, when most of the Pella adults are close to the entrance of the ants' nest, they feign death when attacked by ants. The ants then either ignore the motionless beetles or carry them around and finally discard them on the refuse piles. Later in the season, when the activity of ants and beetles is much higher, the beetles employ a different appeasement technique. Each time they encounter ants they flex their abdomen forward and point the abdominal tip toward the head of their adversaries. Usually the ants respond by antennating the tip and licking it briefly (Figure 13-10). This ordinarily damps the ants' aggressions, allowing the beetle to escape. When on occasion the ants become persistent, the beetle extrudes a white, viscous droplet from the abdominal tip, which the ants eagerly lick up. Histological investigations revealed the abdominal tips of Pella to contain exocrine glandular structures, which Hölldobler has called the “appeasement gland” complex. It is not yet possible to assign one specific gland to the appeasement function.

Kitchen middens and peripheral nest chambers. We have described the genus Pella in some detail as representative of an early evolutionary grade in the myrmecophilous evolution of the aleocharine staphylinids. Species of Pella are specialized predators and scavengers, but they are less advanced in their myrmecophilic relationships than aleocharine species specialized on the kitchen middens, peripheral nest chambers, and brood chambers of the host ants' nests. A representative of the latter, more advanced evolutionary grade is Dinarda. The myrmecophilous habits of this genus have been known since Wasmann's first account published in 1894, and the genus has since been recorded with many species of Formica (Bernard, 1968). Kistner (1982) points out that the species-level taxonomy is still in poor condition, so that the best studied form, Dinarda dentata, might in fact comprise several species. The following account is based mostly on the form (or species) of Dinarda dentata that lives in nests of the red slavemaking ant Formica sanguinea of Europe (Figure 13-11).

The larvae of Dinarda are concentrated in the kitchen middens of the Formica hosts, where they feed on dead ants and debris. When they encounter worker ants they exhibit the same appeasingly defensive behavior described for Pella larvae (Figure 13-12). Not surprisingly, they also possess a similar complex glandular structure in the tip of their abdomens. Some adult Dinarda beetles are found in the kitchen middens, where they exist as scavengers. Most, however, patrol through the peripheral nest chambers, where they feed on arthropod prey brought in by the host workers. Wasmann (1894) reported that Dinarda also eats mites and occasionally even ant eggs and larvae.

Finally, studies of laboratory colonies have revealed that Dinarda taps into the liquid food flow of its hosts (Hölldobler, 1971a, 1973c). This parasitism occurs mostly in the peripheral chambers of the nest, where the bulk of regurgitation occurs between newly returning foragers and nest workers. The Dinarda beetles sometimes insinuate themselves between two workers exchanging food and literally snatch the droplet of food from the donor's mouth. They also use a simple begging behavior in order to obtain food directly from the returning foragers. The beetle approaches an ant and furtively touches its labium, causing the ant to regurgitate a small droplet of food (Figure 13-13). The ant, however, soon recognizes the beetle as an alien and commences to attack it. At the first sign of hostility the beetle raises its abdomen and offers the ant the appeasement secretions at the abdominal tip. The abdominal tip is quickly licked by the ant, and almost instantly the attack ceases. During this brief interlude the beetle makes its escape. Dinarda also possesses a well-developed tergal gland, but its repellent secretions are applied only as a last resort against ant attacks.

It is noteworthy that a myrmecophile belonging to a radically different taxonomic group obtains food in a similar manner to Dinarda. Janet (1896) discovered that the thysanuran Atelura formicaria, which is a very common symbiont of many European ant genera (Bernard, 1968), occasionally snatches food during food exchanges between worker ants. Like the Dinarda beetles, Atelura favors the peripheral chambers of the host nests.

Another example of a myrmecophile adapted especially to kitchen middens and peripheral nest chambers is the histerid beetle genus Hetaerius (Figure 13-14). As Wasmann (1886, 1905) first reported, the European species Hetaerius ferrugineus is most frequently found in nests of Formica fusca, where it feeds on dead and wounded ants. Occasionally it also consumes ant larvae and pupae. Most of the time the ants pay no attention to the Hetaerius. When they do attack an adult, the beetle exhibits death-feigning behavior by holding perfectly still with its legs closely appressed to its body. The ants frequently react to this nonviolent resistance by carrying the beetle around, licking it and finally releasing it. It has been suggested that Hetaerius has special trichome glands opening on the margins of the thorax (Escherich and Emery, 1897; Wasmann, 1903; Wheeler, 1908c). However, no histological investigations have been performed to confirm this assumption.

