2532 M Myrmecomorphy Myrmecomorphy and , and describe some examples of intraspecific variation. James McIver, Gary Stonedahl USDA Forest Service, Pacific Northwest Experiment Station, La Grande, OR, USA

Myrmecomorphy, or the morphological and Spiders have a wide variety of body forms, but behavioral mimicry of ants, has evolved at least compared to ants, typically have relatively short, 70 times in the – 15 times in spiders, hairy bodies. Ants are generally elongate, have a at least 10 times in plant bugs, and seven times medially constricted body with a distinct petiole, in staphylinid beetles. More than 2,000 species elbowed antennae, large compound eyes, and typ- of myrmecomorphic arthropods have been ically a shiny integument. Ant-like spiders on the described thus far, belonging to over 200 genera other hand, are relatively elongate, have a medial in 54 families. Myrmecomorphy forms a subset constriction of the cephalothorax into a head and of ant mimicry, which includes all species that alitrunk, with a narrowing of the posterior cepha- resemble ants through convergence in morpho- lothorax or anterior abdomen to produce a peti- logical, behavioral, chemical, or textural charac- ole and gaster. Ant-like spiders often use the first ters (Fig. 117). The other major group of or second pair of legs as if they were antennae, ant-mimetic species are the myrmecophiles, or have pigmented spots on the cephalothorax that those arthropods that associate closely with resemble large compound eyes, often have shiny ants, but do not necessarily resemble them mor- setae or dense mats of reflective hairs to give a phologically. Although some are also myrmeco- shiny illusion, and can have a transparent cuticle morphic, most myrmecophiles have chemical to give the illusion of a constriction. Many ant- and/or textural characters that facilitate a close like spiders match the color of their ant models relationship with their ant hosts. Here we closely. Populations of the jumping Syne- describe signal properties of myrmecomorphic mosyna aurantiaca are color polymorphic, with arthropods, present their taxonomic distribu- yellow morphs resembling the ants Pseudomyrmex tion, and discuss their adaptive significance. flavidulus and P. oculatus, and black morphs resembling P. g ra c i li s . Correspondence in the color of individual structures in not uncommon, Signal Properties of as in the species-specific mimicCastianeira mem- Myrmecomorphic Arthropods nonia, in which the yellow terminal segments of the front legs correspond to the bright yellow Mimicry can be defined as a system that involves antennal apices of its otherwise black ant model, an organism (the mimic) which simulates signal Pachycondyla obscuricornis. The evolution of ant- properties of another organism (the model) so like behaviors in myrmecomorphic spiders is not that the two are confused by a third organism surprising, given that behavior is often identified (the operator) and the mimic gains protection, as the most conspicuous feature of ants. In both food, or a mating advantage as a consequence of clubionid and salticid spiders, the first or second the confusion. Myrmecomorphic species express pair of legs are waved around in front of the spi- a variety of signal properties that enhance their der, contacting the substrate in much the same resemblance to ants, involving shape, pattern, way that ants use their antennae. The antennal texture, color, behavior, and size. In this section, illusion is often supplemented by a zigzag run- we review how mimicry is achieved for a repre- ning gait, and in jumping spiders, there is a ­general sentative ­sample of myrmecomorphic spiders reluctance to jump. In general, the spiders that Myrmecomorphy M 2533 are most difficult to distinguish from ants in the field are those that have a combination of mor- phological and behavioral ant-like features.

