Human-Impact Gradient and Butterfly Defaunation
By Neha Chowdhary, Suman Haldar, Writuparna Dutta, Supratick Seal, Madhumati Gupta, Puja Ray (Multitrophic Interactions and Biocontrol Research Laboratory, Department of Life Sciences, Presidency University)
Introduction
In the last few decades, our planet has experienced many changes in its environment due to several factors directly affecting the global climatic condition. Most of these changes, quite unfortunately, are adverse to the natural and human resources. Anthropogenic activities have accelerated the degradation or extinction of the resources, natural or biological. Loss of biodiversity is one of those global issues that violate even the existence of the entity of human beings themselves. Expansion of the agricultural grounds for food security issues along with urbanization is the major cause for habitat destruction of the plants and animals (Cohen 2010). Among the many anthropogenic modifications to earth’s ecosystems, habitat loss and degradation pose the most immediate threat to many biota. Using indicator models like butterflies and butterfly data, assessment of environmental status, ecosystem health etc. are done in a relatively shorter time and expenses. The present paper attempts to review the impact of human mediated environmental changes on butterfly species.
Butterflies As Bioindicators Of Environmental Changes
The butterfly is a diverse insect, found in many colours and sizes. These insects enhance the aesthetic value of the environments by their exquisite wing colours. As a wildlife indicator, butterflies tell us almost everything we need to know about the health of an ecosystem (Dobson 2012). Butterflies maintain the ecosystem by acting as pollinator, prey, biological pest control, and induce genetic variation in plants. However, human activities and global climate fluctuation destroy and affect the butterfly habitats. Rosin et al. (2012) studied the relative effects of habitat patch and landscape characteristics on butterflies in habiting calcareous grasslands in southern Poland. Butterflies species and abundance are positively affected by patch size and wind shelter.
Ecological Role Of Butterflies
Butterflies are considered as good ecological indicators for healthy ecosystem and for other invertebrate taxa (Kumar et al. 2009; Kremen 1994; Kremen 1992) and as surrogate representatives of environment quality changes. Butterflies maintain the ecosystem by acting as pollinator, prey, biological pest control, induce genetic variation in plants and enhance environmental beauty. They also can reduce the level of carbon dioxide by the intake of the host plants, which has absorbed carbon dioxide from the environment (Ghazanfar et al. 2016). Nectar produced from flower contains nutritious vitamins, lipids, sugar, amino acid etc. that is important food source for pollinators. Butterflies are also pollinators and visit the flower to feed on nectar; tiny scales on the butterfly bodies brush against anthers and pollen adhere to scales. Now the butterfly visit to another flower, the pollen that attach to its scales, brush in to the flower’s stigma. Adult and larval stages of butterflies provide food for number of animals such as birds, reptiles, amphibians etc. Eggs of some flies and wasps live as parasites inside caterpillar’s body and feed on it. Hence, maintain the food web in ecosystem by eating leaves and being eaten by predators. Some parasitic butterfly, like Niphanda fusca (Bremer and Grey, 1853), lay their eggs where ants tend herds of aphids. The eggs hatches as caterpillars and feed on the aphids (Ehrlich 1984) proving that caterpillars are also useful as biological pest control. Kearney (2015) point out that butterflies collect nectar from plant species, which induce genetic variation in the plants. Some butterfly species migrate over long distance and share pollens across plants which are far away from one another. This help plants to recover against disease and gives them a better chance at survival. They perform essential ecosystem services (Schmidt and Roland 2006), especially in the recycling of nutrients (N,P,K). Their larval stages feed on leaves of several wild plants found in the agricultural systems and therefore release their faeces that contain some amount of nutrients (Marchiori and Romanowski 2006).
Anthropogenic Effect On Butterfly
Human impact on environment or anthropogenic impact on the environment includes change to biophysical environment, ecosystem, biodiversity and natural resource caused directly or indirectly by humans, including global warming, environmental degradation, biodiversity loss, ecological crisis and ecological collapse. These also affect the population, diversity and ecological behaviour of butterflies. Increasing construction work, industrialisation by human results into the deforestation and destruction of the natural ecosystem, which leads to depletion of living habitat of butterflies, resource partitioning and add stress to their thriving population. Natural and human induced fires (Figure 1) change the diversity and composition of forest ecosystems thus impacting the butterfly communities, especially the ones with small, isolated populations are severely affected if their habitats are burned too frequently (Kwon et al, 2013).
