ISSN 20790864, Biology Bulletin Reviews, 2015, Vol. 5, No. 4, pp. 353–365. © Pleiades Publishing, Ltd., 2015. Original Russian Text © N.S. Morozov, 2015, published in Uspekhi Sovremennoi Biologii, 2015, Vol. 135, No. 1, pp. 97–112.
Why Do Birds Practice Anting? N. S. Morozov Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, pr. Leninskii 33, Moscow, 119071 Russia email:
[email protected] Received July 31, 2014
Abstract—Anting is the application of ants or “substitutes” of ants by birds to their plumage. The earliest sci entific reports concerning this behavior appeared in the early 19th century, but the targeted collection of facts began in the late 1930s. As a result, anting has been recorded (in nature or/and in captivity) on all but one continent for more than 200 bird species of several orders, mostly passerines. “Active” and “passive” antings are usually recognized as the two main types of this procedure. In the active procedure, birds take ants with their bill and directly smear their feathers. Other manifold (several dozen variants) living and nonliving objects are also used for active anting. The birds practicing passive anting visit ant colonies, provoke ants to attack, and allow them to pass through their plumage. For a given type of anting, the procedure consists of stereotypic movements and postures. Ants belonging to the subfamily Formicinae (mostly Formica, Lasius, and Camponotus), which spray or exude formic acid in attack and defense, are predominantly used, whereas Dolichoderinae and Myrmicinae take second and third places, respectively. Although anting can be studied by manipulative experiments with captive birds, the functions of this behavior remain unclear. It has been sug gested that anting acts as way of (1) ridding of ectoparasites, (2) feather grooming, (3) decreasing skin irrita tion during molt, (4) food preparation (removing pungent effluents from ant bodies before eating them), (5) sensory selfstimulation, etc. However, convincing support for any of the hypotheses is still absent. Keywords: anting, birds, ants DOI: 10.1134/S2079086415040076
INTRODUCTION The role of ants in land biocenoses can hardly be overestimated. Their high level of social organization not only destined their role as edifiers but also deter mined the exclusive richness and uniqueness of their ecological relationships (Dlusskii, 1967, 1981; Zakharov, 1978, 2004; Hölldobler and Wilson, 1990). It is widely known that ants use plant substrates for nest construction and feeding; they are most impor tant in forest protection against phytophagous insects and seed dispersal (myrmecochory); they compete with other predatory arthropods, are involved in tro phobiosis with aphids and other sapsucking insects, cohabitate with many other arthropod species in ant hills (myrmecophily), and, finally, are food for some vertebrate animals. This familiar set of facts overshad owed the information on smallerscale and more “optional” (yet no less interesting) relationships in which the ants are “voluntarily or involuntarily” involved. This review considers one kind of such cen otic relationship known as anting (Dubinin, 1951, 1956; Formozov, 1976; Anglorusskii…, 1993; Smirnov et al., 2014). Anting (German, Einemsen) is a bird behavior pat tern rarely observed in wildlife that consists of using ants for “grooming” the feathers and possibly skin (Stresemann, 1935b; Ali, 1936; McAtee, 1938; Chish
olm, 1944; Dubinin, 1951; Simmons, 1957, 1966, 1985; Whitaker, 1957; Querengässer, 1973; Clayton et al., 2010). This phenomenon has been described for over 200 avian species (Simmons, 1966; Moyer and Clayton, 2004; Clayton et al., 2010) or even over 250 spe cies (EcoBirds, Anting, http://birds.ecoport.org/Behav iour/EBanting. htm) belonging to several orders, mostly passerines (Passeriformes). “Active” or “direct” and “passive” or “indirect” anting proce dures are usually recognized as the two main types of this behavioral pattern. In the active procedure, birds take ants with their bill and directly rub their feathers. Other living and nonliving objects (several tens of variants) are also used for active anting. The birds practicing passive ant ing visit ant colonies, provoke ants to attack, and allow them to pass through the plumage. The division of ant ing into active and passive types cannot be regarded as absolutely strict, since some species practice both pro cedures; moreover, individual representatives of the genera Turdus (thrushes) and Corvus (ravens) may combine these types within one procedure (Simmons, 1957; Querengässer, 1973; Wiles and McAllister, 2011). Finally, some species practice a kind of “inter mediate” anting procedure that formally belongs to a passive type (see the section Passive Anting). These facts indirectly suggest that similar causes underlie these two anting types and their “relatedness.”
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HISTORICAL BACKGROUND Many known naturalists and scientists have shown interest in anting. According to the reference lists of some European authors, the first mentions of this phe nomenon appeared at the turn of the two first decades of the 20th century. However, that is not the case. The earliest scientific communications on this bird behav ioral pattern date back to the second quarter of the 19th century and refer to birds of the New World (McAtee, 1938; Chisholm, 1944; Whitaker, 1957). It should be said that the first of such communications by Audubon (1831), an outstanding American ornitholo gist and animal painter, reported that wild turkey (Meleagris gallopavo) juveniles “wallowed” in already abandoned ant hills, which presumably refers to another type of grooming their feathers—dusting or dustbathing. Audubon himself explained this behav ior by the fact that the substrate where ants lived was “unbearable” for avian ectoparasites. The second instance is found in a manuscript about the birds of Jamaica by Gosse (1847), a British naturalist. Accord ing to the words of a third party, he mentions that greater Antillean grackles (Quiscalus niger), while col lecting the lime fruits fallen from a tree, fly up to branches, where they rub the wing lower surface with one and then the other leg (?). Frazar (1876, cited according to McAtee, 1938) observed how ants directly removed ectoparasites during a passive anting of a tame crow. The activities of Chisholm, an Australian journal ist, encyclopedist, author of several books about wild life, editor of the journal Emu, and amateur ornithol ogist who was later elected a Fellow of the Royal Aus tralasian Ornithologists Union, considerably expanded the scope of those interested in the phenom enon of anting. Since the year of 1927, he collected information, including oral and newspaper reports by amateur observers, mentioning this unusual handling of ants by birds (Chisholm, 1944). For example, some readers in the Nature notes of The Daily Telegraph (Sydney) expressed the opinion that birds used ants as a deterrent against ectoparasites. Another observation of this kind, published in The Argus (Melbourne) in 1934, was by a 12year old boy, who was drawn away from his play by the strange behavior of common star lings (Sturnus vulgaris). Chisholm not only discussed such cases with experts (for example, Clark, an Aus tralian myrmecologist) but also published several brief notes in Australian and British newspapers. In 1938, he also organized a BBC broadcast, which attracted the attention of many amateurs to this phenomenon. In 1934, Chisholm published a book titled Bird Wonders of Australia, which described the mysterious manipulations of birds with ants (Chisholm, 1934). Next year, Stresemann, a leading German ornitholo gist, responded to this book, writing about a note by Heine (1929) that had appeared five years earlier titled