Insects

While insects are confronted with many of the same problems as spiders for evolving ant-like form, the possession of a similar body plan requires less profound modification. A major con- straint to myrmecomorphy, however, is the one or two pairs of wings found in most adult insects. Consequently, the loss or reduction of wings in the adult is common in ant-like species, often accompanied by a constriction of the poste- rior thorax and/or anterior abdomen. In those species of myrmecomorphic insects that have retained their wings, oblique or transverse pale marks or bands of pale hairs typically interrupt the otherwise darkened forewings, to produce the illusion of a petiole. Still other species, such as aly- dids and mantids, resemble ants only in the imma- ture form. Compared to many insects, ants have relatively large heads with well developed mandi- bles. In general, myrmecomorphic insects tend to possess relatively larger heads than their non- Myrmecomorphy, Figure 117 Ants (top), mimetic relatives, and the illusion of large man- ­myrmecomorphs (mimics; middle), and dibles in many ant-like plant bugs is accomplished ­non-mimetic relatives (bottom). (a) Formica by enlargement of the ventral region of the head, obscuripes (Formicidae), western North America. which also brings the head forward into a more (b) Coquillettia insignis (), western North ant-like horizontal position. Many ant-like insects America. (c) Pronotocrepis clavicornis (Miridae), mimic the elbowed antennae of ants through western North America. (d) Pseudomyrmex tenuis differential pigmentation or enlargement of vari- (Formicidae), Central and South America. (e, f) ous antennal segments. Myrmecomorphic insects ­Synemosyna aurantiaca (Salticidae), ­Trinidad, often display microstructural and color modifica- ­. (g) Habronattus mexicanus (Salticidae), tions that enhance mimicry, including: (i) silvery, southern North America, Central America, reflective hairs to increase body shine, or when Caribbean. arranged in bands, to act as an interruptive agent; (ii) changes in surface texture corresponding with smooth, roughened, or pitted areas on the ant’s As in the spiders, morphological adaptations body; (iii) thoracic or abdominal spines to mimic in ant-like insects are often accompanied by those on the alitrunk and petiole of some ants; resemblance in behavior. Many staphylinid bee- and (iv) color polymorphisms that match avail- tles are difficult to distinguish from their army ant able ant models (Fig. 117). hosts, due to very similar patterns of locomotion. 2534 M Myrmecomorphy Regarding the behavior of alydid bugs, Oliveira Taxonomic and Geographic (1985) remarks, “Nymphs of Hyalymenus have a Distribution of Myrmecomorphy highly differentiated ant-like morphology which is achieved by several structural adaptations. The Myrmecomorphy has been identified in nine fam- similarity is greatly enhance by the nymph’s ant- ilies of spiders and 45 families of insects, repre- like behavior, notably the rapid zig-zag loco- senting 11 different orders. Over 200 spider and motion, the constantly agitated antennae, and insect genera are known to contain myrmeco- the up and down movement of the abdomen morphs, and the number of species involved is cer- (similar to an alarmed ant)”. tainly in the thousands worldwide. Ant-mimicry has arisen at least four times in the spider families Clubionidae and (running spiders), Transformational Mimicry three times in the Salticidae (jumping spiders), and several times each in the Aphantochilidae, Because their ant models are holometabolous, Araneidae (orb-weavers) and Theridiidae (comb- mimic species that develop gradually, like plant foot weavers). In the plant bugs (: Mir- bugs and spiders, tend to resemble a range of idae), morphological resemblance to ants has appropriately sized models, usually representing arisen no fewer than ten times, and this family two or more ant species or genera. This phenom- contains the highest diversity of myrmecomorphic enon is called transformational mimicry, and species among insects. has been described for mantids, plant bugs, aly- Myrmecomorphic arthropods are found in all did bugs, running spiders and jumping spiders. major regions of the world except Antarctica and Species that rely on transformational mimicry the extreme northern Holarctic. The number of are typically -specific mimics, presumably species increases toward the tropics, mirroring the because features that provide species-specificity pattern observed for other mimetic species, for on one life-history stage constrain the evolution ants themselves, and for most other plant and ani- of features that promote close correspondence mal groups. to different ants in other stages. Adaptive Significance Sexual Dimorphism The adaptive significance of myrmecomorphy has While not common in ant-mimetic systems, sexual not been clearly established in most cases. The dimorphism has been described in several groups most common mimetic hypotheses to explain of spiders and some /Heteroptera. The myrmecomorphy are Batesian, Wasmannian, and adult males of the Zuniga magna aggressive mimicry. are striking mimics of Pseudomyrmex gracilis, while females closely resemble the ponerine Pachy- condyla villosa. In both cases, the species-specific Batesian Mimicry mimicry involves remarkably accurate structural and color correspondence between model and For those ant-like species that do not live with or mimic. Many myrmecomorphic plant bugs are sex- attack ants, the most widely supported hypoth- ually dimorphic; brachypterous or apterous females esis for myrmecomorphy is Batesian mimicry. are among the best morphological mimics of ants, The evolution of Batesian mimicry is presumed to while the macropterous males are comparatively occur within the context of an interactive system poor pattern mimics. involving model, mimic, and