sign in sign up
<<
Home , Amphotis, Anoplolepis, Ant cricket, Attaphila, Braula, Braulidae

G

Guests of Social 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 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 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 guests, termitophiles, melittophiles or bee guests, and sphecophiles or guests. The term “myrmecophile” can also be used in a broad sense Synonyms to characterize any that depends on , including some bacteria, fungi, plants, aphids, Inquilines; Myrmecophiles; Nest parasites; and even . 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. and form the largest groups pioneering scholars were Charles Janet, William of guests. The majority of guests are M. Wheeler, and Horace Donisthorpe. They were rove beetles (Staphylinidae), particularly of followed by a number of influential researchers in the subfamilies and . the second half of the twentieth century, most Other -rich groups are flies (especially notably David H. Kistner [4, 5], Bert Hölldobler the ), parasitic , silverfish, and [1], and Carl Rettenmeyer [9]. the beetle families Carabidae, Scarabaeidae, The greatest diversity of guests is found in Tenebrionidae, and [5, 7]. nests of ants and . 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 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 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 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 , 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 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, whereas the host’s odor primarily by physical contact with unspecialized species that avoid their host will the workers (e.g., active rubbing in the myrme- use, or at best, fine-tune strategies that were cophilous silverfish Malayatelura ponerophila) already present in their free-living relatives. and nest material. When isolated they lose the Host specificity appears to be strongly related host-specific hydrocarbons, indicating that these to the level of guest specialization. Specialized are provided by the host. Alternatively, they species target only one or a very few closely can obtain the host’s profile by eating its larvae related hosts. In some cases, such as in Microdon and subsequently recycling the hydrocarbons. mutabilis, guest populations show even adaption This strategy was first described in the to an individual host population and cannot sur- bitaeniata associated with vive in other populations of the host. Generalists, ▶ Oecophylla weaver ants but has, for example, in contrast, are guests that may thrive in nests also been suggested in the wasp-associated beetle of distantly related hosts. Panmyrmecophiles (e. paradoxus. g., the isopod Platyarthrus hoffmannseggii) are (former Maculinea) butterflies even found with most ant species in their distri- () are by far the best-studied myrme- bution range. cophiles, because of their flagship role in butterfly conservation but also due to their fascinating Chemical Communication parasitic biology and use of chemical trickery. Communication in social insects is largely chem- Phengaris females lay eggs on specific host plants ically mediated. These signals play a vital role in (e.g., P. alcon on Gentiana, P. arion on Thymus). coordinating the colony’s activities, such as A Phengaris feeds on the host plant 4 Guests of Social Insects during the first instars and then drops to the ground, hiding, feigning death or emitting repel- ground. It starts to produce cuticular secretions lent substances. Note that the detection of these resembling the odor of the host’s . The cater- guests may be hampered once they succeed to pillars are taken by foraging workers to their nest, enter the nest. The inner walls of the nests where they either devour the ant brood (predatory passively accumulate high concentrations of com- strategy, e.g., P. arion) or are fed mouth to mouth pounds from the colony, which seem to be non- by the workers ( strategy, e.g., P. alcon). colony-specific. This nest odor coating may cause Once the adult emerges, it is recognized as an a saturation of the ants’ antennal receptors, intruder and must escape from the nest. Pre- resulting in a failure of intruder detection. adopted of P. rebeli mimic a large Guests could also target their host by secreting fraction of the hydrocarbon profile of the host’s volatile substances from epidermal glands. Many larvae (chemical ), but they perfect their free-living rove beetles possess a tergal gland integration by the acquisition of additional recog- through which they secrete defensive and toxic nition hydrocarbons in the nest (chemical camou- chemicals. It seems that non-integrated or poorly flage). Selection will favor host ants specialized rove beetles do not chemically mask that discriminate the chemical profile between their presence but rather deter their aggressive nestmates and parasites. Infected host using general tergal gland secretions. populations slightly alter their profile over gener- Some myrmecophilous