The Big Brained Butterfly

As we launch our ninth annual Hillsborough County Hiking Spree, featuring the zebra longwing butterfly on this year's prizes, it seems fitting to explore the fascinating story of our state butterfly.

Last month I wrote about the raptor songbird, the loggerhead shrike. While speaking to staff about the bird, I heard again and again, "That is my favorite bird!" Some of this is undoubtedly due to their charisma, or the lasting impression of finding a shrike "larder" (their public displays of victims). However, I like to think that much of the shrike's appeal lies in how their adaptations demonstrate the extreme pressures exerted on wild animals.

A zebra longwing butterfly nectaring on a native blue porterweed plant. Note the pollen on their proboscis. Photo by iNaturalist contributor, Scott. BY-NC 4.0

How does this relate to the zebra longwing butterfly (Heliconius charithonia)? No, I'm not about to tell you that our state butterfly is secretly a carnivore, hunting down insects on-the-wing (although their larvae do engage in cannibalism from time to time). But, much like the "cute little songbirds" we see at the feeder every day, these butterflies are under intense pressure to adapt in an ever-escalating evolutionary arms race with its host plant, the passion vine. This relationship has driven both species to develop increasingly sophisticated adaptations.

The longwing clade (that is, butterflies related to the zebra longwing) lays their eggs exclusively on passion vine plants (Passiflora species). These eggs hatch, and the caterpillars feed on the plant. This is the manner by which the passion vine serves as a larval host plant, but the relationship is largely one-sided. The passion vines do not appreciate being eaten by the caterpillars and have evolved an impressive array of defenses.

A representation of the extraordinary diversity of leaf shapes between Passiflora species. This diversity is – in part – to deceive herbivores such as the zebra longwing. From Wosch et al. (2015). Fig. 1. "Passiflora spp. – Morphological aspect of leaves – Adaxial side. a. P. actinia; b. P. alata; c. P. amethystina; d. P. capsularis; e. P. cincinnata; f. P. edulis f. flavicarpa; g. P. edulis f. edulis; h. P. incarnata; i. P. morifolia; j. P. urnifolia; k. P. coccinea; l. P. setacea. Ps.: the images were obtained after fixation with FAA. Bars = 2 cm." Revista Brasileira de Farmacognosia, 25(4), 328-343. CC BY-NC-ND 4.0.

Research by de Castro and colleagues documented a variety of leaf forms across Passiflora species, including oval, oblong, elliptical, lanceolate, falcate, and lobate shapes (de Castro et al., 2018). This morphological variability serves as camouflage, making it challenging for butterflies of the longwing clade to recognize suitable host plants. Some Passiflora species even mimic the leaves of entirely different plants, such as laurel or grape vines, to confuse butterflies. If you'd like to read more about our local varieties of passion vine, check out our previous article on the subject.

Zebra longwings are fairly widespread in the tropics. This picture was taken in Costa Rica. Note the tattered edges of this individual's wings; zebra longwing butterflies are particularly long lived due to a unique adaptation to eating pollen. As such, they have a tendency of acquiring lots of wear and tear over their extended lifespan. Photo by iNaturalist contributor, Circc. BY-NC 4.0

Adding to this deception, certain passion vines produce yellow, globular structures that mimic butterfly eggs. Due to the occasional case of aforementioned cannibalism between caterpillars – as well as a desire to avoid competition – butterflies often avoid laying on already occupied plants. Williams and Gilbert demonstrated this effect experimentally; when they removed egg mimics from Passiflora cyanea, females were 60% more likely to lay eggs on the plants. (Williams & Gilbert, 1981)

Zelus biloba (assassin bug) feeding at an extrafloral nectary on maypop. Photo by Dave. BY-SA 3.0

The vines' defenses are particularly sophisticated when it comes to recruiting allies. The native Florida species Maypop (Passiflora incarnata), which you might spot at Rhodine Scrub Nature Preserve, forms a mutualistic relationship with predatory insects by producing nectar from specialized structures called extrafloral nectaries. These sweet secretions attract carnivores, typically ants which, in turn, patrol the plant and protect it from herbivorous insects, including butterfly larvae. Studies by Labeyrie and colleagues found that Passiflora plants without ant protection suffered 26% more herbivore attacks. (Labeyrie et al., 2001)

Scanning electron micrography of defensive trichomes on P. lobata leaves. Cardoso, M. Z. (2008). Neotropical Entomology, 37(3), 247-252. BY-NC 4.0.

Even more direct are the trichomes – tiny hair-like structures that several species of Passiflora have developed into sharp spikes which serve as a deterrent for small herbivores. On species like P. lobata, a Central American passion vine, these trichomes are hooked in such a way that most caterpillars become ensnared and die of starvation, unable to move across the leaf surface. However, Zebra Longwing larvae have specifically developed a solution: they carefully wrap the trichomes with silk and bite off their tips, creating safe passages across the otherwise hazardous leaf surface. Their cousin H. pachinus, by contrast, cannot survive on trichome-defended plants. (de Castro et al., 2018)

Butterflies posses sophisticated vision capabilities which, such as the perception of ultraviolet and polarized light, but the longwing clade of butterflies posses uniquely large structures in it's brain which allow them to better understand their host plants. Photo by iNaturalist contributor, Edgar B. BY-NC 4.0

