Cheating on a Mutualism: Indirect Benefits of Ant Attendance to a Coccidophagous Coccinellid

Abstract

Coccinellids (Coleoptera: Coccinellidae) are generally unable to prey on ant-tended prey. However, particular coccinellid species have morphological, behavioral, or chemical characteristics that render them immune to ant attacks, and some species are even restricted to ant-tending areas. The benefit gained from living in close association with ants can be twofold: (1) gaining access to high-density prey areas and (2) gaining enemy-free space. Here, the myrmecophily of Azya orbigera Mulsant (Coleoptera: Coccinellidae), an important predator of the green coffee scale, Coccus viridis (Green) (Hemiptera: Coccidae), is reported. In this paper, three main questions were studied. (1) Are the waxy filaments of A. orbigera larvae effective as defense against attacks of the mutualistic ant partner of C. viridis, Azteca instabilis F. Smith (Hymenoptera: Formicidae)? (2) Does A. instabilis reduce the rate at which A. orbigera larvae prey on scales? (3) Do A. orbigera larvae gain enemy-free space by living in close association with A. instabilis? Laboratory and field experiments were conducted to answer these questions. We found that, because of the sticky waxy filaments of A. orbigera larvae, A. instabilis is incapable of effectively attacking them and, therefore, the predation rate of A. orbigera on C. viridis does not decrease in the presence of ants. Furthermore, A. instabilis showed aggressive behavior toward A. orbigera's parasitoids, and the presence of ants reduced the parasitism suffered by A. orbigera. This is the first time that this kind of indirect positive effect is reported for an ant and a coccidophagous coccinellid. Furthermore, this indirect positive effect may be key to the persistence of A. orbigera's populations.

Evolutionary Perspectives on Myrmecophily in Ladybirds

“…The Coccinellidae family consists of seven subfamilies [25] among which five include myrmecophilous species: Scymninae, Ortaliinae, Chilocorinae, Coccinellinae, and Coccidulinae [26][27][28][29][30][31] (Table 1). Interestingly, only one myrmecophilous species has been recorded to date in each of the three subfamilies Ortaliinae, Chilocorinae, and Coccinellinae and two in the subfamily Coccidulinae whereas there are eight species from the Scymninae subfamily belonging to four different tribes: one species from the Diomini tribe, two species from the Hyperaspidini and Brachiacanthadini tribes, and three species from the Scymnini tribe.…”

“…Myrmecophilous Brachiacantha quadripunctata (Melsheimer) and B. ursina (Fabricius) even get inside the ants' nest where they feed on ant-tended coccids and adelgids (Hemiptera, Aldegidae) [39,40]. The waxy filaments also allow the myrmecophilous ladybird Azya orbigera (Mulsant) to feed on coccids tended by Azyeca instabilis (F. Smith) [29], and the larvae of the ladybird Ortalia pallens (Mulsant) to feed on Pheidole punctulata (Mayr) workers [34]. However, this waxy coating does not always provide an efficient protection as Pheidole megacephala (Fabricius) ants prey on Cryptolaemus montrouzieri (Mulsant) and A. orbigera ladybird larvae since they are able to remove their protective coating [19].…”

“…A second and important benefit of myrmecophily may arise from the access it provides to an enemy-free space. Ants limit interspecific and intraguild competition as well as access to the parasitoids and predators of ladybirds [29,30,33,51,52]. The competitors of S. interruptus and S. nigrinus, for example, have been noted as being less present on anttended colonies [30].…”

“…The competitors of S. interruptus and S. nigrinus, for example, have been noted as being less present on anttended colonies [30]. Moreover, the presence of ants reduced larval parasitism by Homalotylus platynaspidis (Hoffer) (Hymenoptera, Chalcidoidea) in P. luteorubra [33], and the aggressive behaviour of A. instabilis disturbed the oviposition behavior of H. shuvakhinae (Trjapitzin), the most common parasitoid of A. orbigera [29]. Nonetheless, the observed decreases in parasitism rates do not always directly result from ant protection.…”

“…Only a few myrmecophilous species have been identified to date, but because most coccinellids encounter ants very frequently and often supplement their Psyche 5 essential food sources with other food items (which might help in their being able to shift to new diet and habitat), it would not be surprising that many more myrmecophilous species still remain to be discovered. Among the seven subfamilies of Coccinellidae, myrmecophilous species have been identified in only five of them with, moreover, most of them concentrated in the Scymninae subfamily [26][27][28][29][30]. The predominance of myrmecophily in the Scymninae raises the question of the evolution of traits that promoted such interactions with ants.…”