rove beetles exhibit ations to allow discrimination of the parasite. a more advanced strategy and deceive their hosts However, this results in an evolutionary arms with glandular secretions. Pella beetles associated race in which the chemical profile of the parasite with Lasius fuliginosus release the ▶ alarm pher- must keep pace with the host’s changing profile. omone of the host using their tergal gland, which Guests could also persist within a colony by results in the ants panicking and fleeing. The use suppressing the number of recognition cues on of deceptive volatiles has been brought to its the cuticle. This strategy, commonly known highest point by the symphiles, or highly special- as chemical insignificance, allows the guest ized symbionts. Our knowledge of this mainly to remain undetected. Again, this deception strat- comes from detailed observations and experi- egy can be used to target multiple hosts and is ments with the rove beetles Lomechusa and widespread in nonhost-specific guests. Some are Lomechusoides. In these, the adult and larval able to apply chemical insignificance and mimicry stages of the beetles use multiple glands to in sequence, which was clearly demonstrated in appease the host and induce it to carry them ▶ social parasites. They carry few or no recogni- to the colony’s brood chambers. Symphiles tions cues when they invade the nest of their host, typically possess a battery of glands whose but in time they acquire the host’s odor, which substances are conducted to adjacent tuft-like facilitates their integration. As nestmate recogni- structures (trichomes) (Fig. 1). The hosts regularly tion is probably based on only a subset of the lick the exudates from these trichomes. Although cuticular profile, lacking or carrying low amounts the mechanistic role of glandular products has not of some key components (chemical transparency) been demonstrated in other symphiles than could already mask their presence in the colony. Lomechusa, it is expected that they also help to To date, this strategy has not been conclusively appease the host and are needed for an intimate demonstrated in any guest. association. Social parasites also use volatiles While most studied social insect guests take to facilitate their integration. advantage of one of these advanced chemical deception strategies, unspecialized associates tend to be undisguised and carry an idiosyncratic Social insect guests are typically of the size of the cuticular profile. They are detected by their host or smaller. Small size facilitates crypsis host as intruders, but they escape from host attack and makes the symbiont harder to catch. During by fleeing, agile movements, crouching to the evolution, some body parts were reduced or even Guests of Social Insects 5

Guests of Social Insects, Fig. 1 The specialized in the nest of a Formica host during spring and summer. myrmecophile Lomechusa emarginata (Staphylinidae: Similar to the adults, they are groomed, transported, and ) has an alternating life cycle. The adults fed by trophallaxis. (Photos by Pavel Krásenský – http:// reside in the nest of Myrmica ants during winter. Adoption www.macrophotography.cz (adult) and Thomas and integration in these nests are promoted by different Parmentier (larvae)) glands and yellow trichomes. The larvae of this beetle live lost in many inquilines. As social insect nests (Fig. 4). Interestingly, some specialized guests are dark inside, vision became less important such as the pselaphine rove beetle supertribe for inquilines, and many inquilinous silverfish Clavigeritae (Fig. 5) show recessed mouth parts (e.g., Atelura), Collembola (e.g., Cyphoderus), which favor the exchange of food with their ant (e.g., Platyarthrus), and crickets host. Many guests, both unspecialized and spe- () are blind or possess reduced cialized, have compacted and relatively short eyes and show reduced pigmentation, similar legs and antennae (Fig. 5), presumably to avoid to what we observe in cave-dwelling or cave- damage or loss in antagonistic interactions with burying . The stable nest environment host workers. The coxae of the termitophilous promoted the loss of wings in guests such as in rove beetle tribe Trichopseniini are protective the ant Myrmecophilus (Fig. 2), the myr- plate-like structures, under which the metalegs mecophilous Attaphila, the bee louse can be retracted. In some specialized guests, cauca (Diptera) (Fig. 3), and several most remarkably in the myrmecophilous myrmecophilous and termitophilous phorid flies. Paussinae beetles (Carabidae), the antennae have Some termitophilous sciarid flies emerge with evolved to complex truncate, flattened, tubular or wings, which are later shed to promote mobility disc-like structures possessing a cavity with 6 Guests of Social Insects