a predaceous Myrmecomorphy M 2535 operator(s). The system has four basic features: estimate population sizes of mimics in relation to (i) certain arthropods (models) are unacceptable their models, observational evidence suggests that to predators and advertise this, (ii) predators ants are almost always more common than co- (operators) learn about this unacceptability, occurring mimics. Most evidence suggests that (iii) generalization in predators takes place allowing free-living myrmecomorphs are relatively palat- acceptable species (mimics) to benefit by resem- able – spiders serve as important prey items for blance, and (iv) visual discrimination by preda- birds and lizards, and myrmecomorphs are no tors is sufficient to select for increased mimetic exception to this general rule. resemblance. The behavioral and ecological con- The most likely predators that could serve as ditions presumed to favor the evolution of Bate- operators in Batesian mimicry systems are small sian mimicry include: (i) the model must be an vertebrate predators such as lizards and birds, and unacceptable prey item to at least some predators, predators such as jumping spiders and (ii) the mimic must be an acceptable prey item, wasps. These predators possess relatively good (iii) the model and mimic must have similar tem- vision, necessary to select for the detailed struc- poral and spatial distributions, (iv) the model tural and behavioral adaptations seen in many must be common relative to the mimic, (vi) the myrmecomorphic species. Vertebrate species are mimic must have signal properties that deceive also well known to be capable of associative learn- visually oriented predators within a community ing, including experimental studies involving of alternate prey, and (vii) predators must be mimetic insects. While associative learning has able to learn. Our discussion on the evidence for been demonstrated in social insects, similar data Batesian mimicry addresses these conditions by on arthropod predators are scanty at best, possibly describing the qualities of species within selected because of the greater difficulty in choosing myrecomorphic systems, and offering observa- meaningful stimuli for arthropods that are soli- tional and experimental evidence of functional tary, more reclusive than bees and ants, or have Batesian mimicry in the field. unknown feeding habits. Nonetheless, a few stud- In the best known myrmecomorphic systems, ies have demonstrated the capacity for associative models, mimics and predators tend to possess eco- learning in arthropod predators, involving wasps, logical and behavioral features consistent with a mantids, crab spiders, and assassin bugs. Batesian mimicry hypothesis. Like bees and wasps, Some of the most convincing observational ants have features that make them ideal models in evidence that supports Batesian mimicry in ant- Batesian mimicry systems. Ants are among the like species comes from the existence of a number most common and conspicuous of insects, and of remarkably close species-specific correspon- workers of many species are aggressive and dis- dences between model and mimic, particularly tasteful. Ants are entirely social, and have alarm among the spiders. For example, the running spi- pheromones used for common defense against der Mazax rettenmeyeri features a unique ridge of enemies. Therefore, small vertebrate and inverte- erect hairs along the midline of the cephalotho- brate predators must hunt them with caution. rax, which closely approximates the thoracic keel Although a variety of small predators attack or of its model Camponotus sericeiventris. Other specialize on ants, these species are comparatively characteristics of the mimic, such as color, shape rare, and typically use special hunting tactics. and behavior, accentuate the resemblance between Myrmecomorphs that do not attack ants are model and mimic. Many other species-specific almost always found in the same microhabitat as pairs of model and ant mimic have been described their models, but do not associate closely with worldwide. ants, and often show avoidance reactions to them. Experimental evidence in support of Batesian Although little quantitative work has been done to mimicry includes feeding trials in which visually 2536 M Myrmecomorphy oriented predators behave similarly toward model consequence of selection by both ants (Wasman- and mimic. For example, in a study on the ant- nian mimicry) and by visually oriented preda- mimetic plant bug Coquillettia insignis in north- tors (Batesian mimicry). eastern Oregon (USA), both the jumping spider papenhoei and the assassin bug Sinea diadema accepted non-mimetic plant bug prey Aggressive Mimicry significantly more often than the ant-mimicCoquil - lettia insignis, while their behavior toward the Ants represent an abundant and conspicuous model ant Formica fusca and toward the mimic source of protein for potential predators, and was indistinguishable. In addition, the assassin bug many ant species care for other insect species, Siadema diadema was able to learn and remember from which they extract nutrients. These features unpleasant experiences with the ant model. While attract a considerable diversity of arthropod about half of the field-collected specimens of this predators, and among these predators are some assassin bug attacked the ant-mimic Coquillettia of the more remarkable examples of aggressive insignis, after close confinement with the ant For- ant-mimicry. Aggressive mimicry differs from mica fusca, individual assassin bugs that had previ- Wasmannian mimicry in that aggressive mimics ously attacked C. insiginis were significantly less do not live with their ant models, and typically likely to do so. associate with ants just closely enough to access their resource, either the ants themselves, or their symbiotic associates. Spiders of the genus