Wheeler (1908c) observed that adults of the North American Hetaerius brunneipennis solicit regurgitated food from the host ants. The beetle sometimes waves its forelegs toward passing ants, and by this action appears to attract their attention. A very similar behavior has been more recently recorded in H. ferrugineus. The soliciting beetle takes an upright position, stretching its forelegs widely apart and waving them slightly towards the approaching ant. The ant antennates and licks the beetle with her mandibles usually held relatively closed (Figure 13-15). Tracer experiments have revealed that the beetle also obtains small amounts of regurgitated food (Hölldobler, unpublished results). Thus, contrary to a suggestion originally made by Wheeler, Hetaerius brunneipennis does not represent a more advanced evolutionary state over H. ferrugineus (where food solicitation was previously unknown).

Brood chambers. The brood chambers constitute the optimal niche within an ant nest for a social food-flow parasite, because there the food of the highest quality is concentrated to be fed to the developing larvae, callow workers and queen(s). Moreover, the immature ant stages housed in the brood chambers provide the most valuable prey for specialized ant predators. The brood chambers are nevertheless difficult for parasites to penetrate, because they are fiercely defended by the ants. Very special adaptations are thus needed for myrmecophiles to exploit these sites as an ecological niche. This has been accomplished by some of the evolutionarily most advanced myrmecophilous staphylinids, of which the aleocharine beetles Lomechusa strumosa and several species of the genus Atemeles are the premier examples.

Lomechusa (Figure 13-16) lives with Formica sanguinea in Europe. Atemeles pubicollis (Figure 13-16), also a European species, is normally found with the mound-building wood ant Formica polyctena during the summer. But in the winter it inhabits the nests of ants of the myrmicine genus Myrmica. We know from the observations of Wasmann of more than 70 years ago that these beetles are both fed and reared by their host ants. The behavioral patterns of the larvae of these beetles are similar for Lomechusa and the various Atemeles species; in particular the larvae prey to a certain extent on their host ants' larvae. It is therefore astonishing that nurse ants not only tolerate these predators but also feed and protect them as readily as they do their own brood (Figure 13-17).

Hölldobler (1967a,b) demonstrated that the interspecific communication is both chemical and mechanical in nature. The beetle larvae show a characteristic begging behavior toward their host ants. As soon as they are touched by an ant, they rear upward and try to make contact with the ant's head. If they succeed, they tap the ant's labium with their own mouthparts. This apparently releases regurgitation of food by the ants. The ant larvae beg for food in much the same way but usually less intensively than the beetle parasites. With the aid of experiments using food mixed with radioactive sodium phosphate it has been possible to measure the social exchange of food in a colony. The results show that myrmecophilous beetle larvae present in the brood chamber obtain a proportionately greater share of the food than do the host ant larvae. The presence of ant larvae does not effect the food flow to the beetle larvae, whereas ant larvae always receive less food when they compete with beetle larvae. This disparity suggests that the releasing signals presented by the beetle larvae to the nurse ants may be more effective than those presented by the ant larvae themselves.

The Lomechusa and Atemeles larvae are also frequently and intensively groomed by the brood-keeping ants. Thus it appears probable that chemical signals are also involved in the interspecific relationship. The transfer of substances from the larvae to the ants was detected with the aid of radioactive tracers. These substances are probably secreted by glandular cells that occur beneath the integument of the dorsolateral area of each segment. The biological significance of the secretions was elucidated by the following experiments. Beetle larvae were first completely covered with shellac to prevent the release of the secretion. They were then placed outside the nest entrance, together with freshly killed but otherwise untreated control larvae. The ants quickly carried the control animals into the brood chamber. The shellac-covered larvae, on the other hand, were either ignored or carried to the garbage dump. It was found that for adoption to be successful, at least one segment of the larva must be free of shellac. Furthermore, after all the secretions have been extracted with solvents, the larvae are no longer attractive. When the extracted larvae are then contaminated with secretions from normal larvae, they regain their attractiveness. Even filter paper dummies soaked in the extract are carried into the brood chambers.

