Honeydew Gatherers

From Chapter 13 of The Ants :

A great majority of the members of the three phylogenetically most advanced ant subfamilies, the Myrmicinae, Dolichoderinae, and Formicinae, attend homopterans to some extent. To employ one last term from Wasmann, the ants can be said to have entered into trophobiosis with the homopterans. As trophobionts, the homopterans resemble many of the lycaenid symbionts in a basic way: they obtain their own food and pass some of it on to their hosts. However, unlike the lycaenids that secrete substances from specialized exocrine glands, the honeydew provided for ants by homopterans is an excretion derived from a digestive process (see Plate 17).



When aphids feed on the phloem sap of plants, they pass a complex mixture of nutrients, including sugars, free amino acids, amides, proteins, minerals and vitamins, through their gut and back out through the anus. During this passage the phloem sap changes as some of its components are absorbed and others are converted or added by the aphid (for recent reviews see Ziegler and Penth, 1977; Kunkel and Kloft, 1977; Dixon, 1985; Maurizio, 1985). According to Maurizio, O.2-1.8 percent of the honeydew dry weight is nitrogen and 70-95 percent of the nitrogen are amino acids and amides. The mixture of nitrogen compounds in the honeydew is largely identical to that in the phloem sap. Measurements made on Tuberolachnus salignus by Mittler (1958) show that as much as one-half of the free amino acids are absorbed by the aphid's gut. In a few cases the honeydew contains amino acids which are not present in the phloem sap. Presumably these are metabolic products added by the aphids (Gray, 1952; Ehrhardt, 1962).

By far the largest percentage (90-95 percent) of the honeydew dry weight consists of carbohydrates. Sugars from the phloem sap are partly absorbed or converted, and the diverse mixtures of sugars contained in the honeydew are often species-specific. They usually comprise fructose, glucose, saccharose, trehalose and higher oligosaccharides. Trehalose, which is the blood sugar of insects, composes up to 35 percent of the total sugar amount in the honeydew. Typical honeydew sugars also include the trisaccharides fructo-maltose and melezitose, with the latter making up 40-50 percent of the total sugar. Other sugars detected in honeydew are maltose, raffinose, melibiose, turanose, galactose, mannose, rhamnose, and stachyose. In addition the honeydew contains other classes of substances, including organic acids, B-vitamins, and minerals.

When unattended by ants, many aphids dispose of the honeydew droplets by flicking them away with their hind legs or caudae, or by expelling them through contractions of the rectum or entire abdomen. The honeydew then falls upon the vegetation and ground below. Similar substances are excreted by several other groups of sap-feeding Homoptera, including scale insects (Coccidae), mealybugs (Pseudococcidae), jumping plant lice (Chermidae = Psyllidae), tree hoppers (Jassidae, Membracidae), leafhoppers (Cicadellidae), froghoppers or spittle insects (Cercopidae), and members of the “lantern-fly” family (Fulgoridae). Sometimes honeydew accumulates in large enough quantities to be usable by man. The manna “given” to the Israelites in the Old Testament account was almost certainly the excretion of the coccid Trabutina mannipara, which feeds on tamarisk. The Arabs still gather the material, which they call “man.” In Australia, chermid honeydew is collected as food by the aborigines. Referred to as “sugar-lerp,” up to three pounds can be harvested by one person in a single day. It is no surprise, therefore, to find that ants also gather honeydew of all kinds. Many, perhaps most, species collect it from the ground and vegetation where it falls. But many others have developed the capacity to solicit the honeydew directly from the homopterans themselves.

Most aphid species associated with ants insert their stylets into the phloem of the host plant (Kloft, 1953, 1959a, 1960a,b,c; Kunkel, 1967). Although they can suck up limited amounts of liquid, the aphids appear to depend chiefly on the turgor pressure of the phloem, which forces sap up their stylets (Mittler, 1957; Kunkel and Kloft, 1985). To process a large volume of phloem sap and discard the excess as honeydew evidently costs the aphid fewer calories than a more nearly total extraction from smaller quantities of sap. The amounts of honeydew produced by individuals are often prodigious. First instar nymphs of Mittler's Tuberolachnus extracted honeydew at the rate of seven droplets per hour, each droplet containing 0.065 ul, and the total output per aphid was 133 percent of the aphid's weight every hour. Other species that have been analyzed are slightly more modest, their hourly output ranging from 1.9 to 13.3 percent of body weight per hour (Auclair, 1963).

