Entomological Review, Vol. 82, No. 5, 2002, pp. 569–576. Translated from Zoologicheskii Zhurnal, Vol. 81, No. 5, 2002. Original Russian Text Copyright © 2002 by Novgorodova. English Translation Copyright © 2002 by MAIK “Nauka/Interperiodica” (Russia). Study of Adaptations of Aphids (Homoptera, Aphidinea) to Ants: Comparative Analysis of Myrmecophilous and Nonmyrmecophilous Species T. A. Novgorodova Institute of Animal Systematics and Ecology, Siberian Division, Russian Academy of Sciences, Novosibirsk, 630091 Russia Received June 21, 2001 Abstract—Behavioral patterns of 4 obligatory myrmecophilous and 4 nonmyrmecophylous aphid species from the families Drepanosiphidae, Aphididae, and Lachnidae were studied in nature in the forest-park zone of the Novosi- birsk Scientific Center in 1998–1999. All these species form no galls. Observations were accompanied by an indi- vidual marking of insects. The behavioral repertoires of myrmecophilous and nonmyrmecophylous species are sig- nificantly different. Defensive reactions are absent in the behavior of obligatory myrmecophilous species. Their be- havior includes only elements of adaptation to trophobiosis; most of these are aimed to attract ants and communi- cate with them. The behavior of nonmyrmecophylous species is more flexible and diverse. It includes some ele- ments of passive defense, from jumping off a plant to demonstration of “aggressive” poses, allowing them, at least partly, to avoid predators. Aphids (Homoptera, Aphidinea) are small insects tubules (siphons), these being reduced in myrmecophi- feeding on plant juices. The group is characterized by lous forms. Moreover, a preanal corolla of hairs, found complicated life cycle, with cyclic parthenogenesis. in myrmecophilous species, helps to keep a honeydew With the environment conditions changing, aphids can drop till the appearance of an ant. In contrast to other develop into apterous or alate morphs and start to re- aphids, many Lachnidae possess a filtration chamber, produce in autumn only. Alate specimens of many producing honeydew with increased sugar content species migrate from one plant to another. At present, (Kunkel and Kloft, 1977). The colony size and aphid a total of about 4400 aphid species are known (Stern fecundity have been compared in colonies with and and Foster, 1996). In spite of their small size, aphids without ants in order to assess advantages of mutual produce a great amount of honeydew (sweet, sugar- relations with ants. Nixon (1951) and Way (1963) rich secretion), which is an important source of carbo- summarized the data obtained and demonstrated that hydrates for ants. In turn, ants defend aphids from the visited colonies are larger: aphids feed more ac- predators. Thus, the trophobiontic relationships be- tively and produce more offspring; the probability of tween these two groups are mutually beneficial. In the death is higher in colonies not visited by ants. character of aphid-ant relationship, aphids are usually divided into myrmecophilous (visited by ants) or non- The attitude of ants to aphids during the first meet- myrmecophylous species. In colonies of myrmecophi- ing depends mainly on the behavior of the latter; this lous species, ants are found virtually permanently; in phenomenon has been mentioned in the literature (Sa- nonmyrmecophylous colonies, ants may be either pre- kara, 1994). However, only separate publications have sent or absent. been concerned with ethological mechanisms of aphid- ant relations; in these papers, the main attention was Trophobiotic relations between aphids and ants paid to the ant behavior (Dlusskii, 1967; Hortsmann, have long attracted the attention of entomologists 1973; Novgorodova and Reznikova, 1996; Reznikova (Mordvilko, 1901, 1936; Grinfeld, 1961; Sudd, 1987; and Novgorodova, 1998). Till now, myrmecophilous Vepsalainen and Savolainen, 1994; Stadler and Dixon, aphids have only been studied in relation to a narrow 1999; Molnar et al., 2000; Yao et al., 2000). However, complex of adaptations to honeydew production; no mainly morphological, anatomical, and physiological differences in behavior between myrmecophilous and characters of these insects have been examined. As nonmyrmecophylous species have ever been exam- known, most nonmyrmecophylous aphids possess long ined. 569 570 NOVGORODOVA Table 1. Trophic plants, number of colonies, and body size of the aphids examined Number Size group, mm Species Trophic plant of colonies small medium large Symydobius oblongus Betula verrucosa 17 0.5–1.0 1.5–2.4 2.6–3.2 Aphis craccae Vicia sepium 14 0.3–0.5 0.8–1.3 1.5–2.2 A. viburni Viburnum opulus 23 0.4–0.6 0.9–1.8 2.0–2.7 Cinara boerneri Larix sibirica 27 0.6–1.0 1.5–3.0 3.4–4.0 Acyrthosiphon pisum Pisum sativum 13 0.8–1.2 1.5–3.5 4.0–5.5 Uroleucon cirsii Tragopogon orientalis 6 0.8–1.0 1.5–3.5 4.0–4.8 Megoura viciae Lathyrus pratensis 6 0.7–1.0 1.5–3.0 3.4–4.0 Hyperomyzus pallidus Sonchus arvensis 10 0.5–1.0 1.2–2.4 2.5–3.0 The behavior of nonmyrmecophylous aphids has myrmecophilous [Symydobius oblongus Heyd. (Dre- been