To summarize, the experiments show that the adoption of the Lomechusa and Atemeles larvae and their care within the ant colony depend on chemical signals. It may be that the beetle larvae imitate a pheromone which the ant larvae themselves use to release brood-tending behavior in the adult ants. This inference is supported by the fact that the beetle larvae and host ant larvae can be transplanted from the host species to closely related Formica species. But the ant species that do not accept the larvae of the ant hosts also reject the beetle larvae.

The question next arises as to how the ant colony manages to survive the intensive predation and food parasitism by the beetle larvae. The answer appears to be very simple. The beetle larvae are cannibalistic, and this factor alone appears to be effective in limiting the number of beetle larvae in the brood chambers at any time.

The larvae of both genera pupate in the summer, and they eclose as adult beetles at the beginning of autumn. The young Lomechusa adults leave the ant nest and after a short period of migration seek adoption in another nest of the same host ant species. Atemeles adults, on the other hand, emigrate from the Formica nest, where they have been raised, to nests of the ant genus Myrmica. They winter inside the Myrmica brood chambers and in the springtime return to a Formica nest to breed (Wasmann, 1910a; Hölldobler, 1970b). The fact that the adult beetle is tolerated and is fed in the nest of ants belonging to two different subfamilies suggests that it is able to communicate efficiently in two different “languages.”

The Atemeles face a major problem in finding their way from one host species to another. Formica polyctena nests normally occur in woodland, while those of Myrmica are found in grassland around the woods. Experiments have revealed that when Atemeles leave the Formica nest they show high locomotor and flight activity and orient toward light. This may well explain how they manage to reach the relatively open Myrmica habitat. Once they reach the grassland, the beetles must distinguish the Myrmica ants from among the other species present and locate their nests. Choice experiments in the laboratory have revealed that they identify the Myrmica nests innately by specific odors. Windborne species-specific odors are equally important in the springtime movement back to Formica nests.

Having found the hosts, the beetles must then secure their own adoption. The process comprises the four sequential steps depicted in Figure 13-18. First, the beetle taps the ant lightly with its antennae and raises the tip of the abdomen toward it. The latter structure contains the appeasement glands, the secretions of which are immediately licked up by the ant and appear to suppress aggressive behavior. The ant is then attracted by a second series of glands along the lateral margins of the abdomen. The beetle lowers its abdomen in order to permit the ant to approach this part of its body. The glandular openings are surrounded by bristles, which are grasped by the ant and used to carry the beetle into the brood chambers. By experimentally occluding the openings of the glands, Hölldobler found that their secretion is essential for successful adoption. For this reason he called them “adoption glands.” Thus, the adoption of the adult beetle, like that of the larva, depends on chemical communication, and it most probably entails an imitation of specific brood pheromones (Hölldobler, 1970b).

Before leaving the Formica nest the Atemeles beetle must obtain enough food to enable it to survive the trek to the Myrmica nest. This it obtains by vigorous solicitation from its hosts. The begging behavior is essentially the same toward both Formica and Myrmica (Figure 13-19; see also Figure 7-41). The beetle attracts the ant's attention by rapidly drumming on it with its antennae. Using its maxillae and forelegs it taps the mouthparts of the ant, thus inducing regurgitation. As noted previously, the ants themselves employ a similar mechanical stimulation of the mouthparts to obtain food from one another. It is thus clear that Atemeles is able to obtain food by imitating these very basic tactile food-begging signals.

