Heliconius butterflies have two unique, derived ecological traits that may have facilitated rapid adaptive radiation: pollen feeding and pupal-mating behaviour.
Most adult lepidopterans feed on fluid resources such as nectar, decomposing animals and fruit, and dung. However, Gilbert (1972) showed that Heliconius butterflies collect pollen for its nutritive value, rather than as an indirect result of visits for nectar as had previously been assumed. The butterflies collect and accumulate large loads of pollen and the production of abundant saliva helps keep pollen attached to the proboscis, which can gently masticate the pollen load for long periods, allowing butterflies to obtain amino acids (Gilbert, 1972). Amino acids assimilated from pollen increase egg production and enable a long adult life span of up to six months (Boggs et al., 1981; Gilbert, 1972; Mallet et al., 1998). Also, pollen can provide nitrogen and precursors for synthesis of cyanogenic glycosides that may increase the concentration of defensive chemicals in adult butterflies (Cardoso, 2001; Nahrstedt and Davis, 1981).
Morphological studies have revealed no unique structures among the species that use pollen in their diets (Krenn et al., 2001; Penz & Krenn, 2000). However, there are a combination of features that assist collection and processing of pollen. For example, in Laparus and Heliconius the appendages near the proboscis known as the labial palpi are cylindrical rather than club-shaped as in the rest of the Heliconiina. Penz (1999) suggested that narrow labial-palpi help Heliconius and Laparus to keep pollen attached to their proboscis. Behavioural modifications are also important: pollen-feeding species manipulate Lantana flowers faster and more thoroughly compared to non-pollen feeding relatives (Krenn & Penz, 1998).
The diets of most Lepidoptera are very limited in nitrogenous compounds, and pollen feeding is thought to increase longevity and egg production in Heliconius butterflies. Mathieu Joron
The evolution of pollen feeding in Heliconius has affected the evolution of their pollen sources, plants from the Cucurbitaceae family such as Gurania and Psiguria (Gilbert, 1975). For instance Psiguria vines develop small flowers that contain a high amount of pollen and nectar. Those flowers are produced in an inflorescence and male flowers last only one day, then drop off the inflorescence. Thus, male flowers are a reliable pollen source that guarantee daily visits from pollen feeding but also pollinating butterflies (Gilbert, 1975). Heliconius butterflies only visit male flowers because female flowers do not have pollen. Psiguria vines are all-male, but occasionally a single plant changes sex and produces female flowers. Heliconius while attempting to find pollen in this flower, leave pollen behind that was gathered during visits to other flowers and pollination takes place (Gilbert, 1975). Also, the amount of pollen dispersed by Heliconius is greater than by hummingbirds, the other pollinator of Psiguria (Murawski and Gilbert, 1986).
You might also want to visit The complex relationship between the “Holstein” butterfly (Heliconius sapho), its food plant and its pollen source.
Differences in patterns of pollen exploitation in Heliconius provide evidence of habitat segregation. Among comimics, Boggs (1981) and Murawski (1986) showed that H. erato and H. hewitsoni tends to collect smaller pollen grains such as those of Lantana, while their comimic and sympatric species H. melpomene and H. pachinus, tends to collect bigger pollen grains such as those of Psiguria. Between sister species, the sympatric species H. cydno and H. melpomene differed significantly in pollen load composition for three of the five most commonly collected pollen species as a result of their differences in habitat preferences (Estrada and Jiggins, 2002). H. cydno is found in closed-canopy areas while H. melpomene is found in open areas, suggesting that the chances of encounter between the sister species are reduced in nature contributing to pre-mating isolation (Estrada and Jiggins, 2002). Diversification in microhabitat, larval food use and adult pollen-donor plant use, all contributed to diversification and speciation of the genus (Gilbert, 1975).
A second unusual trait found in some Heliconius species is a unique mating behaviour known as pupal-mating. Males of certain species search larval food plants for female pupae. The males then sit on the pupae a day before emergence, and mating occurs the next morning, before the female has completely eclosed (Gilbert, 1976; Deinert et al. 1994). Various kinds of pupal-mating occur scattered across several insect orders (Thornhill & Alcock, 1993); in passion-vine butterflies almost half the Heliconius species (42%) are pupal-maters (Gilbert, 1991).
