Lucas A. Kaminski

Interaction between Mutualisms: Ant‐Tended Butterflies Exploit Enemy‐Free Space Provided by Ant‐Treehopper Associations

Although mutualisms have been intensively investigated, demonstration of indirect effects between co‐occurring mutualistic systems is rare. For instance, the ecological consequences of co‐occurrence of ant‐tended insects on a plant have never been examined for survival effects on either trophobiont species. Here, we assess the selective pressures mediating co‐occurrence of a facultative ant‐tended butterfly (Parrhasius polibetes) with ant‐tended treehoppers (Guayaquila xiphias) on Schefflera vinosa shrubs. We evaluated host plant selection and caterpillar survival in P. polibetes in the presence and absence of ant‐treehopper associations. Paired trials revealed that butterflies preferably oviposit on branches hosting ant‐tended treehoppers when they had a choice between those and branches without this interaction. Presence of ant‐tended treehoppers on a branch reduced the abundance of P. polibetes’ natural enemies and improved caterpillar survival in both premyrmecophylic and ant‐tended phases. Thus ant‐tended treehoppers create an enemy‐free space on foliage that butterflies exploit to protect larval offspring. These findings connect two widely documented ant‐trophobiont mutualisms and highlight the importance of considering multiple interactions for a proper understanding of ant‐plant‐herbivore systems. Detection of other ant‐based mutualisms on oviposition to improve offspring survival may have represented an important evolutionary step in the process of host plant selection in facultative myrmecophilous butterflies.

Trade-offs underlying polyphagy in a facultative ant-tended florivorous butterfly: the role of host plant quality and enemy-free space

The underlying mechanisms mediating the use of multiple host plants were investigated in Parrhasius polibetes (Lycaenidae), a florivorous and facultative myrmecophilous butterfly. Plant traits such as presence of ant–treehopper associations as a source of enemy-free space, flower bud dimensions, toughness, thickness, trichomes, and the corresponding performance and wear of P. polibetes mandibles were examined for three natural hosts: Schefflera vinosa (Araliaceae), Pyrostegia venusta (Bignoniaceae) and Luehea grandiflora (Malvaceae). Parasitism levels of larvae found on the three hosts were also determined. Almost all Luehea had ant–treehopper associations, and all larvae found on this host were non-parasitized. Parasitism was low in larvae found on Schefflera, half of which hosted ant–treehopper associations. No ant–treehopper association was found on Pyrostegia, where parasitism was significantly higher compared to other hosts. In the laboratory, P. polibetes performed well on Schefflera, followed by Pyrostegia. No larvae survived when fed with Luehea. Flower buds of Luehea were thicker and tougher than those of Schefflera and Pyrostegia. Indeed, mandibles of larvae reared on Luehea showed substantial wear, whereas those reared either on Schefflera or Pyrostegia presented no significant damage. Additionally, we suggest that co-occurrence with ant–treehopper associations on a plant provides parasitoid-free space for P. polibetes larvae. Our results support the hypothesis that ecological trade-offs among host plants (i.e., food quality and enemy-free space) promote polyphagy in natural populations of P. polibetes. Host morphological traits seem to play a relevant role in P. polibetes performance. To our knowledge, this is the first report showing the costs of polyphagy in a myrmecophilous butterfly.

Immature stages of Parrhasius polibetes (Lepidoptera: Lycaenidae): host plants, tending ants, natural enemies and morphology

Natural history and immature stage morphology of the facultative myrmecophilous butterfly Parrhasius polibetes (Stoll) (Lepidoptera: Lycaenidae) are described and illustrated through both light and scanning electron microscopy. Larvae underwent four instars. At the third instar, the dorsal nectar organ became present and functional, and larvae were facultatively tended by several ant species, those also tending plants bearing extrafloral nectaries and honeydew-producing hemipterans. Larvae were florivorous and polyphagous at the species level, using at least 44 species of plants in 19 families. Most host plants (∼ 89%) had some type of ant-attractive features, such as extrafloral nectaries or ant-tended treehoppers. The host range of this butterfly species allows the use of floral resources throughout the year. Food sources that promote ant visitation, flower bud morphology and phenology appear to be related to the evolution and maintenance of polyphagy in this butterfly species.

Natural history and morphology of immature stages of the butterfly Allosmaitia strophius (Godart) (Lepidoptera: Lycaenidae) on flower buds of Malpighiaceae

The natural history and morphology of immature stages of Allosmaitia strophius (Godart) are described and illustrated for the first time, using both light and scanning electron microscopy. The available host plant records for the genus were reviewed suggesting a feeding specialization on reproductive structures of Malpighiaceae. Both concentration of resources in the reproductive tissue of Malpighiaceae and the existence of sequential flowering periods may be important factors involved in the evolution of oligophagy in Allosmaitia. Field and laboratory observations showed that larvae of A. strophius are ignored by tending ants besides the presence of the dorsal nectar organ (DNO). Additionally, larvae present some behavioral and morphological adaptations that were proposed as preventing ant attacks, such as dendritic setae, thick cuticle, perforated cupola organs and absence of a “beat reflex”.