Figure 1: Fires often change the diversity and composition of butterflies in forest ecosystems
Climate Change
Climate change causes shifts in geographical distributions of species (Parmesan and Yohe, 2003, Root et al. 2003) Such shifts are considered to be the results of (meta)population extinction at the equatorial range boundary, and poleward colonisation in regions where climatic conditions have newly become suitable (Opdam and Wascher 2004). Habitat availability and spatial cohesion of habitat patterns play a crucial role in the persistence of species under global temperature rise. Detrimental effects of climate change in fragmented habitat availability, habitat use and inter patch movement do not vary under the expected climate change regime. Thomas et al. (2001) show that such assumption may not be realistic, as they found a significant broadening of the range of habitats used by silver spotted skipper, Hesperia comma L., spreading towards the north–facing hill slope habitat that were previously climatically not suitable. Elevated atmospheric concentration of carbon dioxide reduces the viability of monarch butterflies, Danaus plexippus and increases parasite virulence by altering the phytochemical content in milkweeds (Decker et al, 2018).
Urbanization Gradient
Habitat loss and fragmentation are primary cause of species extinction. Urban and suburban sprawl have been identified as primary cause of habitat fragmentation. Urbanization has a negative impact on butterfly abundance and species richness. Such deleterious effects of urbanization have already been shown (Bergerot et al. 2011, Di Mauro et al. 2007). Several studies have shown that gardens represent food sources for butterflies (Toms et al. 2010, Vickery 1995). The strong positive effect of nectar offer index clearly supports these findings: Nectar offer probably determines the garden carrying capacity. Governmental policy on forestry, farming and road planning has great effect on the abundance and distribution of butterflies (Mubeen et al. 2016).
Alien Species Introduction Into Native Ecosystem
Humans introduce alien species to native environment intentionally (Eichhornia crassipes (Mart.) Solms native to tropical and subtropical America) and unintentionally (by ballast water transport), which become threat to native species. Alien species introduction and their biological invasion are today the second-largest global threat for biodiversity. Once introduced, exotic plant species can modify ecosystem composition, structure and dynamics, eventually driving native species to local extinction. Among the groups of organisms, most likely to be directly affected by exotic invasive plants are herbivorous insects, such as butterflies, which strongly depends on plants throughout their life cycle. There is a co-evolutionary relationship between butterflies and plants.
On one hand, butterflies may benefit from invasive plants if they provide additional or better quality food resources (e.g. more or higher quality of nectar; Graves et al. 2003, Jahner et al. 2011, Pearse and Altermatt 2013). On the other hand, butterfly may suffer from plant invasions if these replace beneficial native plant partners, attract predators or are toxic for the butterflies that feed on them (e.g. Tallamy and Shropshire 2009, Davis and Cipollini 2014).
Pollution Gradient
Three-fourth of the greenhouse gases are generated by the developed countries having only one-fifth of the global population (Intergovernmental Panel on Climate Change 1996). Increasing population result in increasing traffic congestion, electricity consumption etc. that increases the use of fossil fuels and concentrations of gases like carbon dioxide or oxides of sulphur and nitrogen (Cohen 2010). These gases result in senescence in host plants of butterflies that eventually results in anomalies in larvae and ovipositing females (Hellmann 2002). Even interestingly, the lifespan of the adult female butterflies are positively correlated with the length of the duration of the larval stage of it. This dietary period indeed depends upon the resource quality of the host plant which is off course dependent upon the environmental condition in which the host plant is thriving (Jervis et al. 2007).
Pesticides Effects On Butterflies
The use of pesticides on arable crops has profound harmful effects on farmland wildlife (Mellanby 1981). The use of herbicides with chemical fertilizers and drainage reduce the butterfly number indirectly by changing the unimproved grassland in to improved pasture. Thomas explained that mostly butterfly rich farmland habitat is unimproved grassland and therefore, herbicides usage reduces the butterfly population (Thomas and Harrison 1992). Neonicotinoids may be contributing towards the disappearance of butterflies from the countryside, according to the first scientific study to examine the effect of the controversial agricultural pesticides on British butterflies. Researchers found that 15 of 17 species, which commonly live on farmland – including the small tortoiseshell, small skipper and wall butterfly– show declines, associated with increasing neonic use.