Guests of Social Insects, Fig. 2 The Myrmecophilus albicinctus (: Myrmecophilidae) receives a food droplet from its host Guests of Social Insects, Fig. 4 The black gnat Anoplolepis gracilipes. This cricket has no wings and (Diptera: Sciaridae) Pnyxiopalpus rosrii living with its small eyes, typical reductions seen in many social insect termite host Nasutitermes sp. The wing stumps fl guests. It possesses modified mouth parts to facilitate food (highlighted with arrows) indicate that this y sheds its transfer through trophallaxis. (Photo by Taku Shimada – wings after eclosion as an adaptation to an inquilinous life. http://www.antroom.jp/) (Photo by Taisuke Kanao)

Guests of Social Insects, Fig. 3 The bee louse Braula Guests of Social Insects, Fig. 5 The pselaphine beetle coeca (Diptera: ) is a wingless fly with special Claviger testaceus inspected by its host ant Lasius niger. comb-shaped tarsi helping to cling to the hairs of its host This highly specialized parasite enjoys a royal treatment Apis mellifera. (Photo by Yuanmeng Miles Zhang) (grooming, transport, trophallaxis) in the nest, which is mediated by yellow trichomes exposing glandular secre- tions. The central cavity of the beetle’s abdomen serves as a secretory cells. These structures probably secrete handling notch for the ants. The antennae are compacted, appeasing substances that promote integration in which is an adaptation to frequent handling and carrying by – the colony. Highly specialized myrmecophilous the host. (Photo by Pavel Krásenský http://www.macro photography.cz) beetles, such as the pselaphine rove beetle Claviger, enjoy a royal treatment and are are also typical structures of specialized myrme- often picked up and transported in the nest. They cophiles. They are licked by the ant host often possess notches, which ants use to grasp and seemingly facilitate the complete integration them (Fig. 5). These furrows or cavities are often of “symphiles.” Pores connected to glands are accompanied with glandular structures. Tri- located between the trichome hairs. The trichomes chomes, which are tufts of mostly yellow- probably serve as wick-like structures to expose or golden-colored setae on the thorax or abdomen, Guests of Social Insects 7 glandular products. Trichomes are typically found a limuloid (Limulus: horseshoe crab) or drop- in highly specialized myrmecophilous beetles shaped body form [4]. This is an expansion (Figs. 1 and 5), but also some termitophilous of the anterior body part in concert with shorten- beetles and the myrmecophilous wasp Tetra- ing of appendages, covering shields, and reduced mopria carry an analogous structure of trichomes. head size. This smooth body form does not expose A unique morphological feature independently potential grasping points and permits the inquiline evolved in multiple lineages of termitophiles to slip through the mandibles of its host. Finally, (mostly found in rove beetles, but also in phorid the compact, robust body of some free-living flies, gall gnats, and scarabaeids) is physogastry arthropod lineages proved to be preadaptive to [4, 5], the swelling of the abdomen to several successfully integrate into social insect nests. times its initial size (Figs. 6 and 7). Extremely Inquilinous representatives of these groups look enlarged abdomens are recurved and held nearly identical to free-living relatives. Their over the body as seen in the rove beetle tribe tank-like body is well suited to withstand host Corticocini. The exact role of this inflated body aggression, especially when the appendages are is unknown, but it is assumed that it is associated also retracted (e.g., the red wood ant associates with the production of deceiving chemicals Monotoma and Dendrophilus). or may favor tactile mimicry. Physogastry is typ- ically seen in highly integrated termitophiles. Behavior Some physogastric rove beetles (Corotocina) Poorly integrated species exhibit a completely went even a step further and exhibit morphologi- different behavioral repertoire from that of spe- cal mimicry. Their swollen abdomen is strategi- cialized guests. Whereas unspecialized species are cally constricted and supports projecting prudent and avoid direct physical interaction with appendages, resembling in that way the nymphs their hosts, highly specialized species boldly walk of their host as seen from above. Morphological among the host workers without eliciting aggres- mimicry is also manifested in some highly inte- sion. The host will actively interact (antennating, grated myrmecophilous beetles associated with grooming) with the guest as with a worker or ▶ army ants. They closely resemble the body of larva. Even congeneric inquilines can greatly their host through a petiolate abdomen, elongated vary in their behavior, as is seen in the ant cricket legs and body, geniculate antennae, and in some Myrmecophilus. The generalist M. formosanus cases similar body coloration. This myrmecoid targets multiple unrelated hosts. It avoids physical body plan evolved at least 12 times independently contacts with them and escapes attack by running in the rove beetle subfamily Aleocharinae. and jumping. The host-specific M. albicinctus Mimicry of the body plan of a host is known as provokes much less