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.