“Crows Use Ants to Repel Ectoparasites.” Heine described the behavior of hooded crows (Corvus cornix), which tramped in the early spring with par tially unfold wings and tails on the dome of a wood ant hill. Having noticed a strange “use” of ants by starlings in Chisholm’s book, Stresemann proposed that Ger man ornithologists share information about similar cases in the Ornithologische Monatsberichte (Strese mann, 1935a). His initiative brought about several pages of communications (Stresemann, 1935b). It is important that the earlier records (since 1911), which had not been appropriately discussed before, were also in demand. The observations of captive birds, in par ticular, tame birds, demonstrated that they used for this propose not only ants but also manifold objects, including cigarette butts and beer (Ali, 1936; Chish olm, 1944). Initially, Stresemann was inclined to the version of feather treatments against ectoparasites but a year later discarded it in favor of another explana tion, which is considered below. He was the first to propose the term Einemsen (in German) for this phe nomenon, considering it also applicable when birds manipulated with ant “substitutes” (Stresemann, 1935b). Ali (1936), an Indian ornithologist and a pupil of Stresemann, introduced the English equivalent, anting. Thus, a surge of interest in this behavioral pattern marked the period from the late 1930s through the 1950s. The cases of anting in wildlife were recorded in all the continents but, naturally the Antarctic, as well as in some islands (Gosse, 1847; Ali, 1936; Chisholm, 1944; Dubinin, 1951; Sick, 1957; Simmons, 1957; Whitaker, 1957; Fushihara, 1959; Harwin, 1959; Craig, 1999; etc.). The first records on African (Millar, 1944; cited according to Harwin, 1959) and South American (Sick, 1957) birds appeared rather late. Most of such communications have come and con tinue to come from Western Europe and North Amer ica, since many professional ornithologists and ama teur birdwatchers live there. The specialists were immediately attracted by the fact that anting could be observed not only in wildlife but also in captive birds (which is much easier) once they were provided with ants or their substitutes (Adlersparre, 1936; Ivor, 1943, 1956; Goodwin, 1951; Poulsen, 1956; Simmons, 1957, 1966; Whitaker, 1957). However, Simmons (1957) soon had to caution against a direct extrapolation of the observations in captivity for wildlife conditions. Among other things, individual abnormalities in this behavior may be espe cially characteristic of tame birds. By the mid1950s, approximately 250 sources dis cussed anting in some form or other (Whitaker, 1957). Anting already at that time had been observed in at least 148 avian species (including 65 representatives of the New World); of them, 132 species were passerines. Many papers published photos of the birds practicing BIOLOGY BULLETIN REVIEWS
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anting (Ivor, 1943, 1956; Dubinin, 1951; Löhrl, 1956; Poulsen, 1956; Simmons, 1957, 1966; Whitaker, 1957). The list of used ants comprised 24 species. In addition, over 40 other objects used at least once as an ant “substitute” were known (Whitaker, 1957). In a decade, the list of passerines practicing anting exceeded 210 species belonging approximately 40 families and subfamilies (Simmons, 1966). Initially, Russian and Soviet authors were not men tioned in the corresponding reviews published abroad (Simmons, 1957; Whitaker, 1957) and not only because of the notorious language barrier. Our zoolo gists actually had not written anything about anting until the middle of the last century. Some data that could be associated with this behavior were rather unclear. In particular, Shul’pin (1936) reported that hazel hens (Tetrastes bonasia) in the Ussuri taiga fre quently used ant nests for dustbathing because of a deficiency in appropriate sites but did not specify whether the ant hills were inhabited. The review on anting by Dubinin, a parasitologist, in the first part of his review on feather mites directly stated that the phenomenon of anting had not been reported in the domestic literature (Dubinin, 1951, p. 207). However, he described there his own previ ously unpublished data. In the summer of 1943 in Transbaikalia, he shot four Blyth’s pipits (Anthus godlewskii) that had caught wood ants and rubbed their wing feathers with them for 20–40 min. A consider able amount of ant internal fluid and fragments of their body chitin were found on these feathers. The feathers had a strong smell of formic acid, which still remained 12 h after shooting. The number of ants found in the stomachs of all birds and bills of two indi viduals almost coincided with the number of picked insects. Totally, 732 Alaudicola bilobatus (Rob.) feather mites were harvested from these pipits, and 12% of them were dead. The remaining mites dis played an increased motility, with many individuals moving to the upper covert feathers of the wings. In 12 h, quarter mites also died followed by several other individuals. Four additional pipits that did not prac tice anting were shot for the control. The mites on their wing feathers stayed quiet. Totally, 758 mites of the same species were harvested from the control birds to monitor their fate in an analogous manner. The comparison demonstrated that over third feather mites harvested from the pipits died over 24 h after anting versus 0.9% in the control. In September of 1944 in northern Tajikistan, Dubi nin observed two hoopoes (Upupa epops) that came repeatedly during the day to the outlet of an under ground nest of Messor sp. harvester ants. Each time the birds picked up ants with their bills, put their heads under one wing and then the other, and froze for 1.5– 2 min; the overall procedure took 40–60 min. Only once did one of the hoopoes, after being in such a pos BIOLOGY BULLETIN REVIEWS
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ture several times, rub its bill over the internal part of its wing feathers. Minute drops of ant secretion were detected on the feathers of harvested birds and the majority of the feather mites, which Dubinin at that 1
time identified as Pterolichus cuculi subsp., were mov ing. However, the mites collected in tubes did not mas sively die: only 1.7% of the mites died over 12 h versus 0.9–1.2% in the control. Finally, two Eurasian jays (Garrulus glandarius from the neighborhood of Lenin grad (September 1945) and Ussuri taiga (July 1946) were examined after they one by one picked wood ants sitting on their paths and applied them to the inner surface of the wing feathers. However, no significant differences in the localization of the feather mites Proctophyllodes glandarinus (Koch) were observed between these and other birds. In another part of his review, Dubinin (1956) cited the data on anting by grouses observed by Formozov in the Yaroslavl oblast in the first half of the 1950s and commented on them. This review by Dubinin entailed the communication titled “A Russian Contribution to Anting and Feather Mites” by Kelso and Nice (1963) in The Wilson Bulletin, an American ornithological jour nal. The authors regarded the increased mortality rate of the feather mites harvested from Blyth’s pipits after anting as the first published evidence that the proce dure was fatal to the parasites of this group. This case is also referred to in the current foreign reviews, some times with an indication that this nonetheless cannot be regarded as an example of a strict testing (Craig, 1999; Weldon and Carroll, 2006; Clayton et al., 2010). In addition, the observation of hoopoes was not the first instance of recorded anting by this species, or by representatives of the order Coraciiformes in general (Kelso and Nice, 1963), to which the hoopoe was ascribed at that time. The essay on the grouses by Formozov, which was first published after his death in the collection of his selected works, contains a fascinating mention of ant ing (Formozov, 1976, pp. 191–192): “At the end of April, when thawed patches appear in forest in the open sites, hazel grouses find large ant hills. The wood ants (Formica rufa L.) in warm days come out to the thawed tops of their constructions, still half in snow. Having noticed slowly swarming ants, a hazel hen, fol lowed by a male, sits down onto the ant swarm and enthusiastically starts ‘anting.’ This term was long ago accepted by foreign ecologists but is almost not used in 1 Dubinin
later affiliated the mites Pterolichus cuculi subsp. col lected from the hoopoes in 1944 with the species Coraciacarus cuculi (Megn. et Trt.). This is evident from the list of synonyms with references to the papers preceding the C. cuculi description (Dubinin, 1956, p. 231). However, the hoopoe is absent in the list of birds hosting this mite, which is given later in this publica tion (pp. 237–238). The current data on the host specificity of mites suggest a high probability of an incorrect identification. The mites harvested from hoopoes, which most likely belonged to Epoplichus atelus Gaud, 1981 (S.V. Mironov, oral communi cation, November 2013).