aggression. When detected, Wasmannian mimicry. The selection pressure act- it displays a specific defensive behavior: It stops ing on the beetles is still open to discussion walking and humps its back. The host then stops and possibly different mechanisms act in synergy. chasing and antennates the cricket, which allows Wasmann originally argued that the resemblance the cricket to escape. While M. formosanus feeds in body plan of the beetles has been selected on food remnants in the nest, M. albicinctus is to dupe the host, as tactile cues may play a role completely dependent on food delivered by the in colony integration as well. However, since host through trophallaxis (Fig. 2). This transfer army ants have poor vision, this cannot explain of food to other colony members via mouth-to- why some beetles evolved matching coloration. mouth (stomodeal) or anus-to-mouth (proctodeal) It seems likely that it serves in protection from feeding is a key process in social insects. visually hunting predators, especially the various The specialized cricket M. albicinctus imitates birds that attend columns. the begging behavior of a hungry worker by Many poorly integrated termitophilous and tapping the ant’s mouthparts with its forelegs myrmecophilous beetles (Figs. 8 and 9) and sil- or maxillary palps and is rewarded with regurgi- verfish (Fig. 10) have independently evolved tated food. Many other myrmecophiles (e.g., 8 Guests of Social Insects

Guests of Social Insects, Fig. 8 Vatesus are conspicuous rove beetles with a limuloid defensive body shape and are Guests of Social Insects, Fig. 6 The physogastric rove associated with army ants. The adults and larvae walk in beetle (Staphylinidae: Lomechusini) Longipedisymbia sp. the emigration columns of their host, here associated with Longipeditermes longipes. (Photo by burchellii. (Photo by Taku Shimada – http://www. Taisuke Kanao) antroom.jp/)

Guests of Social Insects, Fig. 9 Discoxenus lucidus, Guests of Social Insects, Fig. 7 The unusual, here with its host Hypotermes makhamensis, has a typical physogastric fly Javanoxenia sp. (Diptera: Phoridae, defensive limuloid body form. (Photo by Taisuke Kanao) Termitoxeniinae) associated with the fungus-growing ter- Odontotermes sp. (Photo by Taisuke Kanao) Acoustic Communication It has only recently become apparent that guests Antennophorus in Fig. 11, Atelura formicaria, can exploit the acoustic communication found in , Dinarda maerkelii, many insect societies. They have managed to Claviger, Maculinea species with cuckoo strat- break the acoustic code, similar to what is found egy, Paussus, subtribus Lomechusina), in chemically mimicking guests. Some ants pro- termitophiles (e.g., Sinophilus), and even bee duce low-frequency sounds through stridulation. guests (Aethina tumida) also solicit food. Many These are used to communicate to nestmates of these are highly integrated and even show regarding recruitment, rescue, mating, and caste a reduction in mouthparts (Claviger), but moder- identity or social status. Acoustic deception ately specialized species (Amphotis, Dinarda, was first reported in caterpillars and pupae of Atelura) also engage in trophallaxis. As trophal- . The caterpillar is constantly laxis facilitates the distribution of the nest colony fed by trophallaxis (cuckoo strategy) and even odor among nestmates, food begging by guests supplied with the host’s larvae in case of food may also favor their chemical integration. shortage. The host even rescues the caterpillar in Guests of Social Insects 9

Guests of Social Insects, Fig. 10 Silverfish associated with social insects. (a) Unidentified silverfish with a limuloid body associated with the termite Longipeditermes longipes. (Photo by Taisuke Kanao). (b) Neoasterolepisma sp. associated with barbarus. (Photo by Thomas Parmentier) (c) Atelura formicaria associated with Lasius flavus. (Photo by Thomas Parmentier) preference to its own larvae when the nest Dispersal is disturbed. Caterpillars and pupae closely Dispersal to new nest sites is a critical but poorly mimic the larval hydrocarbon profile of its host studied phase in the life cycle of many guests. (), which helps in getting Given the spatial configuration of host nests as adopted into the colony. However, chemical trans- small islands embedded in an inhospitable land- fer experiments with dummies indicated that scape matrix, effective dispersal is fundamental. chemical trickery was not sufficient to achieve Overall, social insect associates disperse when integration. The royal treatment appears to be they colonize a new host colony or when they achieved by acoustically mimicking the host’s track a mobile host colony as it moves to a new queens. The workers display the same benign site. Guests, especially those that fly, are expected behavior in response to the sounds of the caterpil- to locate new host colonies at a distance by mov- lars as those produced by their own queens. ing toward volatiles emitted from the host workers Acoustic mimicry is even more refined in the or nest. The attractive role of long-range host cues specialized myrmecophile Pausus favieri. This has been clearly demonstrated in phorid flies beetle is able to imitate the sound of three castes parasitizing ants. These cues represent different (worker, soldier, and queen) of its host ▶ Pheidole types of and are produced in several pallidula. It is suggested that this beetle can mod- glands. In addition, positive attraction to host ulate its acoustic signals dependent on its needs volatile cues is reported in some other guests. and the caste with which it is interacting. The myrmecophilous isopod Platyarthrus 10 Guests of Social Insects