studied mainly in gall-formers (families Horma- panosiphidae), Aphis craccae L., Aphis viburni Scop. phididae and Pemphigidae). The data obtained demon- (Aphididae), and Cinara boerneri H.R.L. (Lachnidae)] strate the complex nature of behavioral adaptations in and four nonmyrmecophylous [(Acyrthosiphon pisum these insects. As a rule, specialized castes of soldier Harr., Uroleucon cirsii L., Megoura viciae Buckt., and aphids, actively defending colonies, are mainly consti- Hyperomyzus pallidus H.R.L. (Aphididae)] aphid spe- tuted by 1st and 2nd instar larvae, and less frequently cies were studied. Representatives of these species live by obligatory or facultatively sterile adults (Aoki, in colonies of several to several tens of individuals and 1977; Foster, 1990). The soldiers commonly use form no galls. All aphid species of the first group are the stylet (proboscis) or special head processes as obligatory myrmecophilous forms, they were never a weapon (Stern and Foster, 1992). Together with found without ants of the genera Formica, Lasius, and defending the colony, soldier aphids clean galls and Myrmica, at least in the area examined. also remove honeydew, exuvia, and dead aphids (Ben- ton and Foster, 1992). Occasionally, nonmyrmecophy- Aphids were watched in daytime (10 a.m.–5 p.m., lous aphids also use other defense methods, such as 30 min for each individual); the total observation time secretion of a viscous material from siphons (tubules) constituted about 250 h). Cosmetic means were used or secretion of the alarm pheromone (Dixon, 1958). for individual marking of aphids. Three samples of Only two possible reactions to danger have been men- different sizes, with 20 specimens each, were consid- tioned for aphids forming no galls: an insect can leave ered for each species examined: small, medium, and its feeding site (crawling to another place of jumping large (Table 1). Preliminarily, insects were measured off the plant) or pays no attention to an irritant. The under a binocular light microscope with the use of an “vigilance” of aphids remained unexamined. However, ocular micrometer (50 specimens of each species); in exposed nonmyrmecophylous species may demon- the field, the aphid body length was estimated more strate rather complex behavioral stereotypes, such as, roughly with the use of sliding calipers or a ruler. The e.g., fight for a feeding site (Foster, 1996). first group included 1st instar larvae, and the last, A comparative analysis of myrmecophilous and adults and 4th instar larvae; the medium group in- nonmyrmecophylous aphid species forming no galls cluded 2nd and 3rd instar larvae. In all, about (i.e., accessible to ants) and dwelling in the same for- 500 aphids were marked. est was made. Individual behavioral repertoire and “vigilance” were examined. The aphid behavior was The following experiments were performed in analyzed in terms of their adaptation to contacts with order to study aphid reactions to environmental sti- ants. muli: (1) Imitation of an ant “asking for honeydew.” MATERIALS AND METHODS Aphid abdomen was stroked with a preparation needle The study was performed in the forest-park zone of and the reaction of the aphid was recorded (100 indi- the Novosibirsk Scientific Center in 1998–1999. Four viduals of each species). ENTOMOLOGICAL REVIEW Vol. 82 No. 5 2002 STUDY OF ADAPTATIONS OF APHIDS 571 Table 2. Reactions of nonmyrmecophylous aphid species to danger in relation to their size Number A. pisum U. cirsii M. viciae H. pallidus Reaction of points S M L S M L S M L S M L 1 Neutral + + – + + – + + – + + – 2 Dropping off a plant + + – + + – + + + + + – 3 Passing to another site + + + + + + + + + + + + 4 “Alert” pose – + + – – + – + + – + + 5 “Frightening” pose – – + – – + – – – – – – 6 Aphid “kicks” – – – – – – + + – + + Size categories: (S) small, (M) medium, and (L) large. (2) Imitation of enemy attack. Ladybirds were put moment of predator attack. The interval of observa- on a plant with aphids and the aphid behavior tions (10 min) was sufficient for ladybeetles or ants to was observed during 10 min. Five adult beetles and reach the aphid colony. The responses of insects to five larvae were placed in two colonies of each spe- danger, arranged in order of their increasing activity, cies. constitute a “vigilance scale,” in which the number of (3) In order to assess the reaction of nonmyrmeco- points corresponds to the serial number (1–6) of a be- phylous species to presence of ants (Lasius niger) the havioral element (Table 2). ants were accurately placed on plants with aphids, and the aphid behavior was observed during 10 min. Five RESULTS colonies of each species were examined, with 10 repli- In all, 16 behavioral elements were distinguished. cations. Eight of these are typical of myrmecophilous, and (4) Vigilance test. Touching of aphid antennae with 12, of nonmyrmecophylous species. The most charac- a preparation needle was used as an irritant. The teristic poses of the aphids examined are shown in the touching was repeated 4–5 times with 30 min inter- graph.