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this country, although it is known to parasitologists (Dubinin, 1956). ‘To ant’ means to force the ants recently out of diapause to protect themselves from an ‘attack’ by spraying bird’s feathers with their secretion, referred to in the vernacular as ‘formic acid.’ This par ticular ‘acid’ frees a hazel grouse from the feather mites that parasitize its wing feathers and especially irritate them in spring. Black grouses also practice ant ing in late April–early May but use the nests of awak ened wood ants on the thawed patches of the forest margins already heated by sun Interestingly, I have observed this phenomenon only in the early spring, when awakened ants do not yet bite but lavishly spray their secretion. It is easy to see this by patting the ‘black hat’ of revived ants and then smelling a pleasant and strong odor of formic acid.” ACTIVE ANTING Birds, as a rule, do the anting procedure on the ground or cage floor but sometimes on a “roost site,” for example, a branch or a perch. Most species apply ants to the lower surface of wing feathers, mostly, the outermost remiges. Usually, a bird then sticks out its wings, which are slightly unfolded and lifted, touching the ground by the ends of the wing feathers, and very quickly applies the ant in its bill to the lower feather sur face rubbing from its base to the top. In some cases, the bird may “spin in place” (Anting activity, http://www. youtube.com/watch?v=b8ldqV47i0). The tail is usu ally “rolled” under the body and directed either for ward or to side of the stretched wing. The tail is usually either between the legs or at the side, frequently mak ing the bird lose its balance, sometimes toppling to a side or even backward. In the manipulations with rub bing the wing feathers, it frequently seems that the bird also applies the ant to its tail feathers; however, this is mainly an optical illusion. In fact, the lower tail sur face, mainly the outermost rectrices, are sometimes rubbed but much rarer than it seems. Some species, mainly Corvidae, Icteridae, and Dicruridae, also smear with ants some other body sites, for example, the tail coverts and the feathers around the vent, on the breast, and shoulders (Ivor, 1943; Goodwin, 1953; Poulsen, 1956; Simmons, 1957, 1966, 1985; Whitaker, 1957; Hauser, 1973; Lunt et al., 2004). Most frequently, birds take only one ant in their bill, which can be either immediately smashed or ini tially remain intact. The bird, as a rule, only once rubs the feather with an ant; in some cases, the ant is used several times but very rarely more than thrice, and then the ant is replaced by a new one (Ivor, 1943; Poulsen, 1956; Lunt et al., 2004). It is known that some species, for example, the redbilled leiothrix (Leiothrix lutea), family Timaliidae, or the blue jay (Cyanocitta cristata), hold an ant with the bill at its thorax and its abdomen free (Simmons, 1966; Eisner and Aneshansley, 2008). Some avian species can manipulate several ants and even a “ball” of crushed ants. For example, starlings
tend to collect a full bill of ants as the procedure progresses (Poulsen, 1956; Simmons, 1957, 1966; Whitaker, 1957). However, observations in captivity suggest that this specific feature appears in young star lings approximately at the age of 2 months, and they apply only single ants before this, during their second month of life (Querengässer, 1973). In an active anting procedure, the movements may be so fast that an “inexperienced” observer can notice nothing unusual, taking anting as ordinary feather cleaning. The large number of inaccuracies in descrip tions of anting procedure is explainable by this (Sim mons, 1957). Some species, for example, the orchard oriole (Icterus spurius), strictly speaking do not rub an ant along the feather but several times quickly touch it with the bill in repeated series with vibrating move ments of their head (Whitaker, 1957). In individual cases, the bird applies the ant in the bill to a certain site of its feather and keeps it there for 1–2 min (Groskin, 1943; Dubinin, 1951). The used ants are either eaten or thrown away. An active anting procedure usually takes several minutes to half an hour; however, longer episodes with short intervals have been observed, including proce dures exceeding 1 h (Simmons, 1957; Whitaker, 1957). Birds can practice anting both alone and in groups, usually with a few individuals. However, groups of concurrently anting starlings may reach ten and a half birds (Chisholm, 1944). Once a group of at least 19 yellowshouldered blackbirds concurrently anting for 8 min was observed in Puerto Rico (Post and Browne, 1982). The majority of species practicing anting follow an active strategy. As has been mentioned, an active variant of the manipulations with the socalled ant substitutes is also referred to as anting. The birds smear their feathers with representatives of some other invertebrate groups, for example, the garlic snails Oxychilus alliarius (Miller), amphipods, millipedes, dermapterans, cat erpillars, grasshoppers, hemipterans, mealworm (Tenebrio molitor L.) larvae, and wasps. The leaves and flowers of several plants can be also used as ant substi tutes, as well as some fruits and fruit juices, especially citruses; walnut shell juice; bulb onion; mustard; vin egar; cucumber brine; hot chocolate; soap suds; beer; tobacco products, including burning cigarettes; burn ing or fuming matches; and some chemicals, for example, naphthalene (Ali, 1936; Dubinin, 1951; Simmons, 1957, 1966; Whitaker, 1957; Clark et al., 1990; Clayton et al., 2010). A video record (Strange behavior in grackles, http://www.youtube.com/ watch?v=yfQbqyYXHjo) shows several common grackles (Quiscalus quiscula), North American passe rines with a size of a large thrush belonging to the ict erid family, rubbing their feathers with large mothballs scattered over the yard to repel skunks. Common grackles are likely to be the champions in the number of individuals jointly practicing the anting procedure employing ant “substitutes.” This was BIOLOGY BULLETIN REVIEWS
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observed in the United States, in southern Pennsylva nia in the suburb of Lancaster. The substitute was the juice of young walnut (Juglans regia) shells; the grack les applied it year after year for a considerable part of summer. The birds separately sat on “bunches” of hanging nuts, punched the shells with the bill, extracted the juice, and immediately smeared the juice over their feathers. The number of participants of such “parties” could simultaneously reach 20–30 individu als (Groff and Brackbill, 1946). Tame birds have become the “heroes” of several curious episodes. Perhaps the most amazing was the episode with a handreared common magpie (Pica pica) recorded in the United Kingdom. It would get a full bill of ants, seat itself on the shoulder of some per son smoking a pipe, place the bill with ants into the hot ash in the bowl of the pipe, and apply the resulting mixture to under its wings (Chisholm, 1944). A video record on the Internet, accessible in the beginning of 2014, shows a common starling that in the kitchen or in the bathroom “smeared” bubbles of tap water into its wing feathers with the movements characteristic of an active anting (http://www.youtube.com/ watch?v=w4VMuJVrrIM). In the class of birds, almost exclusively passerines practice active anting; however, there are observations that active anting is also used by the scaled quail Cal lipepla squamata (Thomas, 1957); two species of the trumpeter, Psophia crepitans and P. leucoptera (Parkes et al., 2003); the hoopoe (Dubinin, 1951); and several species of the order Piciformes (Whitaker, 1957; Hauser, 1973; Wiles and McAllister, 2011). According to these observations, the trumpeters applied diplo pods to their feathers and the remaining nonpasserine species used ants. However, some known experts “deny” the ability of nonpasserine birds to practice anting in any form (Simmons, 1957, 1966, 1985), as is detailed below. Such an active procedure, both with substitutes or ants, is sometimes referred to as anointing rather than anting (Weldon and Carroll, 2006). However, the use of fuming matches or burning cigarettes (see the last episode at The anting, tingling or bathing of ants by the birds, http://www.youtube.com/watch?v= 98_UlErwM5Y), as well as open flame (Simmons, 1957), may be an “intermediate link” between anting and another related behavioral pattern referred to as “smoke bathing” (Whitaker, 1957). Not only birds, but also mammals, mostly pri mates, practice anointing. The consolidated list of objects they use for this purpose is rather long; some cebid monkeys use ants (Weldon and Carroll, 2006; Lynch Alfaro et al., 2012; Jefferson et al., 2014). Thus, the term anting is formally applicable to birds only, although this is only a remote analogy between the behavioral patterns of representatives belonging to two classes (Simmons, 1966). The cebid monkeys, as well as night monkeys (family Aotidae), practice not only selfanointing or individual/solitary form of furrub BIOLOGY BULLETIN REVIEWS
