Honeydew amino acids in relation to sugars and their role in the establishment of ant-attendance hierarchy in eight species of aphids feeding on tansy (Tanacetum vulgare)

Abstract. The ratio of the concentration of honeydew total amino acids to total sugars in the honeydew of eight species of aphids, all feeding on tansy, Tanacetum vulgare (L.), was determined and correlated with honeydew production and ant‐attendance. The honeydew of the five ant‐attended aphid species [Metopeurum fuscoviride (Stroyan), Trama troglodytes (v. Hayd), Aphis vandergooti (Börner), Brachycardus cardui (L.), Aphis fabae (Scopoli)] was rich in total amino acids, ranging from 12.9 to 20.8 nmol µL^?1 compared with the unattended aphid Macrosiphoniella tanacetaria (Kalt.) with only 3 nmol µL^?1. Asparagine, glutamine, glutamic acid and serine (all nonessential amino acids) were the predominant amino acids in the honeydew of all species. The total concentration of amino acids in the phloem sap of tansy was much higher (78.7 nmol µL^?1) then in the honeydew samples, and the predominant amino acids were glutamate (34.3%) and threonine (17.7%). A somewhat unexpected result was the finding that those aphid species with the highest total amino acid concentration in the honeydew always had the highest concentration of sugars. The lowest amino acid–sugar combined value was 104–28.8 nmol µL^?1 in the non ant‐attended species M. tanacetaria, and the highest value was an average of 270–89.9 nmol µL^?1 for the three most intensely attended aphid species M. fuscoviride, A. vandergooti and T. troglodytes. There is no evidence that any single amino acid or group of amino acids in the honeydew acted as an attractant for ant‐attendance in these eight aphid species. The richness of the honeydew (rate of secretion × total concentration of sugars), along with the presence of the attractant sugar melezitose, comprised the critical factors determining the extent of ant‐attendance of the aphids feeding on T. vulgare. The high total amino acid concentration in sugar‐rich honeydews can be explained by the high flow‐through of nutrients in aphids that are particularly well attended by ants.     

Large interclone differences in melezitose secretion in the facultatively ant-tended black bean aphid Aphis fabae

Many aphids are known to engage in a trophic mutualism with ants, whereby the aphids secrete sugary-rich honeydew which is collected by the ants for food, and the ants, in exchange, protect the aphids against natural enemies. Previous results, however, suggest that the production of some of the honeydew sugars, such as the ant-attractant trisaccharide melezitose, may induce an indirect cost to the aphids. This led us to believe that large differences in the nature of the secreted honeydew might exist, due to some clones capitalizing more or less on their mutualistic interaction with ants, or due to some “cheater” clones foregoing the production of particular sugars, instead taking advantage of the ant-attracting effect of other non sugar-deficient clones, co-occurring on the same plant. Here we present data on clonal variation in the composition of honeydew of the black bean aphid Aphis fabae which confirm this prediction. In particular, our results show that there was large interclone variation in the amount of glucose, melezitose and total sugar produced. The variation in the production of melezitose, however, showed particularly large differences, with 54% (7 out of 13) of the clones screened being virtually deficient for the production of this sugar, irrespective of whether the aphid colonies were ant-tended or not. The consequences of this finding in the context of the evolution and maintenance of the ant–aphid mutualism, as well as the adaptive benefits of oligosaccharide synthesis in aphids and other insects are discussed.     

Relative fitness of aphids: effects of plant quality and ants

We investigated the response of four species of aphids ( Metopeurum fuscoviride , Brachycaudus cardui , Aphis fabae , and Macrosiphoniella tanacetaria ) on tansy ( Tanacetum vulgare ) to plant quality and attendance by an ant, Lasius niger . The aphids experienced one of four different environments for two consecutive generations. Ant-attendance significantly affected the time needed to reach maximum fecundity only in Me. fuscoviride and plant quality in Me. fuscoviride and B. cardui . Maximum daily fecundity was positively affected by plant quality and the magnitude of the effect was inversely associated with the degree of myrmecophily. Ant-attendance had a positive effect on maximum fecundity only in the obligate myrmecophile, Me. fuscoviride . The intrinsic rate of population increase, r _m, on high quality plants, was lowest for the obligate myrmecophile, intermediate for the facultative myrmecophiles and highest for the unattended species. On high quality plants the fitness of Me. fuscoviride was more adversely affected by the developmental stage of the plant and absence of ants than that of A. fabae or Ma. tanacetaria , which were able to maintain a high relative fitness in all the environments. The implications for aphids experiencing different degrees of ant-attendance and seasonal changes in plant quality are discussed.     

The foraging behaviors of larvae of the ladybird beetle, <Emphasis Type="Italic">Coccinella septempunctata</Emphasis> L., (Coleoptera: Coccinellidae) towards ant-tended and non-ant-tended aphids

The foraging behaviors of larvae of the ladybird, Coccinella septempunctata L., towards both the ant-tended aphid, Aphis craccivora Koch, and the non-ant-tended aphid, Acyrthosiphon pisum Harris, were investigated in the field and in laboratory experiments. Although there were no differences in the development and growth of the ladybird larvae that preyed on either Ac. pisum or Ap. craccivora, the foraging efficiency of the ladybird larvae that preyed on Ap. craccivora was higher than that of the ladybird larvae that preyed on Ac. pisum in the absence of ants. This result was explained by the fact that the number of Ac. pisum that escaped by dropping off the plant was conspicuously larger than the number of Ap. craccivora that escaped in this fashion and derived from the non-ant-attendance associated with Ac. pisum. In the laboratory experiments, fewer ladybird larvae climbed onto a plant with Ap. craccivora in the presence of ants than onto a plant with Ac. pisum in the absence of ants. The ladybird larvae did not switch from foraging for Ap. craccivora to foraging for Ac. pisum, even after suffering attacks by ants on a plant with Ap. craccivora, and it would appear that ladybird larvae are unable to remember where they have previously been attacked by ants. These results could explain why the ladybird larvae in the field more frequently visited Vicia angustifolia plants with Ap. craccivora than those with Ac. pisum and made more visits when ants were absent than when they were present.     

An aphid-ant interaction: effects on different trophic levels

The interaction between the aphid Aphis coreopsidis (Thomas) (Hemiptera, Aphididae) and the ant Camponotus sp.1 (Hymenoptera, Formicidae) on the plant Bidens pilosa L. (Asteraceae) was studied. We manipulated the presence of ants and other insects to understand the effects of this aphid-ant interaction on: (a) the growth of A. coreopsidis population, (b) the seed production of B. pilosa, (c) the density of predator spiders. The growth of the A. coreopsidis population was positively affected by attending ants, showing greater increase on ant-present control plants than on ant-excluded plants. The density of aphids on control plants was positively correlated with the density of attending ants, while the density of aphids on ant-excluded plants was positively correlated with the density of spiders. Plants with ants had a significantly lower quantity of viable seeds than those without ants. These results show that: (a) the presence of Camponotus ants reduces the number of predator spiders on B. pilosa, (b) the population of A. coreopsidis increases when attended by the ants, (c) this increase in aphid density as a result of ant attendance reduces the number of viable seeds of B. pilosa, and thus (d) an interspecific interaction between two species can have an indirect negative fitness effect on other partners.