Adult and early-stage characters of Brassolini contain conflicting phylogenetic signal (Lepidoptera, Nymphalidae)

This study examines the contribution of early‐stages and adult characters to the reconstruction of the phylogeny of Brassolini butterflies. Parsimony analyses used both equal weights and implied weights, and a series of analyses were performed. First, we analysed adult and early‐stages partitions independently and in combination for a subset of 27 species; in these cases the matrices were mostly complete. Whereas the adult partition alone produced a topology that was well resolved and congruent with previous studies, the early‐stages partition produced a poorly resolved tree under equal weights. Furthermore, implied weights produced a well‐resolved early‐stages topology that differed significantly from the adult topology. When both partitions were combined for 27 species, implied weights yielded a topology that resembled the adult tree except for the positions of Bia and Penetes, but statistical node support was generally lower. This suggests that stochastic noise increased when early‐stage characters were added to the adult partition, but the combined partitions topology was not statistically different from that based on adult characters alone. Second, given that preserved early stages are not as readily available as adults, we analysed a matrix including 45 species in which early‐stage data were missing for 18 species, and compared the topology to that produced by the adult partition alone. Results were similar to the analyses including fewer species; the combined partitions tree was similar to that from the adult partition except for the position of Bia and Penetes. We compare our findings to other genus‐level phylogenetic studies within Lepidoptera that have also used early‐stages and adult characters.

Natural history of an ant–plant–butterfly interaction in a Neotropical savanna

Non-myrmecophilous lepidopteran larvae using plants bearing ant attractants such as extrafloral nectaries are good models for studying morphological and behavioural mechanisms against ant predation. Udranomia spitzi (Hesperiidae) is a butterfly whose larvae feed on leaves of Ouratea spectabilis (Ochnaceae), a plant with extrafloral nectaries. We described the early stages of U. spitzi, and used field observations and experiments to investigate the defensive strategies of caterpillars against predatory ants. Larvae pass through five instars and pupation occurs inside larval leaf shelters. Ant-exclusion experiments revealed that the presence of ants did not affect significantly caterpillar survival. Predation experiments showed that vulnerability to ant predation decreased with increase in larval size. The present study showed that predatory ants are not as relevant as demonstrated for other systems, and also illustrates how observational data and field experiments can contribute to a better understanding of the biology and ecology of a species of interest.

Immature Stages of Caria plutargus (Lepidoptera: Riodinidae), with Discussion on the Behavioral and Morphological Defensive Traits in Nonmyrmecophilous Riodinid Butterflies

Abstract Aspects of the natural history and early stage morphology of the nonmyrmecophilous butterfly Caria plutargus (F.) (Lepidoptera: Riodinidae) are described. Immature stages were observed through scanning electron microscopy, emphasizing larval structures that may be related to myrmecophily or not. The larvae have several types of setae (balloon, echinoid, dendritic, plumose) and perforated cupola organs. The presence of balloon setae in C. plutargus is the first record for Riodinini. These structures have been described for some Riodinidae tribes, such as Nymphidiini and Helicopini, and also for some taxa in the incertae sedis section. The literature has proposed that balloon setae play a role in the symbiosis between larvae and ants in myrmecophilous riodinids. However, the discovery of balloon setae in nonmyrmecophilous riodinids spurs a new debate concerning the function and evolution of these specialized setae (Ann. Entomol. Soc. Am. 97: 310–321, 2004). The morphological and behavioral traits here described are discussed in the context of defense against predators.

BEHAVIORAL ECOLOGY AT THE ANT-PLANT-HERBIVORE INTERFACE: INTERACTIONS BETWEEN ANTS AND LEPIDOPTERANS.

BEHAvIORAL ECOLOGy AT THE ANT-PLANT-HERBIvORE INTERFACE: INTERACTIONS BETWEEN ANTS AND LEPIDOPTERANS. Ants are one of the most prominent groups of terrestrial organisms in terms of diversity, relative abundance, and biomass. Their importance is due primarily to eusociality combined with complex communication systems, which enable them to recruit nestmates to capture prey and/ or protect profitable resources. Tropical foliage is rich in renewable food sources that promote visitation by ants. Because they are the principle predators among foliage, ants can strongly affect the communities of herbivorous insects and promote trophic cascades with relevant consequences to plants. The presence of ants on foliage can affect herbivores in two ways: (1) ant foragers can decrease the number of herbivores on plants through antagonistic interactions (e.g. aggressiveness, predation), (2) ants can create an enemy-free space for myrmecophilous herbivores (i.e. those living in close association with ants). Here, we discuss the ecological scenario in which these interactions occur, and examine the effects of foliage-dwelling ants on the biology and behavior of lepidopteran larvae.

Morfologia externa dos estágios imaturos de heliconíneos neotropicais: VI. Dione moneta moneta Hübner (Lepidoptera, Nymphalidae, Heliconiinae)

The external features of the egg, larva and pupa of Dione moneta moneta Hubner, 1825 are described and illustrated, based upon light and scanning electron microscopy.

Natural History, New Records, and Notes on the Conservation Status of Cyanophrys bertha (Jones) (Lepidoptera: Lycaenidae)

Abstract The natural history of the potentially threatened hairstreak butterfly Cyanophrys bertha (Jones) is discussed, and the morphology of its penultimate and last instar larvae and pupa are described and illustrated. New distribution records from southern Brazil are provided. Based on morphological and ecological traits of immatures and adults, the conservation status of this species is discussed and compared with other sympatric Eumaeini.