Guests of Social Insects, Fig. 11 Different ectoparasitic on the mandibles of an Eciton dulcium army ant major. mites associated with ants. (a) The ectoparasitic mite Ante- (Photo by UConn BRC/C. W. Rettenmeyer – Kodachrome nnophorus sp. steals food from two Lasius capitatus database at http://aagc.uconn.edu). (c) Macrocheles workers in trophallaxis. These mites also directly beg for rettenmeyeri on the hind leg of the army ant . food by stimulating the worker they are riding on with its (Photo by b and c: UConn BRC/C. W. Rettenmeyer – long front legs. (Photo by Taku Shimada – http://www. Kodachrome database at http://aagc.uconn.edu) antroom.jp/). (b) Two individuals of Circocylliba crinita hoffmannseggii shows positive chemotaxis to an Host detection in Phengaris butterflies is more increasing gradient of formic acid, a defensive complex. Gravid females of P. arion are not volatile abundantly secreted by many of its attracted by host ant cues but rather respond to host’s workers. Females of the hover fly volatiles emitted by their host plant, Origanum bombylans, of which the larvae live in bumble bee vulgare. Because of the sequential host exploita- nests, are triggered to deposit their eggs when they tion of the host plant and the Myrmica ants, female detect the odor of bumble bee nests. P. arion butterflies preferentially lay eggs on the Further evidence of the attractive role of host plants located near Myrmica nests. Females host cues comes from work on Lomechusa. are guided to these particular plants by carvacrol, These beetles have a remarkable life history. a monoterpenoid volatile emitted by oregano Larval development and pupation take place in a as a response to root disturbance by nesting Formica nest. The emerged adult then seeks Myrmica ants. a Myrmica nest to hibernate (Fig. 1). In spring While little is known of the attractive role and females locate a Formica nest, in which they nature of volatile cues emitted from the nest, mul- deposit their eggs. Experiments showed that tiple studies demonstrated that myrmecophiles adult beetles are strongly attracted to an air flow can track their host’s trails. Nearly directed over nest material of the host. Interest- all army ant symbionts tested could follow the ingly, this positive response in the adult beetles pheromone trails of their hosts (Fig. 8). As toward the Myrmica cues only lasted 2 weeks after the nomadic ants constantly move to new nest leaving the Formica host. It was also reported that sites, it is adaptive for the guests to closely keep newly emerged adults of some myrmecophilous up with them. Poorly integrated army ant guests rove beetles were more active and exhibited a have been observed flying to the bivouacs, so it greater tendency to fly than older individuals. was suggested that they locate their host by vola- These findings suggest that dispersal propensity tile nest cues. in guests peaks during a short period of time and Trail following has also been documented in may depend on specific conditions. guests associated with non-nomadic ants. They Guests of Social Insects 11 probably use these pheromone trails to find nests cling to the bodies of the workers and are carried connected to these trails, but the localization of into the wasp nest. They crawl into cells with full- distantly located nests likely requires the tracking grown larvae and consume them (Fig. 12). of volatile nest cues. Some ants with permanent Phoresy is especially well-developed in army ant nests, such as ▶ red wood ants and weaver ants, guests. Army ants do not have a permanent nest, occasionally move to new sites as well. The com- and most species are often on the move. Many of plete colony may look for a new home when their associates are less mobile and can only track nest conditions are deteriorate. Alternatively, the fast-moving mass by hitchhiking on workers, ▶ polydomous colonies with multiple queens brood, or booty. In that way, they are also often bud fragments of the colony. Recent obser- protected from lurking predators during migra- vations showed that a large part of the parasitic tions. The recently discovered histerid beetle larvae of the beetle Clytra quadripunctata were Nymphister kronaueri uses a stunning mechanism able to follow their red wood ant host when it of phoresy. With its long mandibles, it clings to its moved to a new nest