Impacts of ants attending citrus-infesting aphids on the aphid parasitoid assemblage

Influences of mutualism between honeydew-producing aphids on citrus shoots and ants attending the aphids, particularly aggressive behaviors shown by the ants towards the aphids' predators and parasitoids and the responses of these enemies, on the structure of the aphids' parasitoid assemblage (the structure was represented by the number of emerging adults of each parasitoid species) were assessed by field experiments at a no-pesticide citrus grove. Attendance by an ant species, Lasius niger, on the cotton aphid, Aphis gossypii, infesting citrus shoots significantly increased the number of emerging adults of the aphid's primary parasitoid, Lysiphlebus japonicus, and hyperparasitoids per aphid colony by repelling intraguild predators from the attended aphid colonies, compared with when ants were absent. Ovipositing females of the primary parasitoid concentrated in the aphid colonies attended by the ant, avoiding ant-absent aphid colonies, although the females were frequently attacked or disturbed by the ant workers. The ants disregarded aphids parasitized by L. japonicus, and therefore incidentally protected them against large predators. This led to a greater number of mummified aphids in the ant-attended colonies. Furthermore, the ants reduced intraguild predation and hyperparasitism on L. japonicus larvae and pupae within mummies. Impacts of two species of ants, L. niger and pristomyrmex pungens, attending the cotton aphid with different levels of aggressiveness on the number of emerging adults of the aphid's primary parasitoid did not differ significantly. This was because the primary parasitoid females deposited eggs into more aphids in the aphid colonies attended by a relatively less aggressive ant, P pungens, than in the colonies attended by another more aggressive ant, L, niger, due to the lower degree of interference by the former, but because protection of the parasitoid immatures within aphids by the less aggressive P pungens against intraguild predators and hyperparasitoids was less effective. Consequently, significantly more hyperparasitoid adults emerged in the aphid colonies attended by the less aggressive P. pungens than in the colonies attended by, the more aggressive L. niger. Effects of the two ant species on the number of emerging adults of the aphid's primary parasitoid and hyperparasitoids differed, when the ants attended a different aphid species, the brown citrus aphid Toxoptera citricidus (the season when the ants attended aphids was also different). The less aggressive ant, P pungens, significantly increased the emerging adult numbers of both the primary parasitoid and hyperparasitoids, whereas the more aggressive ant, L. niger, had no considerable impact on them. This is considered to be because aggressiveness of the latter more aggressive L, niger towards the primary parasitoid females is enhanced either when the ant attends the particular aphid species (i.e., T. citricidus) or in the particular season (i.e., summer), and because the primary parasitoid females therefore avoid the aphid colonies attended by the highly aggressive ant species Based on these results, the present study proposes a novel hypothesis that aphid-attending ant species exhibiting intermediate levels of aggressiveness maximize the number of emerging adults of the aphid's primary parasitoids and hyperparasitoids per aphid colony.