What is the significance of the seasonal changes in hosts in Atemeles? There are good reasons for believing that Atemeles first evolved myrmecophilic relationships with Formica rather than with Myrmica. It seems likely that the ancestral Atemeles beetles hatched in Formica nests in the autumn and then dispersed, returning to other Formica nests only to overwinter. This simpler life cycle is followed by Lomechusa today (Wasmann, 1915b; Hölldobler, 1972). However, in the Formica nest the immature stages disappear during the winter, and consequently social food flow is reduced. In contrast, the Myrmica colony maintains brood throughout the winter. Thus, in Myrmica nests, larvae and nutrients from the social food flow are both available as high-grade food sources to the myrmecophiles. These circumstances, coupled with the fact that the beetles are sexually immature when they hatch, suggest why it is advantageous for the beetle to overwinter in Myrmica nests. While there the Atemeles complete gametogenesis, so that when spring comes the beetles are sexually mature. They then return to the Formica nest to mate and lay their eggs. At this time the Formica are just beginning to raise their own larvae and the social food flow is again maximized. The life cycle and behavior of Atemeles is thus synchronized with that of its host ants in such a manner as to take greatest advantage of the social life of each of the two species in turn.

The North American staphylinid myrmecophiles of Xenodusa seem to have a similar life history as Atemeles. The larvae are found in Formica nests and the adults overwinter in the nests of the carpenter ants of the genus Camponotus (Wheeler, 1911). It is undoubtedly significant that Camponotus, like Myrmica, maintains larvae throughout the winter. It may well be that the host-changing behavior of Xenodusa has the same significance as that inferred for Atemeles.

Wasmann considered Lomechusa strumosa to be the most evolutionarily advanced of the myrmecophilous staphylinids. We agree with this assessment, which is supported by a more recent analysis of the myrmecophilous behavior of Lomechusa (Hölldobler, 1971a, and unpublished results). Lomechusa also appears to have at least one migratory phase in spring, when, shortly after overwintering as an adult inside the Formica sanguinea nest, it travels to another nest of the same host species, where mating takes place (Figure 13-20). The adoption procedure into the new host ants' nest is even more complicated than that of Atemeles.

Like other aleocharine myrmecophiles, Lomechusa is equipped with well-developed tergal glands that produce defensive substances. The secretion consists of benzoquinone, methyl-benzoquinone, ethyl-benzoquinone and n-tridecane, with the latter compound accounting for more than 80 percent of the volatiles (Blum et al., 1971). This powerful repellent mixture, however, is normally employed only when the beetle is attacked by non-host ants. When approached by host ants Lomechusa behaves much more gently. It first presents the trichome structures on its legs, particularly the femora. The beetle then slowly circles around on the spot, with its legs widely extended so that the femoral trichomes are easily accessible. Simultaneously the beetle antennates the ants, bending its body sideways or backwards in order to reach the ants with its antennae. Next it slowly points its abdominal tip at the ants. Lomechusa possesses a battery of exocrine glands at the abdominal tip, and during the early adoption phase it frequently extrudes a whitish, viscous droplet which is eagerly licked up by the ants. The secretion is proteinaceous and contains no appreciable amounts of carbohydrates. The ants that feed on the material seem to grow calmer in the process. The Lomechusa now permit the ants access to trichomes along the lateral margins of the abdomen that project above the adoption glands. The ants lick and grasp the trichome bristles and finally carry or drag the beetle into the brood chambers of their nests. Inside the nest the Lomechusa continues to be tended by its host ants, despite the fact that it preys on the ants' brood (Figure 13-21). In addition the adult Lomechusa, like the larva, receives food directly from the nurse ants. Its soliciting behavior is markedly different from that of adult Atemeles. Lomechusa possess trichomes at the labrum, which are frequently licked by the ants. During this procedure the beetle uses its maxillae to stimulate the mouthparts of the ants, an action that seems to elicit the regurgitation of liquid food. In contrast to Atemeles, however, Lomechusa does not use its forelegs when begging for food. One gets the impression, as Wasmann first suggested, that the ants' feeding behavior toward adult Lomechusa resembles more the nursing behavior toward ant larvae than the trophallactic food exchange between adult ants. It is possible, but not yet proved, that Lomechusa is fed primarily with high-grade secretions from the postpharyngeal and labial glands of nurse workers--in other words, the same food given the larvae.

In short, Lomechusa strumosa presents its host ants with a complex variety of chemical signals, including imitations of brood-tending pheromones and other kinds of pseudopheromones. The species is thereby superbly well adapted to live with Formica sanguinea, especially in the brood chambers where it finds both food and a protected and regulated environment.

