The vanishing ghost butterfly and a faint hope for their continued existence in urban forests fragments

Blog written by Antonio C. de Andrade & Matthew Adams. Read the full paper here.

There is a large, white butterfly (Morpho epistrophous nikolajewna) that still flies within the Brazilian Atlantic forest; once common, but now vanishing. Unfortunately, we only have a vague idea of what could be driving this species into oblivion.

The Brazilian Atlantic forest was at the front line of the havoc wrought by the early Europeans centuries ago. By fire and axe, as so elegantly and poignantly described by Dean (1995), the forest was converted to a small patchwork of forests that today is mostly immersed in sugarcane fields. Yet forest fragmentation is not the sole culprit for the demise of the ghost butterfly. There are other agents at work, some obvious (e.g. pesticides and logging) and other not so obvious (subtle local microclimate alteration and by-products of agricultural practices). Our paper details a history of loss, but also hope, which was found in an unexpected forest sanctuary surrounded by roads, buildings and all the urban chaos that can stress wildlife.

Sugarcane burning. Photo by Craig Elliot, FreeImages

The deleterious effects of human activities are greatly augmented in cities. The best example, and perhaps the most emblematic, is vehicular pollution. Thus, we were quite amazed to find a thriving population of ghost butterfly in an urban forest fragment, which are often subject to profound additional environmental stresses compared to rural ones.

The side effects of anthropogenic activities can be scary, yet it is difficult to comprehend their magnitude and how exactly they affect the biodiversity. For example, a group of amateur German entomologists and scientists (Hallmann et al. 2017) reported an alarming 76% decline in the biomass of flying insects over a period of 27 years in protected areas. They could not pinpoint the precise driving forces responsible for this decline, although suggesting agricultural intensification (e.g. pesticide use and habitat loss) as a plausible cause.

It was disappointing, but also important, to find out that many suitable areas failed to maintain populations of this butterfly. Why is the ghost butterfly absent from larger and well-preserved rural forests, while occurring in an urban forest fragment? This is puzzling. The most striking difference we found between these fragments is that all rural fragments we surveyed are surrounded by a matrix of sugarcane that is burned before harvesting, and perhaps during the ghost butterfly’s development they could be subjected to higher particulate pollution in rural fragments.

Pre-harvest burning of sugarcane is a widespread practice – the crops are burned in order to facilitate the harvesting process. The resulting smoke contains harmful gases and tiny particles. Insects can be sensitive to changes in air quality due to the direct way the air enters cells inside their body; they breathe via spiracles, valve-like openings on the outside of their exoskeleton. These openings connect to internal tracheal tubes that form a branching network that reach every part of the insect’s body. We think the effects of the pre-harvesting burning might have a negative effect in the ghost butterfly population, and may have previously been neglected.

It is noteworthy that the proportion of silicon dioxide (SiO2) in the sugarcane ashes is quite high (Le Blond et al. 2010) and could act as insecticide on herbivores (Edwards & Schwartz, 1981). The deposition of particulate, with a high amount of silica, on leaves inhibits feeding, which probably occurs via  physical action by wearing down the mandibles due to the abrasiveness of ashes/dust. Ashes could also cause the impairment of the spiracular function leading to respiratory stress (Elizalde 2014).

Dorsal and ventral views of male ghost butterfly. Photo by Andre V. Lucci Freitas.

The wider implications that the pre-harvest burning of sugarcane might have an impact on biodiversity remains speculative, yet plausible. The presence of a population of butterflies in one place, versus absence at several other places, does not provide unequivocal support for the assumed drivers of rarity. Indeed, the full extent of the effect of smoke pollution still needs to be investigated. Unambiguous evidence of the mechanism we suggest would require some experimental manipulation e.g.  transplants of caterpillars/adults to fragments surrounded by pasture, or experimentally smoking caged individuals using sugar cane residue.

We suggest that the long-life cycle of the ghost butterfly makes it especially sensitive to the sugarcane burning pollution. In this sense, it is interesting to highlight that the endangered M. menelaus eberti occurs in one larger rural fragment – Gargau. This species has multiple generations per year (Andre V. Lucci Freitas, personal communication).

Of course, there could be a number of other hypotheses for causal agents of decline, but in these cases, one would need to show change in abundance through time, and the causal agent of decline. Monitoring ghost butterfly population in urban areas, and comparing these to populations in rural forest remnants is essential to provide a foundation for the assessment of suitable habitats and elucidate the key drivers affecting population dynamics of the ghost butterfly within the Brazilian Atlantic forest.

Our paper shows the importance of native urban forest remnants for conservation i.e. unexpected sanctuaries given the pollution found in cities. Whether urban pollution will drive these populations to evolve, or disappear into oblivion, remains unknown. Human activities have a profound effect on biodiversity and our study serves as a warning regarding the many, often subtle, ways that these activities can cause rarity of once common species.

References

Dean, W. (1995) With broadax and firebrand: the destruction of the Brazilian Atlantic forest. University Press of California.

Edwards, J.S. & Schwartz, L.M. (1981) Mount St. Helens ash: a natural insecticide. Canadian Journal of Zoology 59, 714–715.

Elizalde, L. (2014) Volcanism and arthropods: a review. Ecologia Austral 24, 3–16.

Hallmann, C.A. et al. (2017) More than 75% decline over 27 years in total flying insect biomass in protected areas. PLoS ONE 12, eo185809.

Le Blond, J.S. et al. (2010) Generation of crystalline silica from sugarcane burning. Journal of Environmental Monitoring 12, 1459-70

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