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bing but also social anointing or a social form of fur rubbing with ants, diplopods, other invertebrates, some parts of plants including fruits, and some soil types. In the last case, two or several conspecific indi viduals are in close contact and rub against one another while anointing their fur (Leca et al., 2007; Lynch Alfaro et al., 2012; Jefferson et al., 2014; Mon key medicine at living links in Edinburgh Zoo, http:// www.youtube.com/watch?v=I5TDlG441gA). PASSIVE ANTING In a passive anting procedure, birds stay, hover, and wander on an ant hill or squat upon it, pressing their tail and wings, “floundering in ants.” They pass their bill and head along different parts of the plumage, including the wing feathers, as if provoking ants to attack or smearing something, removing ants from individual body parts, especially legs, from time to time (Crow anting, http://www.youtube.com/watch?v= IcRgjUaK4RA; http://www.youtube.com/watch?v= LoDvLsk6C5g,NR=1,feature=endscreen; http:// www.youtube.com/watch?v=SJaiHorf8qI). The attempts of ants to run on the bird’s head are usually prevented by energetically shaking. Among the passe rines, a passive anting has been mainly observed among the robins (genus Turdus) and Corvus ravens and less frequently, in other birds, such as the family Estrildidae, common starling, and house sparrow (Passer domesticus), which usually practice active ant ing (Simmons, 1957, 1966; Whitaker, 1957; Querengässer, 1973). Most of the procedures inter preted by observers as anting and recorded in compar atively a few nonpasserine birds (Whitaker, 1957; Craig, 1999) are regarded as a passive anting variant (see Taxonomic Composition of the Birds Practicing Anting). Related species may practice different types of ant ing procedure, which is especially pronounced in the family of corvids. Some representatives of this family practice active anting; some practice passive; and some, as is mentioned above, combine both anting types. Finally, the set of actions practiced by another three species—the jay, common green magpie (Cissa chinensis), and redbilled blue magpie (Urocissa eryth rorhyncha)—is so peculiar that it is sometimes regarded as a variant of the passive procedure or even an individual “intermediate” anting type (Goodwin, 1951, 1953; Löhrl, 1956; Poulsen, 1956; Simmons, 1957). After a bird finds itself among a swarm of ants, it spreads and stretches forward both wings at once (not in turn, as is characteristic of most species prac ticing active anting) and “sits down” on its tail, attracting the insects to come. The wings spread for ward are quivering (Goodwin, 1953; Simmons, 1957). Along with the other gestures, the bird from time to time passes its bill down along the inner edges of the primary and secondary feathers, similar to the “true adherers” of an active procedure. However, it has no
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ant in its bill. The bird allows the ants to freely migrate over the body (see photos in Löhrl, 1956; Simmons, 1957; Morozov, 2014; Jay being attacked by ants, http:// www.youtube.com/watch?v=314HtWIOps). Inter mediate anting is practiced not only by individual cor vid species but also by some members of the family Estrildidae (Simmons, 1966), as well as the Japanese gray thrush Turdus cardis (Fushihara, 1959; Simmons, 1966). STEREOTYPIC CHARACTER OF BIRD BEHAVIOR The set of movements and postures characteristic of each anting type is rather stereotypic. On the other hand, individual (groups of) species have evident “nuances,” for example, the preference of certain ant species or the number of insects in the bill (one or sev eral) manipulated by an “adult” (with formed behav ior) bird (Simmons, 1966). This is innate behavior, which is observed in an individual never taught the behavior, in particular, juveniles (McAtee, 1938; Ivor, 1943; Miller, 1952; Poulsen, 1956; Simmons, 1957; Whitaker, 1957; Querengässer, 1973; Eisner and Ane shansley, 2008). In birds that have no such experience, this pattern can be “triggered” with the help of certain olfactory stimuli, first and foremost, the odor of for mic acid. However, it is likely that they learn to visually perceive ants (and substitutes of these insects) as appropriate objects for anting during individual devel opment (Simmons, 1966). Many observers get the impression that birds enjoy anting sometimes to the state of ecstasy. However, this state is accompanied by a transient decrease in caution and aggressiveness (Ivor, 1943; Whitaker, 1957; Sim mons, 1966). The pleasure of this procedure is the par ticular factor sometimes used to explain why birds in the process usually draw their nictitating membrane across the eyes more frequently or for a longer period (Simmons, 1957; Whitaker, 1957; http://www.you tube.com/watch?v=IcRgjUaK4RA; http://www.you tube.com/watch?v=LoDvLsk6C5g,NR=1,feature=end screen; http://www.youtube.com/watch?v= SJaiHorf8qI0). On the other hand, the assumption that this serves to protect the eyes against chemicals is no less convincing (Poulsen, 1956; Simmons, 1957; Whitaker, 1957). The opinions of different researchers on the com bination of anting and other feather grooming prac tices are contradictory. Some of them emphasize that anting is followed by preening or waterbathing, whereas other deny such association (Simmons, 1957, 1966; Whitaker, 1957; Querengässer, 1973). TAXONOMIC COMPOSITION OF THE BIRDS PRACTICING ANTING For some reason, the species practicing anting are most nonuniformly distributed between families, even
among the order Passeriformes. This behavioral pat tern is (almost) untypical of many families, such as Hirundinidae, Alaudidae, Laniidae, Sylviidae, Paridae, and Sittidae. Anting is to the highest degree characteristic of Corvidae, Sturnidae, Icteridae, Frin gillidae, Ploceidae, Turdidae, and Timaliidae; how ever, this phenomenon has not been observed in all species (Simmons, 1957, 1966; Whitaker, 1957). Spe cies such as the common starling, blue jay, common jay, hooded and carrion crows (Corvus cornix and C. corone), common grackle, American robin (Turdus migratorius), and northern cardinal (Cardinalis cardi nalis) are recordholders among the enthusiasts of anting (Whitaker, 1957; Hauser, 1973). In addition to passerines, anting has been observed in solitary or a few species of the orders Falconiformes, Galliformes, Gruiformes, Columbiformes, Psittaci formes, Strigiformes, Coliiformes, Upupiformes and Piciformes. Both types of anting have been described for the hoopoe (Dubinin, 1951; Craig, 1999) and northern flicker Colaptes auratus (Wiles and McAllis ter, 2011). The members of Columbiformes, Psittaci formes, several species of Piciformes, one species of Galliformes, and two species of Gruiformes practice active anting; as for the remaining orders (including several species of Galliformes and one species of Grui formes), they practice passive anting (Dubinin, 1956; Whitaker, 1957; Formozov, 1976; Hauser, 1973; Craig, 1999; Parkes et al., 2003). Some popular science sites on the Internet also mention the anting of individual representatives of Cuculiformes and Trogoniformes. However, recognized experts are skeptical of any information about anting in nonpasserines. In particular, Poulsen (1956) emphasizes that ant hills for Galliformes may be attractive as dustbathing sites rather than anting. He himself failed to “achieve” anting of any of 15 individuals belonging to six species of to the subfamilies Perdicinae and Phasianidae in captivity, although they ate ants every now and then. That is why he put into doubt both the communica tions of American authors on the wild turkey and the data of Reymond (1948) on anting by the black grouse (Lyrurus tetrix), western capercaillie (Tetrao urogal lus), and rock partridge (Alectoris graeca). Analogous reasoning may cast doubt on the passive anting of a tame great horned owl (Bubo virginianus) that was repeatedly seen “bathing” in the material of live ant hills full of ants of unidentified species. The observa tions of this bird were the reason to add Strigiformes to the list of orders practicing anting (Whitaker, 1957). However, Whitaker believed that this opinion was insufficiently grounded. Simmons (1957, 1966, 1985) profoundly mis trusted the reports on anting by any nonpasserines. He noted that all of the specialists (including himself) who studied bird anting in (partial) captivity, which involved an impressive number of individuals and spe cies belonging to different orders and families, observed this phenomenon, at least, in an explicit BIOLOGY BULLETIN REVIEWS