And that confusing foliage? The adult butterflies have evolved their own adaptations for finding suitable host plants. Research by Montgomery, Merrill, and Ott showed that Heliconius butterflies have developed specialized mushroom bodies; these are regions associated with learning and memory. Mushroom bodies in the longwing clade are proportionally larger than in any other butterfly studied, enabling them to remember and recognize suitable host plants even among the passion vines' confusing variety of leaf shapes. Female butterflies have developed heightened chemosensory receptors on their legs, enabling them to chemically assess plant suitability upon landing, they then use this chemical confirmation to validate their memory of the leaves, committing ambiguously shaped passion vines to memory. (Montgomery et al., 2016)

The zebra longwing caterpillar is may look thorny, but it is harmless to the touch. However, they sequester toxins from passion vine plants which make them quite unpalatable. Photo by iNaturalist contributor, Mock. BY-NC 4.0

Like many charismatic butterflies, they also sequester the plants' toxic compounds within their own bodies, rendering themselves unpalatable to most predators – a defense that persists into adulthood. Their distinctive black and white striped wings serve as warning coloration, advertising their toxicity to potential predators. To better take advantage of this, zebra longwings roost together in groups at night. This communal behavior amplifies their warning signals to predators. Finkbeiner et al. (2012)

Zebra longwing butterfly roosting together. Note the pollen on the proboscis of the bottom-right butterfly. Photo by iNaturalist contributor, Cissys. BY-NC 4.0

As a quick aside, zebra longwings have also developed some unique behaviors unrelated to their battle with passion vines. They are one of the only butterflies known to digest pollen in addition to nectar - this extra protein source can extend their lifespan up to six months, extraordinarily long for a butterfly. They also engage in an unusual mating strategy where males seek out and guard female pupae, mating with females as they emerge from their chrysalis, and in some cases before. (Beltrán et al., 2007) This behavior is documented dramatic fashion in WFSU producer, Rob Diaz de Villegas' excellent article: The strange and dangerous love lives of zebra longwing butterflies.

A zebra longwing passing by one of their offspring. Photo by iNaturalist contributor, CHeather A. Wise. BY-NC 4.0

Witnessing the complex interactions between zebra longwings and passion vines can sometimes be bittersweet, and less than the harmonious ideal we have come to associate with butterfly gardens. However, such events are integral components of a healthy ecosystem. To quote Rob from the aforementioned article, "If I see a dead monarch in my yard, it’s because I have habitat for monarchs in my yard." The same principle applies to all the plants and animals we invite into our gardens.

By cultivating native plants like passion vines in our gardens, we are not simply supporting butterflies but entire ecological processes. Predation is an essential element of food webs, sustaining a diverse array of organisms. Recognizing and embracing these natural dynamics will help regulate your caterpillar population and ultimately lead to a healthier ecosystem. If you'd like to see what other species of butterfly frequent our preserves, why don't you visit in person by participating in the 2024-2025 Hiking Spree (remember, you can earn some awesome zebra longwing swag)! Or, you can check out some of our burn manager Bill's excellent butterfly pictures.

A zebra longwing perched atop a Viscaria asterias. Photo by iNaturalist contributor, CAli and Brice. BY-NC 4.0

References

Beltrán, M., Jiggins, C.D., Brower, A.V.Z., Bermingham, E., & Mallet, J. (2007). Do pollen feeding and pupal-mating have a single origin in Heliconius butterflies? Inferences from multilocus DNA sequence data. Biological Journal of the Linnean Society, 92, 221-239.

de Castro, É.C.P., Zagrobelny, M., Cardoso, M.Z., & Bak, S. (2018). The arms race between heliconiine butterflies and Passiflora plants – new insights on an ancient subject. Biological Reviews, 93, 555-573.

Diaz de Villegas, R. (2022, September 28). The strange and dangerous love lives of zebra longwing butterflies. WFSU Ecology Blog. Retrieved from https://blog.wfsu.org/blog-coastal-health/author/rdiazdevillegas/.

Finkbeiner, S.D., Briscoe, A.D., & Reed, R.D. (2012). The benefit of being a social butterfly: communal roosting deters predation. Proceedings of the Royal Society B: Biological Sciences, 286, 20191225.

Labeyrie, E., Pascal, L., Delabie, J., Orivel, J., Dejean, A., & Hossaert-McKey, M. (2001). Protection of Passiflora glandulosa (Passifloraceae) against herbivory: impact of ants exploiting extrafloral nectaries. Sociobiology, 38, 317-321.

Montgomery, S.H., Merrill, R.M., & Ott, S.R. (2016). Brain composition in Heliconius butterflies, posteclosion growth and experience-dependent neuropil plasticity. Journal of Comparative Neurology, 524, 1747-1769.

Williams, K.S., & Gilbert, L.E. (1981). Insects as selective agents on plant vegetative morphology: egg mimicry reduces egg laying by butterflies. Science, 212, 467-469.

Cardoso, M. Z. (2008). Herbivore handling of a plant's trichome: The case of Heliconius charithonia (L.) (Lepidoptera: Nymphalidae) and Passiflora lobata (Killip) Hutch. (Passifloraceae). Neotropical Entomology, 37(3), 247-252. https://doi.org/10.1590/S1519-566X2008000300002

Wosch, L., Imig, D. C., Cervi, A. C., Moura, B. B., Budel, J. M., & Santos, C. A. M. (2015). Comparative study of Passiflora taxa leaves: I. A morpho-anatomic profile. Revista Brasileira de Farmacognosia, 25(4), 328-343. https://doi.org/10.1016/j.bjp.2015.06.004