Wasmannian Mimicry Aphantochilus possess a shiny and granular integument, characters that are thought to facili- Myrmecophilic arthropods that also possess a tate acceptance by their cephalotine ant models, body shape or texture that closely resembles which are their only source of food. The adult their ant models are called Wasmannian mimics. crab spider Amyciaea forticeps attacks workers Some observers have argued that the body shape of the Oecophylla smaragdina. Under and texture of ant-like rove beetles that associate normal circumstances, the crab spider does not with army ants evolved as a consequence of closely resemble the weaver ant. While hunting, selection by the ants themselves. This view is however, the spider adopts a behavior in which it consistent with the general observation that looks like a dying or struggling weaver ant, and when encountering one another, doryline army other workers often come nearer to investigate. ants and other swarm raiding species antennate The spider then pounces on its prey and quickly the petiolar area of their nestmates, and that the withdraws to a more remote location. Myrme- same behavior performed by a myrmecomor- comorphic arthropods may also have evolved phic rove beetle allows the mimic to function ­ant-like morphology and behavior to gain with the colony as if it were an ant. Yet among access to the Hemiptera that some ants tend for the rove beetles that associate with ants (myrme- honeydew. Several authors have noticed a corre- cophiles), most species that do not resemble ants lation between the distribution of ant-tended occur entirely within the nest of their hosts, aphids and various species of the ant-like plant while all known ant-like rove beetles live with bug . It is widely believed that legionary ants, spending the majority of their ­myrmecomorphy in Pilophorus serves as a tem- adult lives on the surface, exposed to the full porary ­illusion, allowing the plant bugs to closely range of visually oriented predators that accom- approach and seize their aphid prey. pany the foraging raids. Hence, ant-like body Mimicry is very common in nature, and form in some rove beetles may have evolved as a occurs in a bewildering array of plant and Myrmecophiles M 2537 groups. Species that are abundant and ecologically demonstrated that the guests take food from the dominant generally make excellent models in hosts and may even prey upon them. Outstanding mimicry systems, and so it is no surprise that so cases, such as more specialized species, that pass many myrmecomorphic arthropods have evolved the entirety of their life cycle in the nest, may best since ants came on the scene some 100 million illustrate why “nest parasite” is the most com- years ago. Myrmecomorphic species offer abun- monly cited role of social insect symbionts. dant opportunities for exploring ecological and Throughout their lifespan, these myrmecophiles evolutionary aspects of mimicry and can lead to a receive regurgitations from nurse ants tending the deeper understanding of related fields, such as ant ant larvae, and in the process, drain the resources social organization, systematics, and predator-prey that would have otherwise gone to the host ant relationships. larvae. The larval myrmecophile also preys upon  Ants the ant larvae, even in the presence of the nurse  Mimicry ants. Nonetheless, many myrmecophiles may not  Myrmecophiles be solely parasitic on the hosts. More highly adapted species may even provide benefits to their host col- onies for at least part of their life cycle, possibly References indicating that they are mutualistic with the hosts. A great number of taxa have evolved Edmunds M (1974) Defence in . Longman, Essex, myrmecophilous lineages. Mites (Acarina), beetles United Kingdom, 357 pp (chiefly Staphylinoidea), flies (Phoridae) and a few McIver JD, Stonedahl GM (1993) Myrmecomorphy: morpho- logical and behavioral mimicry of ants. Annu Rev Ento- other soil-dwelling insect species have the most mol 38:351–379 myrmecophilous species and are also the most Oliveira PS (1985) On the mimetic association between abundant. Myrmecophiles are found living in nests nymphs of Hyalymenus spp. (Hemiptera: ) and of nearly every species of ant. Colonies that are ants. Zool J Linn Soc 83:371–384 Reiskind J (1970) Multiple mimetic forms in an ant-mimicking larger and more persistent at maturity, such as clubionid spider. Science 169:587–588 army and driver ants, have more species and indi- Wickler W (1968) Mimicry in plants and animals. World Uni- viduals of myrmecophiles than smaller mature versity Library, London, England, 255 pp colonies, such as ponerine and dacetine ants. Addi- tionally, the species found in larger colonies tend to be more specialized than are those living with Myrmecophiles ants that have smaller, less permanent colonies. Irrespective of the type of colony, the total relative James A. Danoff-Burg abundance of myrmecophiles is low, often on the Columbia University, New York, NY, USA order of 1:5,000 ants. Myrmecophiles are found in nearly every area of the nest including the refuse One of several types of social insect symbionts, middens, foraging columns, brood chamber and myrmecophiles are animals that live with ants for the queen chamber. A single species typically spe- at least part of their life cycle. Other similar sym- cializes in one of these niches within the nest. bionts are termitophiles (guests of termites), melit- tophiles (guests of bees) and sphecophiles (guests of wasps). Of these, myrmecophiles and termito- Ecological Categories philes are the most abundant, species-rich and morphologically diverse. Myrmecophilous species generally play one of All of these social insect symbionts are thought three consistent roles in the nests of the ants. to be nest parasites. Many previous studies have Symphilic species, the best integrated into the host