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form, exclusively in the passerines. Simmons (1957) had doubts even about Piciformes, stressing that the information about solitary cases observed in nature did not come from specialists and were most likely explainable by erroneous interpretation of the behav ior of avian species regularly consuming ants, namely, the Eurasian wryneck (Jynx torquilla) and European green woodpecker (Picus viridis), when speaking about British fauna. However, the relevant literature contains data (although not always convincing) on the active anting of several North American woodpecker species (Whitaker, 1957; Hauser, 1973; Wiles and McAllister, 2011). In the context of Poulsen’s opinion, which is shared by Simmons (1957), extracts from the field journal of Formozov of April 9, 1951, as cited by Dubi nin (1956), are of great interest. They describe traces of black grouse “bathing” on the tops of three wood ant hills (p. 80): “The holes are round and rather deep; two of them are with fresh grouse droppings. The hill material is still humid, as is everything around it; thus, there could be no question of a “dustbathing.” Dur ing the period April 9–21, 1953, Formozov frequently found traces of hazel grouse “bathing” in ant hills. According to Dubinin (1956, p. 81), these traces also suggested a true anting, since only one wood ant was found in the crops of 12 harvested hazel grouses, while “on the other hand, macrogfragmental material from ant hills (dry conifer needles, bud scales, branchlets, dried spruce male inflorescences, etc.) is inappropri ate as a “dust” for dust baths, the more so that it was insufficiently dry even at the surface.” WHAT ANTS ARE “APPLIED”? In the majority of cases when the ants used for the procedures were identified to a species or a genus level, they belong to the subfamily Formicinae, mostly of the genera Formica, Lasius, and Camponotus (Brackbill, 1948; Groskin, 1950; Whitaker, 1957; Simmons, 1966; Craig, 1999; Wiles and McAllister, 2011). However, birds on occasion may use other Formicinae. In par ticular, application of the weaver ant Oecophylla sma ragdina Fabricius was observed in India (Ali, 1936) and of Anoplolepis custodiens (F. Smith) and Lepisiota capensis (Mayr) in South Africa (Craig, 1999; Lunt et al., 2004). The Formicinae worker ants have a rudi mentary nonfunctional sting. When defending or attacking, they bite with the mandibles and spray the venom gland secretion, stored in the reservoir, through the acidopore at the abdomen’s end. The secretion is a mixture of formic acid and some other substances with water; the concentration of formic acid is ~50% and does not exceed 65% together with free amino acids and short peptides (Blum, 1992; Braekman and Dal oze, 1996; Revis and Waller, 2004; Torres et al., 2013). Some members of the genus Formica, in particular, the wood ants of the F. rufa group, are able to spray this BIOLOGY BULLETIN REVIEWS
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venom to a distance up to several tens of centimeters from the end of their abdomen extended forward. The key role in emergence of anting in birds is fre quently ascribed to formic acid (Simmons, 1966). However, the list of pungent and toxic substances secreted by various ants in emergency is longer (Sim mons, 1966; Blum, 1992; Braekman and Daloze, 1996; Torres et al., 2013). Presumably, that is why birds sometimes also apply ants that do not secrete formic acid, for example, Dorymyrmex pyramicus (Roger), Forelius pruinosus (Roger), and Tapinoma sessile (Say) from the subfamily Dolichoderinae (Whitaker 1957) as well as Messor sp., M. capensis (Mayr), Monomo rium pharaonis (L.), Myrmecina graminicola nipponica Wheeler, Pheidole megacephala (Fabricius), Ph. mor risi Forel, Pogonomyrmex badius (Latreille), Cremato gaster ashmeadi Mayr from the subfamily Myrmicinae (Dubinin, 1951; Poulsen, 1956; Fushihara, 1959; Hauser, 1973; Craig, 1999; Lunt et al., 2004). Similar to Formicinae, the Dolichoderinae ants lack a functional sting. However, they have anal glands secreting drops of fluid with a specifically smell, which some authors regard as repellents (Simmons, 1966). As for Myrmicinae, the above list contains both nonst inging species or those that rarely use the sting (for example, according to Kugler (1979), the sting of Myrmecina graminicola is too short and poorly scleri fied) and stinging (the last four species). Hauser (1973) has demonstrated that birds in North Carolina frequently apply the last three (stinging) species, mainly, Pogonomyrmex badius, which additionally have a sharp odor. However, birds generally “prefer” Formicinae ants, with Dolichoderinae being the sec ond in the list, while Myrmicinae as a tool for rubbing feathers are frequently rejected, at least, in captivity (Whitaker, 1957; Simmons, 1966; Lunt et al., 2004). It seems that birds in the majority of cases immediately distinguish ants spraying or secreting pungent and “repellent” substances from the remaining ants, including the stinging variants lacking such “weapon.” HOW FREQUENTLY AND IN WHAT SEASON IS ANTING OBSERVED? Thanks to the observations of captive and tame birds, wide differences have been revealed between individuals in anting frequency within some passerine species. Some individuals practice anting on a regular basis, for example, every few days, sometimes for days and several times a day, while others do not practice anting at all or do it very seldom, for example, once in several years (Simmons, 1957; Whitaker, 1957; Querengässer, 1973). There are also some individual specific features in preference of the objects used for anointing. Simmons (1966) believes that these differ ences emerge as a result of a confluence of factors within the life of an individual, the innate response to key olfactory stimuli (first and foremost, formic acid), and the subsequent establishment of individual visual
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patterns of the objects “appropriate” for the proce dure. It is unknown how frequently migrants from high latitudes practice anting during their overwintering in lower latitudes. In the temperate latitudes of the Hol arctic, anting is mainly observable in wildlife during the “warm half year.” This is not surprising at first glance, in light of the absence of migratory birds and the decreased accessibility of ants from the late fall to the beginning of spring. However, warm periods are common, for example, in many North American regions within moderate and subtropical belts; during these periods, ant activity on the surface of their nests is typically rather high. Some birds overwintering there are “worldlevel champions” in active anting, namely, the common starling, blue jay, American robin, and common grackle. Nonetheless, only a few cases of active anting have been observed in several avian spe cies in November, December, and March over this vast area with the large army of amateur ornithologists liv ing there (Whitaker, 1957; Hauser, 1973; Potter and Hauser, 1974; Wiles and McAllister, 2011). It seems as if so few recorded cases of winter anting is explainable not only by the decreased accessibility of ants but also by the weakening of the corresponding motivation in the avian species overwintering in temperate latitudes for reasons yet unknown. This hypothesis agrees with aviary experiments by Ivor (1943) conducted in different months in south eastern Canada involving 73 individuals of 31 avian species belonging to nine families. They also