Most of the more casual observations of regurgitation between host and symbionts suggest that the exchange is exploitative, meaning that the liquid flows exclusively from the host to the symbiont. Experiments with radioactive tracers have proved this to be the case for the larvae and adults of Atemeles and Lomechusa (Hölldobler, 1967a,b, 1970b, and unpublished data). However, an exception has been reported in the case of Amorphocephalus coronatus. Adults of this brenthid beetle live with Camponotus in southern Europe (Figure 13-22). According to Le Masne and Torossian (1965) they receive food from some of the host workers and regurgitate part of it back to other host workers. This is the first reported example that could be construed as altruistic behavior on part of the symbiont beetles (Wilson, 1971). However, quantitative investigations are needed to see how much of the received food the beetle shares with other host ants. It could very well be that Amorphocephalus returns only very small portions of the food to the colony and that this “pseudo altruistic” behavior is one other mechanism of a symbiont to become fully integrated into the host colony.

Other adaptations of predators in the ants' brood chambers. Entomologists generally agree that a select few of the aleocharine staphylinids, including Atemeles and Lomechusa, have reached the evolutionary pinnacle of myrmecophilous adaptations. In mimicking the ants' important communication signals they are able to integrate themselves into the ant societies and exploit the hosts' brood chambers. There nevertheless exists a diversity of other arthropods that also preys on ant brood but uses a very different set of sophisticated techniques to invade the ants' nests. An especially instructive example is provided by the scarabaeid beetle genus Cremastocheilus (Figure 13-23).

Cremastocheilus is a North American genus comprising about 50 species (Krikken, 1976), various of which have been studied by Wheeler (1908b), Cazier and Mortenson (1965), Alpert and Ritcher (1975), and Kloft et al. (1979). Most recently Alpert (1981) has provided an insightful review of the ecology, behavior and evolution of the genus.

Various species of Cremastocheilus, the greatest number of which are found in the deserts of the southwestern United States and Mexico, use the formicine ants Formica, Myrmecocystus, Lasius and Camponotus, and the myrmicines Pogonomyrmex, Veromessor and Aphaenogaster as hosts. Ant nests in this arid area provide a high concentration of food resources and a refuge from predators and severe climatic change. Cremastocheilus larvae, like other scarabaeid larvae, feed primarily on decaying vegetable material. They develop within piles of vegetable matter inside ant nests, despite the apparent lack of any morphological adaptations for defense from their hosts. Alpert's field observations revealed few interactions between beetle larvae and ants. Experiments showed that the larvae are generally ignored by ant workers, while unrelated scarabaeid larvae of similar size used as controls were attacked immediately. Only highly excited ants were observed to attack Cremastocheilus larvae, which then defended themselves with powerful “mandibular strikes” and escape maneuvers. Alpert concluded that while Cremastocheilus larvae are not nutritionally dependent on ants (they can be raised in complete isolation), they gain protection from predators and desiccation simply by virtue of their residency in ant nests.

Cazier and Statham (1962) suggested that the adult beetles are first brought into the ant nests as booty by the foraging ants. The beetles, however, are so well protected by their heavily sclerotized cuticle that the ants are unable to kill them. Once inside the nest, the beetles themselves prey on the ant larvae (Cazier and Mortenson, 1965). This scenario has been basically confirmed by Alpert's (1981) field and laboratory observations. Although Cremastocheilus adults are capable of feeding on any species of ant larvae, only one or a few ant species are selected as hosts under natural conditions. This specificity appears to be a product of the host-searching process.