site. Nevertheless, the host army ant host between the petiole and postpetiole could profit from regularly ▶ relocating the nest while retracting its appendages. Another excep- when a large part of the associated parasites is not tional mode of transport is found in the snail capable of tracking the host to the new site. Allopeas myrmekophilos. This snail produces Many guests climb on the body of their host to a foam which is highly attractive to its track their host or to disperse to a new nest. Such ▶ Leptogenys army ant host. The workers pick phoresy is especially found in mites. Phoretic up the snail and transport it to a new nest site as mites associated with Neotropical army ants they do their brood. are adapted to particular positions (between tarsal claws, antennae, mandible) on the host’s Synchronization of Reproduction body (Fig. 11). The beetles Odontoxenus and Our knowledge of the biology of social insect Doryloxenus are equipped with special hairs that guests is fragmentary, and the life cycles of assist in holding onto their termite or ant hosts. only a few species have been worked out. Some phoretic mites are ectoparasitic, but most Nevertheless, it appears that the life cycle of phoretic mites and beetles appear to be commen- guests is narrowly synchronized with the repro- sals that consume exudates or organic material on ductive cycles in the host’s colony. This is nicely the host’s body. Some myrmecophilous mites illustrated in the rove beetle Vatesus (Fig. 8). The preferentially attach to virgin queens, which are colony cycle of its army ant host alternates the dispersing individuals in ant colonies. The between a 2-week nomadic phase in which it wingless cockroach Attaphila fungicola also migrates to a new site every day and a statary takes advantage of virgin queens to colonize phase in which it is based in the same site for new nests. After mating, the cockroach seems to about 3 weeks. Egg maturation in the female remain with the alate queen when it enters an beetles starts at the end of the nomadic phase, established nest. The queen can also found and egg laying occurs at the beginning of the a new nest, but then the cockroach appears to stationary phase. As such, the beetle’s eggs hatch separate from its vector and seeks an established in the temporary nest (bivouac), where the larvae nest. Some phoretic parasites also target foraging can directly benefit from host’s resources. Once workers, which carry them into the nest. This the colony starts to move again, the larvae follow is nicely demonstrated by Metoecus beetles, obli- it to new sites. Mature larvae leave the colony and gate parasites of eusocial wasps. The main host pupate, and the adults search for a new host col- of is . This ony, probably on the wing. strange-looking beetle lays eggs in the crevices of Reproductive synchronization can also be decaying wood. The following spring, the larvae found in guests associated with red wood ants hatch and wait for a visiting wasp worker to come in Europe. The nest conditions alternate collecting wood for nest construction. The larvae between hibernation and a phase of active 12 Guests of Social Insects

(Batesian mimicry). The larvae of most European species are commensals feeding on detritus or refuse. The larvae of V. inanis, however, have evolved to consume the wasp larvae (Fig. 13), which is reflected in their deviating feeding apparatus. Mutualistic interactions between guests and the host have not been demonstrated in social insects. In solitary bees, some mites have a sani- tary effect in the brood cells by consuming contaminating fungi. Likewise, fungivorous social insect guests, such as springtails and mites, or guests feeding on dead corpses, may Guests of Social Insects, Fig. 12 The beetle Metoecus provide hygienic services to their host, although paradoxus () in the nest of its host Vespula vulgaris. Soon after emergence from a larval cell of its host, this has not yet been demonstrated. the beetle will leave the nest. (Photo by Tom Wenseleers – Social insects regularly support multiple spe- https://bio.kuleuven.be/ento/index.htm) cies of guests, and it can be expected that these species not only interact with their hosts but also thermoregulation from April until August. The with each other. A network of predator-prey larvae (and adults) of associated rove beetles interactions was demonstrated in the large com- reach peak abundance during the warmest period, munity of myrmecophiles associated with red which overlaps with the peak of ant brood ▶ wood ants [8]. The host indirectly benefits and retrieved prey. This synchrony with the opti- from the presence of some predatory guests, mal temperature and maximum availability of as they also capture parasitic guests. Next to resources promotes the beetles’ rapid growth and predatory interactions, interspecific competition can even lead to multiple generations in one sea- may also drive the dynamics of symbiont commu- son. When temperatures drop in autumn, larval