included three European and two Asian species. Over half of these birds were tame, and some were so tame that they did the procedure while sitting on his arm. Four ant species belonging to the genera Formica, Lasius, Cam ponotus, and Tapinoma were used in the experiment. In this set of experiments, 20 bird species displayed an active anting; seven of these species overwintered in wildlife in the south of North America, Central, and/or South America. However, anting in February and March was observed only for eight individuals belonging to two species when “half asleep” ants Cam ponotus pennsylvanicus (De Geer) were placed into aviaries. These species were the Baltimore oriole (Ict erus galbula), overwintering between 30° N and the equator, and the redbilled leiothrix, a South Asian species popular for cage keeping. On the other hand, the majority of birds belonging to different species ate ants during these two months (Ivor, 1943). Whitaker (1957) experimented for two and a half years on the porch and in the yard of her house in Oklahoma with a tame female Baltimore oriole—a species that overwinters in wildlife between the North ern Tropic and equator. The bird practiced anting all year round. Note that the intensity of the procedure varied within individual months of both the cold and warm halves of the year. During the cold season, solitary cases of the use of ant substitutes were recorded. A tame blue jay kept
indoors somewhere in or near Chicago rubbed its feathers with hot chocolate in January and February and with warm soap suds in midMarch (Nice, 1955). It is more difficult to estimate the distribution pat terns of anting episodes in wildlife during the warm half of the year. The available data (Dubinin, 1956; Formozov, 1976; Whitaker, 1957; Hauser, 1973; Potter and Hauser, 1974) fail to give an unambiguous picture and somewhat contradict the conclusions of research ers, which involve data obtained in captivity or semi free keeping. For example, experiments conducted in Canada suggest that the periods of the highest “predis position” to anting of the bird species practicing active anting span from the second half of April to the end of July (Ivor, 1943), while field observations in North Carolina give a period of the end of July–end of Sep tember (Potter and Hauser, 1974). FUNCTIONS OF ANTING: HYPOTHESES Despite the wide possibilities in experiments with birds in captivity, the functions of anting are still vague. As has been assumed (Ali, 1936; McAtee, 1938; Chisholm, 1944; Brackbill, 1948; Groskin, 1950; Dubinin, 1951; Poulsen, 1956; Simmons, 1957, 1966, 1985; Whitaker, 1957; Potter and Hauser, 1974; Craig, 1999; Revis and Waller, 2004), these functions may consist of (1) the prevention from and removal of ecto parasites and undesirable arthropod inhabitants, espe cially mites and plumage lice, as well as fungi and bac teria; (2) better grooming, for example, an increase in saliva secretion during feather cleaning by bill or the removal of “old” grease; (3) the enhancement of vita min D production (which is then swallowed while feather grooming) from the oil gland exposed to sun light; (4) a decrease in skin irritation during molting; (5) the removal of venoms and pungent substances used by insects for attack and defense (primarily, for mic acid) from ant bodies prior to their ingestion in order to decrease the amount of these substances entering the gut (implying that the bird rubs a living ant against a feather in order to stimulate it, causing it to release a considerable portion of such substances); and (6) a pleasant sensation (it is not denied that the pleasant sensation may be combined with a sort of irri tation, for example, something like tickling). When speaking about the decisive role of one of these func tions in the origin and existence of this behavioral pat tern, facts and arguments appear that directly contra dict such an explanation. A hypothesis postulating that this is the way to store live feed (with ants remaining on the plumage) before long flights was also proposed (Chisholm, 1934, 1944; McAtee, 1938; Groskin, 1943, 1950), which caused indignation on the part of Dubinin (1951). Indeed, the different explanations are by no means incompatible. As follows from the historical excursion in the beginning of this review, the hypothesis stating that anting is a method to control ectoparasites, primarily, BIOLOGY BULLETIN REVIEWS
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feather mites and plumage lice, was the very first. This assumption later appealed to many scientists, since it appears to be very reasonable. Some experts in pri mates also believe that fur anointing by monkeys is a tool against ectoparasites (Baker, 1996; Valderrama et al., 2000; Falótico et al., 2007; Leca et al., 2007; Meunier et al., 2008); however, members of this scien tific community also have other hypotheses (Leca et al., 2007; Lynch Alfaro et al., 2012). The fact that almost all objects used “instead of ants” are typically pungent and have a strong odor or, as in the case of invertebrates, are able to release secretions with such properties in critical situations favors this hypothesis (Whitaker, 1957; Clark et al., 1990). For example, different groups of Diplopoda milli pedes, the third in size class (after insects and arach nids) of terrestrial arthropods, possess an impressive “range” of toxins for selfdefense (Parkes et al., 2003; Carroll et al., 2005; Sekulic et al., 2014). Birds using members of this taxa for anointing plumage have been observed in different parts of the world (Parkes et al., 2003), and primates anointing their fur with them have been observed in the New World (Valderrama et al., 2000; Lynch Alfaro et al., 2012; Jefferson et al., 2014). The toxins secreted by Diplopoda (for example, some benzoquinones) may be dangerous not only for ecto parasites, but also for higher vertebrates once these substances enter their bodies. It is assumed that the immdiate benefit of the procedure for the monkeys that use “carriers” of such toxic substances on a regu lar basis for anointing “outweighs” the risk of adverse side effects (Valderrama et al., 2000). Where are the facts that may prove the efficacy of anting in combating bird ectoparasites, besides those of direct mite and lice extraction by ants during a pas sive procedure (Frazar, 1876, cited according to McAtee, 1938) and the aforementioned data by Dubi nin (1951)? Apparently, they are almost absent (Potter and Hauser, 1974; Revis and Waller, 2004; Clayton et al., 2010). According to the studies in captivity, birds that carry a few mites and plumage lice may for long time practice active anting (Poulsen, 1956; Whitaker, 1957). For example, no parasites at all were found on a female orchard oriole over the 3month period of its life before it was studied. Nonetheless, it commenced anointing with ants and infrequently “skipped” such an opportunity in the subsequent two and a half years. For example, at the age of 2 years (June 30–Septem ber 19, 1954), this bird had free access to Dorymyrmex pyramicus (Roger) on the porch and did the procedure during at least 34 of 41 days. The longest period of daily anting was 10 days and the next in duration was 7 days. In general, the durations of the procedure, fre quently reaching 45 min, were reduced in the case of daily access to the ants (Whitaker, 1957). In fact, the birds of the species that practice anting may employ the procedure “for prevention” or only when weakly infested (or not infested at all), thanks to BIOLOGY BULLETIN REVIEWS
