G Guests of Social Insects resources and homeostatic conditions. At the same time, successful adaptation to the inner envi- Thomas Parmentier ronment shields them from many predators that Terrestrial Ecology Unit (TEREC), Department of cannot penetrate this hostile space. Social insect Biology, Ghent University, Ghent, Belgium associates are generally known as their guests Laboratory of Socioecology and Socioevolution, or inquilines (Lat. inquilinus: tenant, lodger). KU Leuven, Leuven, Belgium Most such guests live permanently in the host’s Research Unit of Environmental and nest, while some also spend a part of their life Evolutionary Biology, Namur Institute of cycle outside of it. Guests are typically arthropods Complex Systems, and Institute of Life, Earth, associated with one of the four groups of eusocial and the Environment, University of Namur, insects. They are referred to as myrmecophiles Namur, Belgium or ant guests, termitophiles, melittophiles or bee guests, and sphecophiles or wasp guests. The term “myrmecophile” can also be used in a broad sense Synonyms to characterize any organism that depends on ants, including some bacteria, fungi, plants, aphids, Inquilines; Myrmecophiles; Nest parasites; and even birds. It is used here in the narrow Symbionts; Termitophiles sense of arthropods that associated closely with ant nests. Social insect nests may also be parasit- Social insect nests provide a rich microhabitat, ized by other social insects, commonly known as often lavishly endowed with long-lasting social parasites. Although some strategies (mainly resources, such as brood, retrieved or cultivated chemical deception) are similar, the guests of food, and nutrient-rich refuse. Moreover, nest social insects and social parasites greatly differ temperature and humidity are often strictly regu- in terms of their biology, host interaction, host lated. The precious nest spaces are commonly distribution, behavior, and diversity. In contrast closely defended by a multitude of workers to the mutualistic trophobionts, like some aphids equipped with strong mandibles, venom, and/or and other homopterans, guests do not provide a battery of other chemical weapons. The nest is clear benefits to their host but range from com- therefore to be regarded as a resource-rich but mensals to severe parasites. impregnable fortress. The founding father of the study of this A remarkably diverse group of arthropods remarkable group was Erich Wasmann other than the resident social insects thrives in (1859–1931) of Austria, who collected and just such a situation, exploiting the nest’s described hundreds of social insect guests, as © Springer Nature Switzerland AG 2020 C. Starr (ed.), Encyclopedia of Social Insects, https://doi.org/10.1007/978-3-319-90306-4_164-1 2 Guests of Social Insects well as writing extensively about their relation- physical or behavioral) seem to be preadapted in ships to their hosts [11]. Other important this way. Mites and beetles form the largest groups pioneering scholars were Charles Janet, William of guests. The majority of beetle guests are M. Wheeler, and Horace Donisthorpe. They were rove beetles (Staphylinidae), particularly of followed by a number of influential researchers in the subfamilies Aleocharinae and Pselaphinae. the second half of the twentieth century, most Other species-rich groups are flies (especially notably David H. Kistner [4, 5], Bert Hölldobler the Phoridae), parasitic wasps, silverfish, and [1], and Carl Rettenmeyer [9]. the beetle families Carabidae, Scarabaeidae, The greatest diversity of guests is found in Tenebrionidae, and Histeridae [5, 7]. nests of ants and termites. The number of myrme- The fossil record hints that the intricate cophile species is estimated at between 10 and 100 relationship between guests and social insects thousand, but no catalogs have been compiled in has developed early in the radiation of social recent times. In comparison, social bees and social insects and has been sustained over geological wasps support a relatively low number of guests. time. The oldest unequivocal termitophile is an This difference is evidently not due solely to the aleocharine beetle from 99-million-year-old sizes of the potential host groups, as several fac- amber. Recently, a clown beetle preserved in tors promote diversity and coexistence of symbi- amber of the same period was described as the onts found in ants and termites, but not in bees and earliest myrmecophile fossil. wasps. The largest diversity of guests lives in very Wasmann already recognized that social large ant or termite colonies peaking at millions of insect guests greatly differed in their strategies workers, much larger than those of any social bees to bypass host vigilance. He placed guests in or wasp. In