Using population data from 1985 to 2012 gathered on more than 100 sites across the country, scientists at the universities of Stirling and Sussex, in partnership with butterfly Conservation and the Centre for Ecology and Hydrology, found that neonicotinoid use better explained steep population declines than other factors. Scientific studies have shown how neonics stay in the soil for years, leak into water and could be absorbed by wildflowers and grasses growing in field margins, which provide nectar for butterflies and food for caterpillars. The Essex skipper declined by 67% between 2000 and 2009 and the small skipper declined by 62% in the same period. Other common farmland butterflies too have suffered steep declines include the small tortoiseshell (64%), the wall brown (37%) and the large skipper (35%).
Conclusion
Butterflies maintain the ecosystem by acting as pollinator, prey, biological pest control, induce genetic variation in plants, and enhance environmental beauty, reduce the level of carbon dioxide in air. Wepprich et al. (2019) during 21 years of systemic monitoring of 81 butterfly species reported 2% yearly decline per year, resulting in cumulative 33% reduction in butterfly abundance. Butterfly population is declining rapidly and it is suggest that greater emphasis should be placed on management of habitat and better integration of protected areas. Farmers are encouraged to adopt polyculture-cropping systems integrated to good management of floral resources in the margins of field to offer habitat and nectar sources to butterflies in the farmland. Conservation of butterfly fauna in a small landscape, particularly in human dominated area, might be a good model for maintaining optimal habitat within fragments and with high plant diversity might be a very good option for the conservation of species (Sharma et al. 2012). Ultimately, environmental education is required which include awareness on ecology and biodiversity, practical involvement, understanding of the degree of the consequence and constructivism, which the mob encounters generally. The education must begin from the school to the aged citizens with enquiries and possibilities (Krasny et al. 2013). Moreover, flexible and non-political thinking and decision making is also required in parallel for the conservation of the biodiversity while reducing the negative impact induced by human (Parmesan et al. 2014).
References
1. Bergerot B, Fontaine B, Julliard R, Baguette M (2011). Landscape variables impact the structure and composition of butterfly assemblages along an urbanization gradient. Landscape Ecology 26(1): 83–94.
2. Cohen JE (2010) Beyond Population: Everyone Counts in Development (Report). Centre for Global Development. Working Paper-220.
3. Davis SL, Cipollini D (2014) Do mothers always know best? Oviposition mistakes and resulting larval failure of Pieris virginiensis on Alliaria petiolata, a novel, toxic host. Biological Invasions 16:1941–1950.
4. Decker LE, Roode JC, Hunter MD (2018) Elevated atmospheric concentrations of carbon dioxide reduce monarch tolerance and increase parasite virulence by altering the medicinal properties of milkweeds. Ecology Letters. 21 (9): 1353-1363.
5. Di Mauro D, Dietz T, Rockwood L (2007) Determining the effect of urbanization on generalist butterfly species diversity in butterfly gardens. Urban Ecosystems, 10(4):427–439.
6. Dobson F (2012) Butterflies act as wildlife indicators, warning us of ecosystem changes. Environmental news network.
7. Ehrlich PR (1984) The structure and dynamics of butterfly populations, The Biology of Butterflies, Academic Press, London 25-40.
8. Ghazanfar M, Malik MF, Hussain M, Iqbal R, Younas M (2016) Butterflies and their contribution in ecosystem: A review. Journal of Entomology and Zoology Studies 4(2): 115-118.
9. Graves SD, Shapiro AM (2003). Exotics as host plants of the California butterfly fauna. Biological Conservation 110(3):413-433.
10. Intergovernmental Panel on Climate Change (1996) Second assessment report. Climate Change. Cambridge University Press, New York. Volume: 1–3.
11. Jahner JP, Bonilla, MM, Badik KJ, Shapiro AM, Forister, ML (2011). Use of exotic hosts by Lepidoptera: widespread species colonize more novel hosts. Evolution: International Journal of Organic Evolution 65(9):2719-2724.