Gilbert (1991) suggested that pupal-mating might play an important role in the radiation of Heliconius as well as in the packing of Heliconius species into local habitats. Pupal-mating might enhance the possibility of intrageneric mimicry because in most cases, each mimetic species pair consists of a pupal-mating and a non pupal-mating species. The strikingly different mating tactics of these groups could allow phenotypically identical species to occupy the same habitats without mate recognition errors. Second, this mating tactic may influence host-plant specialisation, as it has been suggested that pupal-mating species may displace other heliconiines from their hosts by interference competition (Gilbert, 1991). Males of these species sit on, attempt to mate with, and disrupt eclosion of other Heliconius species of both mating types. This aggressive behaviour may prevent other heliconiine species from evolving preference for host plants used by pupal-mating species.
Virtually all larvae in the Heliconiina sub-tribe are warningly coloured to some degree and almost 50% of Heliconius species deposit their eggs in clusters with associated larval gregariousness (Brown, 1981). Sillen-Tullberg (1988) proposed that aggregation among butterfly larvae arises after the evolution of unpalatability, because gregariousness ought to be disadvantageous for palatable organisms that live in exposed habitats and are relatively immobile. In contrast, gregariousness can be advantageous for unpalatable organisms, since the predator avoids prey after a few encounters.
For more information about hostplants and general biology of Heliconius species visit Tree of Life Heliconius pages
Boggs CL, Smiley JT, Gilbert LE. 1981. Patterns of Pollen Exploitation by Heliconius Butterflies. Oecologia 48, 284-289.
Brown KS. 1981. The Biology of Heliconius and Related Genera. Annual Review of Entomology 26, 427-456.
Cardoso NZ. 2001. Patterns of pollen collection and flower visitation by Heliconius butterflies in southeastern Mexico. Journal of Tropical Ecology 17, 763-768.
Deinert EI, Longino JT, Gilbert LE. 1994. Mate competition in butterflies. Nature (London) 370, 23-24.
Estrada C, Jiggins CD. 2002. Patterns of pollen feeding and habitat preference among Heliconius species. Ecological Entomology 27, 448-456.
Gilbert LE. 1972. Pollen Feeding and Reproductive Biology of Heliconius Butterflies. Proceedings of the National Academy of Sciences of the United States of America 69, 1403-&.
Gilbert LE. 1975. Ecological consequences of a coevolved mutualism between butterflies and plants. In: Coevolution of Animals and Plants (eds. Gilbert LE, Raven PR), pp. 210-240. University of Texas Press, Austin, TX.
Gilbert LE . 1976. Postmating Female Odor in Heliconius Butterflies – Male-Contributed Anti-Aphrodisiac. Science 193, 419-420.
Gilbert LE . 1991. Biodiversity of a Central American Heliconius community: pattern, process, and problems. In: Plant-Animal Interactions: Evolutionary Ecology in Tropical and Temperate Regions (eds. Price PW, Lewinsohn TM, Fernandes TW, Benson WW), pp. 403-427. John Wiley & Sons, New York.
Krenn HW, Penz CM. 1998. Mouthparts of Heliconius butterflies (Lepidoptera : Nymphalidae): A search for anatomical adaptations to pollen-feeding behavior. International Journal of Insect Morphology & Embryology 27, 301-309.
Krenn HW, Zulka KP, Gatschnegg T. 2001. Proboscis morphology and food preferences in nymphalid butterflies (Lepidoptera : Nymphalidae). Journal of Zoology 254, 17-26.
Mallet J, McMillan WO, Jiggins CD. 1998. Estimating the mating behavior of a pair of hybridizing Heliconius species in the wild. Evolution 52, 503-510.
Murawski DA. 1986. Pollination ecology of a Costa Rican population of Psiguria warscewiczii in relation to the foraging behaviour of Heliconius butterflies Dissertation, University of Texas. Austin, TX.
Murawski DA, Gilbert LE. 1986. Pollen Flow in Psiguria-Warscewiczii – a Comparison of Heliconius Butterflies and Hummingbirds. Oecologia 68, 161-167.
Nahrstedt A, Davis RH. 1981. Cyanogenic glycosides in butterflies: detection and synthesis of linamarin and lotaustralin in Heliconiinae. Planta Medica (?CHECK) 42, 124-125.
Penz CM, Krenn HW. 2000. Behavioral adaptations to pollen-feeding in Heliconius butterflies (Nymphalidae, Heliconiinae): An experiment using Lantana flowers. Journal of Insect Behavior 13, 865-880.
Sillen-Tullberg B. 1988. Evolution of Gregariousness in Aposematic Butterfly Larvae: A Phylogenetic Analysis. Evolution 42, 293-305.
Thornhill R, Alcock J. 1983. The evolution of insect mating systems Harvard University Press, Cambridge, Mass.