It was originally believed that secretions from glandular trichomes, located on prominent pronotal angles in all species of Cremastocheilus, attracted ants to beetles outside the nest and induced adoption (Cazier and Mortenson, 1965); but experiments conducted by Alpert did not confirm this assumption. Alpert released dead Cremastocheilus and other scarabaeid beetles with live C. stathamae near Myrmecocystus colonies. There was no significant preference by the ants for live C. stathamae, suggesting that special exocrine gland secretions are not involved in the adoption of the beetles by their ant hosts. Nor did glandular extracts elicit special attraction on the part of the ants. All the evidence supports the hypothesis that certain Cremastocheilus species are mistaken for prey items and thereby gain access to the nest. In fact, Cremastocheilus beetles commonly feign death when approached by ants, retracting their antennae into protective grooves and sticking out their heavily sclerotized legs. While some species gain entry into the host ants' nest by mimicking prey items, other species are able to march directly through the nest entrance or burrow through thatch piles into the interior. Often the beetles are attacked by ants inside the nest. Occasionally they are forcibly ejected, only to be carried in again by other ants. Attacks usually persist for several minutes, until the ants give up and the Cremastocheilus move to concealed corners in chambers or passageways. In the end the beetles move slowly toward the brood chambers, where they are completely ignored by the ants. Alpert reports “when the adult beetles (C. stathamae) approached ant brood, or while beetles were feeding, the host ants clearly licked the surface of the beetle. Although pronotal angles were specifically licked, most of the dorsal surface of the beetles was also involved.” Similar observations were made on other Cremastocheilus species. Alpert concludes that while adults of Cremastocheilus feed on ant brood, trichome secretions may distract workers, reduce aggression, and prevent workers from evacuating brood, while other glands serve to absorb colony odors.

Kloft et al. (1979) proposed that secretions from trichomes at the prosternal apophysis are sought by Camponotus castaneus and evoke food sharing behavior in the ants. They claimed that by transferring Cremastocheilus trichome substances to other workers, the entire colony could be appeased. In addition they suggested that the enlarged and projecting propygidial spiracles are glandular and “a possible source of secretions” attractive to the ants. By carefully sectioning Camponotus castaneus and members representing most of the other species groups, Alpert (1981) has shown that this conclusion is incorrect. The prosternal apophysis and propygidial spiracles are not glandular in the genus Cremastocheilus. Alpert nevertheless did find many new areas that bear exocrine glands. In a series of experiments with radioactive tracers, he further discounted the claim by Kloft et al. (1979) that trophallaxis occurs between host ants and Cremastocheilus. Furthermore, he was unable to find evidence of a “peace making” allomone transferred from trichomes to the colony.

Entomologists continue to be intrigued by the possible evolutionary pathways that led to the specialized predaceous behavior of Cremastocheilus. One hypothesis is that Cremastocheilus has changed from what was almost certainly a herbivorous diet to become a fully carnivorous scarabaeid (Wilson, 1971; Kistner, 1982). This route might have started with the adaptation of larvae for development in ant nests. In typical scarabaeid fashion Cremastocheilus larvae eat vegetable matter in the soil, and because of the concentration of vegetation in ant nests and protection from predators, ant colonies became the new oviposition site. Such behavior is known in cetonine scarabaeids, such as Euphoria inda, which develops in Formica obscuripes nests in North America (Windsor, 1964), and the European species Cetonia curprea, the larvae of which also develop in Formica nests (Donisthorpe, 1927). Alpert (1981), on the other hand, argues that the adults of Ephoria and Cetonia are not preadapted for survival in ant colonies and did not evolve in this direction. Cremastocheilus adults, in contrast, have many morphological adaptations for integration into ant nests and an examination of other genera of Cremastocheilini gives the best understanding of how the genus Cremastocheilus might have evolved. In Alpert's view, “The tribe Cremastocheilini reflects an evolutionary route from adult predation on soft bodied insects to specialized feeding on ant brood and subsequent development of larvae in ant colonies.” The Indian cremastocheiline Spilophorus maculatus, in fact, is a predator on membracids and lives independently of ant colonies (Ghorpade, 1975). Genuchinus ineptus develops in plants of the liliaeceous genus Dasylirion of Mexico and the southwestern United States, and any association with ants is entirely accidental. The adults are general predators, feeding on many different soft bodied insects in the laboratory. Dasylirion plants are inundated with fly larvae, the most probable source of food for Genuchinus ineptus in the field. Genuchinus ineptus, in this interpretation, is preadapted for myrmecophilous existence as a predator on ant brood. The predaceous mouthparts of Genuchinus ineptus adults are almost identical to those of Cremastocheilus. There are other morphological features common to Genuchinus and Cremastocheilus which are apparently adaptations for predation. These include the flattened body shape, hard, pockmarked integument, retractable antennae, and protective mentum. The larvae of Genuchinus ineptus develops in leaf compost of Dasylirion plants, and the pupae are sheltered by protective cases. The Genuchinus differ from Cremastocheilus by remaining inside their cases until spring.