nities. Maculinea and Microdon larvae can co- numbers rapidly decline and hibernation takes occur in Myrmica colonies, although both are place in the adult phase. brood predators that severely exploit the host’s resources. Larval development of Maculinea caterpillars takes place during spring, whereas Niches of Social Insect Guests the Microdon larva growth occurs during the sum- mer. It was suggested that larvae of both parasites Trophic Niche can coexist due to this temporal segregation. Many social insect guests negatively affect their hosts. They either prey on the brood, pilfer Spatial Niche foraged food, solicit food, or even consume culti- Nests of social insects are heterogeneous in vated fungi. However, a large fraction of guests resources, building material, climatic conditions, does not seem to harm the host. They live as and worker density. Especially large nests, with commensals and thrive in the refuse of the nest. a greater variety of niches, presumably harbor It is generally assumed that the most specialized a richer symbiont community. The brood is typi- guests are strictly parasitic, whereas poorly cally confined to the deep and central parts of integrated species act as scavengers, facultative the nest and is surrounded by the greatest density parasites, or commensals. Interestingly, different of workers. Other typical niches are refuse trophic strategies can occur among congeneric pits and locations where prey or nectar is stored. species. Volucella are spectacular syrphid flies of Specialized guests circumvent host aggression which the larvae develop in the nests of bees using deception and so may enter the heavily and wasps and the adults resemble the host adults protected brood chambers where they feast on Guests of Social Insects 13

Guests of Social Insects, Fig. 13 Left: The adult hover fly (Diptera: Syrphidae) is a Batesian mimic of the social wasp Vespula vulgaris. (Photo by Keith Edkins. Right: The fly’s larva feeds on larvae of the wasp host. Photo by Bob Brown) host’s eggs and larvae. Unspecialized guests, consider some of the most interesting topics for rather, reside in the peripheral parts of the nest the coming period: or in the refuse area, which is characterized by fewer agonistic interactions and more hiding 1. While a great number of guests of social insect opportunities. Exceptions are some unspecialized guests have been recorded and described, red wood ant inquilines that are found in highest many more remain to be discovered. Their numbers in the brood chambers. It is noteworthy hidden existence ensures that large numbers that some obligate guests (apart from the typical have been overlooked. They are markedly trophobionts) live outside the nest and so are undersampled in many parts of the world, strictly speaking not inquilines. These arthropods including and all tropical regions. live at the periphery of the nest, along the Many unrecognized new species are undoubt- trails or in extranidal refuse pits. One group is edly also sitting in museum collections. harmful to the host and captures living workers The Carl W. & Marian E. Rettenmeyer Army (Aleocharinae: Pella and Zyras living with Ant Guest Collection at the University of Lasius fuliginosus), feeds on aphid herds (the Connecticut contains more than 100,000 myr- ladybirds magnifica and Platynaspis mecophile specimens. It recently became clear luteorubra), or begs for food (Amphotis that cryptic diversity could be exceptionally marginata). high in social insect guests, with very similar- looking species specialized to different hosts. Multidisciplinary approaches integrat- ing large-scale sampling, morphology, and Future Directions emerging genetic tools could help us to resolve the complicated of guest lineages. Our knowledge of social insect guests has steadily An improved taxonomy of social insect guests grown in the last decades. Still, they must be will help us to assess the pervasiveness of regarded as poorly understood, with a great inquilinism in different arthropod lineages. many fruitful avenues still open for both field It will give us a better understanding of com- and laboratory studies. The following are what I munity structuring in social insect-symbiont 14 Guests of Social Insects

networks across different scales, and new metacommunities. Surprisingly, the mecha- patterns in host specificity and host switching nisms that inquilines use to disperse from one will be unraveled. nest to another and the rate of dispersal are 2. A large part of recent research on guests poorly known. It can be expected that symbi- has focused on their chemical ecology. More onts use different strategies to persist in the specifically, manipulative adaptations to the metacommunity. This variation may have cuticular chemical profile have been examined a profound effect on the structure and stability in different types of guests. Unfortunately, of the local host-inquiline networks. Field research on the glandular secretions of guests observations and experiments in concert