addition, the density of ant and termite different categories according to degree of spe- nests per unit area is often much higher, and these cialization [11]. Synechtrans (persecuted guests) nests are stable and of long duration. Furthermore, are unspecialized inquilines that are recognized as ant and termite nests typically contain much more intruders and provoke an aggressive response. organic material and debris which attract scaven- They can survive by means of hiding, swift move- gers. Finally, ant and termites probably defend ments, repellent secretions, or mechanical defen- their nest less efficiently. In spite of the low num- sive structures. Synoeketes (indifferently tolerated ber of bee guests, they gain much attention guests) are also relatively unspecialized but are because of their destructive effect on commercial ignored because of their slow movement, small apiculture. The most notorious bee guests are size, lack of protruding appendages, or an appar- Varroa mites, but the small hive beetle (Aethina ently indistinct odor. Symphiles (true guests) are tumida) and wax moths are also considered as highly specialized inquilines that have evolved serious parasites of honey bees. different types of chemical, morphological, and behavioral adaptations that deceive the host. Because of this trickery, they are not attacked Evolution but are accepted as members of the colony. They are rewarded with food, grooming, protection, The transition from free-living organism to inqui- and transport. These arthropods have succeeded line in social insect nests has evolved in many in “breaking the code” of their hosts. The last terrestrial arthropod lineages [2, 4, 5]. Guests group of guests in Wasmann’s classification come from multiple insect orders, as well as in is ectoparasites which live on the body of their spiders, mites, isopods, pseudoscorpions, and mil- host. lipedes. Nevertheless, inquilinism is heavily Kistner devised an alternative classification skewed to particular groups of arthropods that with only two categories, non-integrated and appear preadapted to a shift toward this peculiar integrated species [4] that is now preferred. habit. Small scavenging or predatory arthropods The group of non-integrated species roughly with some sorts of defensive features (chemical, encompasses Wasmann’s synoeketes and Guests of Social Insects 3 synechtrans, as well as most ectoparasites, response to danger, allocation of food sources, whereas the category of integrated species is and distribution of fertility and dominance sig- almost equivalent to Wasmann’s symphiles. nals. Chemical cues are also pivotal in ▶ nestmate While these and other classifications have recognition, which is based on a colony-specific their merits, they leave out the fact that the blend of low-volatile cues present on the cuticle. degree of specialization in guests is continuous, In ants, wasps, and termites, the colony odor is so that the proposed categories are situated at a bouquet of linear ▶ cuticular hydrocarbons, the extremes of the generalist-specialist spectrum. whereas other compounds such as fatty acids Many guests thus do not fit into the distinct and esters are important in bees as well. Workers categories of these classifications. For example, treat individuals with the same odor as members the rove beetle Dinarda maerkelii is recognized of the colony and reject or attack individuals with by its Formica ant host and provokes a a deviating chemical profile [10]. A large group strong aggression response. On the other hand, of arthropods has succeeded in exploiting this it frequently begs for food and engages in sophisticated communication system [6]. The ▶ trophallaxis, a highly specialized behavior same chemical deception strategies can be found typically seen in symphiles. in social insect guests and in ▶ social parasites. The mimicking of the host’s chemical profile may result in complete acceptance into the colony [2]. Strategies It appears that highly specialized guests with a narrow host range can synthesize the components In the course of adapting to life in social prior to the contact with their host (chemical mim- insect nests, guests have evolved specialization icry), but this strategy is rather rare. Other guests, in different traits. Surprisingly, different arthropod such as the infamous Varroa mites, acquire the lineages often evolved independently the same colony odor passively by transfer of components strategies to facilitate integration into the colony. from the host (chemical camouflage). This strat- As a general rule, an associate that shows an egy is more flexible, as it allows the exploitation intimate relationship with its hosts will capitalize of hosts with different profiles. Associates gain on advanced integration strategies,