About Bamboo, Ants, Scales and a Strange New Butterfly: Four-Level Interactions and the Evolution of Complex Life-History Traits in Annulata (Lepidoptera: Riodinidae).

Annulata J. Hall is a recently described monotypic riodinid genus composed of a single myrmecophilous butterfly species, Annulata annulifera Godman, which occurs in bamboo forests in the Amazonian region. Here, we describe a new species of this genus, Annulata kaminskii Seraphim, Freitas & Mota sp. nov., from the southern Brazilian Amazonia, in addition to its life history and immature stages. This new species is aphytophagous and involved in a four-level trophic interaction with the bamboo plants it inhabits, scale insects whose honeydew and wax it feeds on, and two different, parabiotic ant species that tend to young and older larvae. This is the first case of a butterfly larva observed to offer, as rewards to tending ants, both a secretion produced by specific ant-organs (tentacle nectary organs) and an anal exudate that probably results from its liquid diet. Annulata kaminskii sp. nov. larvae present both tentacle nectary organs and vibratory papillae as ant-organs but anterior tentacle organs are absent. Furthermore, we provide a preliminary attempt at a phylogenetic hypothesis suggesting its systematic position within the Nymphidiini, as a member of the Lemoniadina subtribe (Nymphidiini: Riodininae), despite its lack of anterior tentacle organs. We further discuss the evolution of complex life-history traits in myrmecophilous butterflies in light of current published evidence.