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the anting they practiced during the period before a particular observation. In other words, neither a high nor a low infestation rate of the individuals anting at the moment are serious arguments in favor or against an antiparasitic function of anting. As for the results of a few experiments, they actually disfavor this hypoth esis (Clayton et al., 2010; Judson and Bennett, 1992; Revis and Waller, 2004). It has been shown that formic acid applied to human skin at concentrations of 50 and 85% or the secre tion of a South American ant, Camponotus rufipes (F.), which contains this acid and is frequently used by the tufted capuchin (Cebus apella) for anointing, acts as a repellent for the nymphs of ixodid ticks belonging to the genus Amblyomma and its adult individuals. How ever, the effect of ant secretion is weaker as compared with formic acid at the indicated concentrations (Falótico et al., 2007). In the laboratory, the spraying of the plumage lice with 50% formic acid solution kills most of them over 15 min. In order to assess the effect of anting procedure on feather mites and plumage lice under more natural conditions, Bennett and Clayton (Clayton et al., 2010) conducted “an open air” exper iment. They used 32 caught common starlings; each bird was placed into a separate cage with a volume slightly exceeding half cubic meter. The cages were placed on the ground, half (experimental) over the wood ant paths and the other half (control) near the ant paths. The cages lacked a floor, making the ants passing under the cage accessible to birds. The lower cage parts were covered with a Teflon film that the ants could not cross; thus, they were unable to climb the cages and bother birds. The starlings of the experimen tal group frequently used anting, and their plumage by the end of experiment (which lasted three days during the daytime; the birds were removed from cages at night) had a strong odor of formic acid. The control birds deprived of the access to ants rarely tried to per form anting and had no smell of formic acid. One day before the experiment and three days after its completion, each bird was examined for the num ber of mites and plumage lice. The last 3 days were intended for the birds to clean their plumage and for the parasites to return to their preferred plumage sites. All of the found mites belonged to one species, Sturn otrogus truncates (Trouessart), and the lice belonged to four species: Menacanthus eurysternus (Burmeister), Myrsidea cucullaris (Nitzsch), Brueelia nebulosa (Bur meister), and Sturnidoecus sturni (Schrank). Complete data were obtained for 14 starlings from the experi mental group and 11 control birds. Any differences in the counts of feather mites and plumage lice between the groups were statistically insignificant. In other words, anting had no considerable effect on the abun dances of these two arthropod categories (Clayton et al., 2010). Formic acid is not only an insecticide and an acar icide; it also possesses bactericidal and fungicidal properties. It has been assumed that the function of
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anting may consist in the inhibition of bacteria or fungi that are adverse for the bird plumage (Ehrlich et al., 1986). However, experimental application of the extract from ant bodies failed to inhibit these two groups of organisms, unlike pure formic acid (Revis and Waller, 2004). Most likely, formic acid is effective in this manner only at the highest concentrations and under laboratory conditions. However, it has been mentioned that the secretion of Formicinae ants is an approximately 50% aqueous solution of formic acid. The hypothesis on the removal of ectoparasites is also not confirmed by some indirect considerations, such as the following. The number of reports on bird anting evidently differs for individual regions. These variations are in many respects determined by the dif ference in the intensity of ornithological observations but probably not only by this factor. If anting is actu ally a tool for controlling ectoparasites, the number of such reports should also depend on the general risk of infestation, as well as the bird infestation rate in the region. Does it really depend on the climate and local weather? It has been shown that an arid climate is adverse for some plumage lice and bacteria that dam age bird feathers (Clayton et al., 2010). Once anting is directed against these groups of ectoparasites, the reports from dry areas should be less numerous than from the other regions. However, such a trend is at least not evident. Species especially prone to anting practice it under the most variable natural conditions. For example, the common starling, which was long ago introduced to North America, Australia, and South Africa, has not lost the need to rub itself with ants (McAtee, 1938; Chisholm, 1944; Whitaker, 1957; Potter and Hauser, 1974; Craig, 1999; Wiles and McAllister, 2011). In fact, “the anting passion” is not the only exam ple of how quite reasonable hypotheses on the fatal or repellent effects of odorous and pungent substances, which birds “borrow” or secrete themselves for cer tain, still unclear purposes, are not confirmed. In par ticular, the plumage of the crested auklet (Aethia cris tatella), a colonial seabird of the suborder Alcae, has a strong “citrus” scent. As has been shown, the scent comes from saturated and monounsaturated alde hydes with short chains. Some assumptions suggest that this is a tool against arthropod ectoparasites. However, laboratory experiments with two plumage louse species parasitizing the wild pigeon failed to confirm that the volatile substances giving this smell have any harmful effect on these lice, at least over 30 h. Moreover, the abundance of several louse species on the crested auklet was considerably higher (even with a correction for the difference in size) as compared with the least auklet, which nests in the same colony but lacks this smell (Douglas et al., 2005). The absence of any evidence for anting efficacy against ectoparasites supports the interest in other hypotheses (Potter and Hauser, 1974; Judson and Bennett, 1992; Lunt et al., 2004; Eisner and Anes
hansley, 2008). For example, Potter and Hauser (1974) paid attention to the fact while processing data from North Carolina that the active anting frequency increased in the case of high humidity, especially after long or strong rainfalls. Having failed to find any sig nificant infestation with mites and plumage lice in the species practicing anting, they explained the observed pattern by an increase in feather “losses” by molting birds getting wet in the rain. The researchers inferred that anting and sunbathing (sunning) were comple mentary behavioral patterns for decreasing the dis comfort during molting, when birds lost many feathers at once. According to the hypothesis by Potter and Hauser, solar radiation and ant secretions have the same “soothing” effect on skin irritation in birds sim ilar to that of a hot towel or shaving lotion on human skin itch. On the other hand, some experts still believe that sunbathing is also a way to control ectoparasites 2
(Clayton et al., 2010). In addition, the aviary experi ments with the Cape whiteeyes (Zosterops pallidus) captured in wildlife in South Africa over 7 months in general confirmed a positive correlation between active anting and molting but still demonstrated that anting not always coincided with active molting peri ods. Moreover, birds actively employed ants beyond molting periods, although less frequently (Lunt et al., 2004). A hypothesis proposed almost 80 years ago by Adlersparre (1936), a Swedish scientist, unexpectedly found a “second life.” Based on experimental data, he inferred that the purpose of an active anting procedure was to remove the secretion containing formic acid from ant’s bodies before eating them. Stresemann, one of the leading ornithologists of that time, immediately adopted this hypothesis, but Chisholm (1944) cate gorically disapproved it. Later, Simmons (1957) also criticized this assumption. Rather recently, two papers (Judson and Bennett, 1992; Eisner and Aneshansley, 2008) reported new experimental data confirming this hypothesis, which actually implies that birds utilize their plumage as a blotting paper. The evidence is suf ficiently convincing in light of the particular objects of observation (the common starling and Formica rufa L. ants in one case and the blue jay raised in captivity and F. exsectoides Forel in the other), but it unfortunately does not fit many scenarios with other “characters,” for example, those practicing passive procedures. This hypothesis fails to explain numerous episodes when feathers are rubbed with inedible ant substitutes. Finally, by no means does an active anting procedure with ants always end in eating the insect (Chisholm, 2
This opinion is based on the data that birds more frequently “soak up the sun” in hot, rather than chill, weather and heat their plumage to temperatures that can, according to laboratory experimental data, elevate the mortality rate of at least some ectoparasites. In an experiment with a species of American swal lows, application of antimite and antilouse preparation reduced their sunbathing (Clayton et al., 2010).