Most myrmecophilous homopterans, especially aphids, have special structural and behavioral adaptations for life with ants (Way, 1963; Kunkel, 1973; Kunkel and Kloft, 1985). Aphids frequently associated with ants tend to have poorly developed cornicles, a reduced cauda, and at most a thin coating of wax filaments. However, a few ant-attended species have large cornicles and others are densely covered with wax. In the case of one such species, Prociphilus fraxini, the ants simply remove wax from the bodies of the aphids (Zwölfer, 1958; Kunkel, 1973). And where most pseudococcids are covered with wax, the ants often clean the symbionts bare. Kunkel (1973) notes that myrmecophilous aphids generally have more setae on the dorsal body surface and tibiae. Anal setae in particular are very numerous in myrmecophilous aphids. They form a basket (“trophobiotic organ”) that holds the honeydew droplet until it is imbibed by the ants (Zwölfer, 1958; Kunkel, 1973).

Novgorodova (2015a) - Trophobiont insects play an important role in the life of many ants. Their excreta (the honeydew) are rich in carbohydrates and form one of the main trophic resources for the ant colony (Dlussky, 1967; Delabie, 2001); therefore, protection of the trophobionts from various competitors is a fairly important task for ants. This is especially true of the species whose colonies include tens of thousands and more workers and require great amounts of carbohydrate food (Oliver et al., 2008). The efficiency of protection of trophobionts from their natural enemies varies significantly depending on the ant species (Itioka and Inoue, 1999; Gibernau and Dejean, 2001; Katayama and Suzuki, 2003; Novgorodova and Gavrilyuk, 2012). As a result, different representatives of the multi-species ant assemblage differently affect the survival of their symbionts (Addicott, 1978; Bristow, 1984; Buckley and Gullan, 1991).

Representatives of the genus Formica, living in large colonies (104 - 106 ind.) and dominating in multispecies ant associations, provide the most promising object for studying the interactions between ants and aphidophages. Species of this group are characterized by the highest level of “professional” specialization among the honeydew collectors (Reznikova and Novgorodova, 1998a; Novgorodova, 2008) and the highest level of aggression towards aphidophages (Novgorodova and Gavrilyuk, 2012). Due to these traits, they offer their symbionts the most efficient protection from natural enemies (Gavrilyuk and Novgorodova, 2007; Novgorodova and Gavrilyuk, 2012). In addition, the aggressive behavior of the honeydew collectors of these species towards aphidophages is to a greater extent related to protection of symbionts from potential competitors, rather than to simple predation. For example, as compared to ants with a simpler variant of honeydew collection (performed by non-specialized foragers with only partial division of labor), the honeydew collectors of ants of the subgenus Formica s. str., acting as obligatory dominants in multi-species ant assemblages, do not switch over to collecting proteinaceous food (Novgorodova, 2005a).

Novgorodova (2015b) - Aphid honeydew is one of the main energy sources for various ants in the temperate zone, nevertheless relatively little is known about the organization of the work of honeydew foragers (aphid milkers). This study focuses on the honeydew collecting strategies used by different ants in steppe and forest multi-species communities in Western Siberia. The behaviour of marked foragers of 12 species (Formica - 7, Lasius - 2, Camponotus - 1, Myrmica - 2) was recorded. Depending on the degree of the aphid milker specialization and degree of protection of the aphids five honeydew collecting strategies of various complexity were distinguished: unspecialized foragers in (I) "unprotected" aphid colonies (attended by ants <60% of time) and (II) "protected" colonies (attended >95% of time); (III) low "professional" specialization (ants "on duty" constantly attending aphid colonies); (IV) medium and (V) high "professional" specialization (clear division of tasks: honeydew collecting by "shepherds" and protection of trophobionts by "guards"; and honeydew transportation by "transporters" in V). Task specialization of the honeydew foragers is facultative: different ant taxa demonstrate a certain range of the honeydew collecting strategies of different complexities (Formica - I-V, Lasius - I-II, Camponotus - III, Myrmica -I-II) depending on the needs of their colony. The strategy used by ants did not depend on the species of aphid attended, but is strongly dependent on the species of ant, their colony size, available food resources and seasonality. In summer, the aphid milker specialization becomes more complex as ant colony size increases at both intra-and inter-specific levels and when food is scarce. In autumn Formica s. str. ants, which have the most advanced foraging strategy, adopt a simpler honeydew collecting strategy. Overall, the variety of honeydew foraging strategies seems to reflect the unequal contribution of different ants in forming trophobiotic interactions with aphids.