with has been losing momentum. The difficult new molecular tools using next generation identification and isolation of glandular com- sequencing (NGS) will enable us to disclose pounds requires expertise in advanced organic the dynamics of these spatial networks. chemistry, which clearly discourages many Next, large-scale studies focusing on patterns biologists. Given the plethora of glands found and processes that shape inquiline communi- in many guests, it can be expected that they ties are completely lacking. A macroecology play a pivotal role in appeasing, deceiving, approach could, for example, help us to and/or deterring the host. Guests probably understand how host distribution patterns require both cuticular and glandular secretions vary across different groups of symbionts to exploit the benefits of the colony to the (termitophiles vs myrmecophiles/parasites vs. fullest. It would be very useful to compare mutualists). We could also gain insight into glandular and cuticular compositions along how abiotic nest conditions and features of a gradient of guest specialization while using the host affect the assembly of inquiline com- glandular and cuticular composition of free- munities. At present there are only some vague living relatives as a reference, for example, indications that host colony size and the pres- in the rove beetle subfamilies Aleocharinae ence of organic nest material (cf. red wood or Pselaphinae. Integrating phylogeny into ants, Lasius fuliginosus) may positively affect the study of chemical deception could help guest diversity. Recently it was argued that us to better understand the evolution of social insect guest communities are ideally inquilinism. Next to the chemical deception suited to approach with an ecological network strategies, we have little or no knowledge framework [3]. Historically, the interaction of the chemical cues that attract guests. It is between a host and a guest was studied in intriguing how they can locate their host nest separation from other interactions. However, from a distance. Some guests are generalists different guests often interact directly (preda- with little or no host specificity, yet even these tion, competition) or indirectly with other seem always to be confined to one of the four guests and may target multiple host species. social insect groups. A community-wide approach can integrate 3. Ecological research on social insect guests these multispecies interactions and reveal new is rather scant and limited to a few local ecological and evolutionary patterns for com- field studies. The unique spatial distribution parison with other ecological networks. of inquiline communities makes them very good models for small-scale studies of spatial ecology. Inquiline communities can be References conceptualized as metacommunities, because the symbionts live in spatially distinct nests 1. Hölldobler, B., & Wilson, E. O. (1990). The ants. (patches) susceptible to colonization from Cambridge, MA: Harvard University Press. other local communities and surrounded by 2. Howard, R. W., McDaniel, C. A., & Blomquist, G. J. (1980). Chemical mimicry as an integrating mecha- an inhospitable landscape. Therefore, inquiline nism: Cuticular hydrocarbons of a termitophile and its communities are among the few true terrestrial host. Science, 210, 431–433. Guests of Social Insects 15

3. Ivens, A. B. F., von Beeren, C., Blüthgen, N., & 8. Parmentier, T., Bouillon, S., Dekoninck, W., & Kronauer, D. J. C. (2016). Studying the complex com- Wenseleers, T. (2016). Trophic interactions in an ant munities of ants and their symbionts using ecological nest microcosm: A combined experimental and network analysis. Annual Review of Entomology, 61, stable isotope (d13C/d15N) approach. Oikos, 125(8), 353–371. 1182–1192. 4. Kistner, D. H. (1979). Social and evolutionary signif- 9. Rettenmeyer, C. W., Rettenmeyer, M. E., Joseph, J., & icance of social insect symbionts. In H. R. Herman Berghoff, S. M. (2010). The largest association (Ed.), Social insects (Vol. I, pp. 339–413). San centered on one species: The army ant Eciton Francisco/London: Academic. burchellii and its more than 300 associates. Insectes 5. Kistner, D. H. (1982). The social insects’ bestiary. Sociaux, 58, 281–292. In H. R. Hermann (Ed.), Social insects (Vol. III, pp. 10. van Zweden, J. S., & d’Ettorre, P. (2010). Nestmate 1–221). London: Academic. recognition in social insects and the role of hydrocar- 6. Lenoir, A., D’Ettorre, P., & Errard, C. (2001). bons. In G. J. Blomquist & A.-G. Bagnères (Eds.), Chemical ecology and social parasitism in ants. Insect hydrocarbons biology, biochemistry and chem- Annual Review of Entomology, 46, 537–599. ical ecology (pp. 222–243). New York: Cambridge 7. Parker, J. (2016). Myrmecophily in beetles (Coleop- University Press. tera): Evolutionary patterns and biological mecha- 11. Wasmann, E. (1894). Kritisches Verzeichniss der nisms. Myrmecological News, 22,65–108. myrmekophilen und termitophilen Arthropoden. Berlin: F. L. Dames. xv.