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1944; Poulsen, 1956; Simmons, 1957, 1966; Whitaker, 1957; Craig, 1999; Lunt et al., 2004). CONCLUSIONS Precisely six decades have elapsed since Julian Huxley, one of the leading figures in the evolutionary synthesis, participated in the discussion on the func tions of anting at the 11th International Ornithologi cal Congress in Basel (Switzerland) in 1954 (Sim mons, 1957) and referred to this behavior as one of the most famous enigmas in ornithology (Sick, 1957, p. 187). However, the question in the title of this review still remains unanswered. The opinion by which anting is akin to such human habits as smoking, drugs, or alcohol addiction—that it is aimed only at selfstimulation and pleasure and has no essential adaptive value—was criticized by Simmons (1966). Simmons emphasized that such a view on a rather widespread and stereotypic phenomenon did not withstand scrutiny from the evolutionary standpoint. As has been mentioned, birds during the anting proce dure frequently lower their guard and even get euphoric, thereby becoming evidently more notice able and vulnerable for predators. It is difficult to imagine that such a behavioral pattern would not be eliminated by natural selection unless it gives, at least in certain situations, some benefits to the correspond ing individuals. It should be emphasized that, although bird anting in captivity has long been studied, even the evident applications of the experimental approach are far from being exhausted. For example, there are no experi ments in which a wider range of ant species and taxo nomic groups, as well as other invertebrates that pos sess different chemical protection tools and delivery routes to “the enemy,” are offered to birds of the same species. ACKNOWLEDGMENTS The author thanks D.I. Berman for his persistent appeal to write this review; A.A. Zakharov for his advice and identification of ants; S.V. Mironov for the data on current names and host specificity of the feather mites mentioned in publications of the 1940s– 1950s; and O.L. Makarova and N.A. Formozov for the indication of some information sources. The work was supported by the Russian Foundation for Basic Research (project no. 110400941a), the program for the leading scientific schools of the Russian Feder ation (grant no. NSh3807.2012.4), and Presidium of the Russian Academy of Sciences under programs “Living Nature: Current State and Problems in Devel opment” and “Problems in the Origin of Life and Development of Biosphere.” BIOLOGY BULLETIN REVIEWS
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WHY DO BIRDS PRACTICE ANTING Reymond, E., Myrmécophilie chez la Perdix bartavelle, Nos Oiseaux, 1948, vol. 19, p. 288. Sekulic, T.Lj., Vujisic, Lj.V., Curcic, B.P.M., et al., Quino nes and nonquinones from the defensive secretion of Unciger transsilvanicus (Verhoeff, 1899) (Diplopoda, Julida, Julidae), from Serbia, Arch. Biol. Sci., Belgrade, 2014, vol. 66, no. 1, pp. 385–390. Shul’pin, L.M., Promyslovye, okhotnich’i i khishchnye ptitsy Primor’ya (Commercial, Hunting, and Raptorial Birds in Primorye), Vladivostok: Dal’nevost. Fil., Akad. Nauk SSSR, 1936. Sick, H., Anting by two tanagers in Brazil, Wilson Bull., 1957, vol. 69, no. 2, pp. 187–188. Simmons, K.E.L., A review of the antingbehavior of pas serine birds, Br. Birds, 1957, vol. 50, no. 10, pp. 401– 424. Simmons, K.E.L., Anting and the problem of selfstimula tion, J. Zool., 1966, vol. 149, part 2, pp. 145–162. Simmons, K.E.L., Anting, in A Dictionary of Birds, Camp bell, B. and Lack, E., Eds., Vermillion, South Dakota: Buteo Books, 1985, p. 19. Smirnov, N.N., Panov, E.N., and Mikheev, V.N., Russko angliiskii i anglorusskii slovar’ po ekologii, etologii i okhotovedeniyu (RussianEnglish and EnglishRussian Dictionary of Ecological, Ethological, and Hunting Terms), Moscow: Librokom, 2014. Strange behavior in grackles. http://www.youtube.com/ watch?v=yfQbqyYXHjo Stresemann, E., Werden Ameisen durch Vögel zum Ver treiben von Aussenparasiten benützt? Ornithol. Monats ber., 1935a, vol. 43, no. 4, pp. 114–115. Stresemann, E., Die Benutzüng von Ameisen zur Gefieder pflege, Ornithol. Monatsber., 1935b, vol. 43, no. 5, pp. 134–138. ˆ
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The anting, tingling or bathing of ants by the birds. http://www.youtube.com/watch?v=98_UlErwM5Y Thomas, J.W., Anting performed by scaled quail, Wilson Bull., 1957, vol. 69, no. 3, p. 280. Torres, A.F.C., Quinet, Y.P., Havt, A., et al., Molecular pharmacology and toxicology of venom from ants, in An Integrated View of the Molecular Recognition and Toxicology—from Analytical Procedures to Biomedical Applications, RádisBaptista, G., Ed., InTech, 2013, pp. 207–222. Valderrama, X., Robinson, J.G., Attygalle, A.B., and Eis ner, T., Seasonal anointment with millipedes in a wild primate: a chemical defense against insects?, J. Chem. Ecol., 2000, vol. 26, no. 12, pp. 2781–2790. Weldon, P.J. and Carroll, J.F., Vertebrate chemical defense: secreted and topically acquired deterrents of arthro pods, in Insect Repellents: Principles, Methods, and Uses, Debboun, M., Frances, S.P., and Strickman, D., Eds., Boca Raton: CRC Press, 2006, pp. 47–76. Whitaker, L.M., A résumé of anting, with particular refer ence to a captive Orchard Oriole, Wilson Bull., 1957, vol. 69, no. 3, pp. 195–262. Wiles, G.J. and McAllister, K.R., Records of anting by birds in Washington and Oregon, Wash. Birds, 2011, vol. 11, pp. 28–34. Zakharov, A.A., Muravei, sem’ya, koloniya (The Ant, Fam ily, and Colony), Moscow: Nauka, 1978. Zakharov, A.A., The ants: life in the forest, in XX Chteniya pamyati V.N. Sukacheva “Nasekomye v lesnykh biogeo tsenozakh” (The XX Conf. Dedicated to the Memory of V.N. Sukachev “Insects in Forest Biogeocenosises”), Chernov, Yu.I., Ed., Moscow: KMK, 2004, pp. 54–82.
Translated by G. Chirikova