12. Jervis MA, Ferns PN, Boggs CL (2007) A trade-off between female lifespan and larval diet breadth at the interspecific level in Lepidoptera. Springer Science and Business Media BV Evolution Ecology. 21:307–323. doi 10.1007/s10682-006-102-3.
13. Kearney L (2015) How the Butterfly Can Shape an Ecosystem and Why We need to protect them, one green planet.
14. Krasny ME, Lundholm C, Shava S, Lee E, Kobori H (2013) Urban landscapes as learning arenas for biodiversity and ecosystem services management. Urbanization, Biodiversity and Ecosystem Services: Challenges and Opportunities: A Global Assessment. doi 10.1007/978-94-007-7088-1_30.
15. Kremen C (1992) Assessing the indicator properties of species assemblages for natural areas monitoring. Ecological Applications 2(2): 203–217.
16. Kremen C (1994) Biological inventory using target taxa: a case study of the butterflies of Madagascar. Ecological Applications 4(3):407–422.
17. Kumar S, Simonson SE, Stohlgren TJ (2009) Effects of spatial heterogeneity on butterfly species richness in Rocky Mountain National Park, CO, USA. Biodiversity and Conservation 18 (3):739–763.
18. Kwon TS, Kim SS, Lee CM, Jung SJ (2013). Changes in butterfly communities after forest fire. Journal of Asia Pacific Entomology 16(4): 361-367.
19. Marchiori MO, Romanowski HP (2006) Species composition and diel variation of a butterfly taxocene (Lepidoptera, Papilionoidea and Hersperioidea) in a restinga forest at Itapu˜a State Park, Rio Grande do Sul, Brazil. Revista Brasileira de Zoologia, 23(2):443–454.
20. Mellanby K (1981) Farming and wildlife (The New Naturalist). London, Collins. ISBN 13:9780002192392.
21. Mubeen Ghazanfar, Muhammad Faheem Malik, Mubashar Hussain,Razia Iqbal, Misbah Younas,(2016). Butterflies and Ecosystem. Journal of Advanced Botany and Zoology, V3I1. DOI: 10.15297/JABZ.V3I1.04.
22. Opdam P, Wascher D (2004) Climate change meets habitat fragmentation: linking landscape and biogeographical scale levels in research and conservation. Biological Conservation 117:285–297.
23. Parmesan C, Williams-Anderson A, Moskwik M, Mikheyev AS, Singer MC (2014) Endangered Quino checkerspot butterfly and climate change:Short-term success but long-term vulnerability?. Springer International Publishing Switzerland. Journal of Insect Conservation. 19:185–204. doi 10.1007/s10841-014-9743-4.
24. Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42.
25. Pearse IS, Altermatt F (2013) Predicting novel trophic interactions in a non‐native world. Ecology Letters, 16, 1088–1094.
26. Root TL, Price JT, Hall KR, Schneider SH, Rosenzweig C, Pounds JA (2003) Fingerprints of global warming on wild animals and plants. Nature 421:57–60.
27. Rosin ZM, Myczko L, Sko´rka P, Lenda M, Moron, Sparks TH, Tryjanowski P (2012) Butterfly responses to environmental factors in fragmented calcareous grasslands. Journal of Insect Conservation 16:321–329.
28. Schmidt BC, Roland J (2006.) Moth diversity in a fragmented habitat: importance of functional groups and landscape scale in the boreal forest. Annals of the Entomological Society of America 99(6): 1110–1120.
29. Sharma V, Kumawat R, Meena D, Yadav D, Sharma KK (2012) Record of Tailed Jay Butterfly Graphium agamemnon (Linnaeus, 1758) (Lepidoptera, Papilionidae) from central Aravalli foothills, Ajmer, Rajasthan, India. Journal on New Biological Reports 1(1): 17-20.
30. Tallamy WD, Kimberley JS (2009) Ranking Lepidopteran use of native versus introduced biology. Conservation biology. DOI:10.1111/j.1523-1739.2009.01202.x.
31. Thomas CD, Bodsworth EJ, Wilson RJ, Simmons AD, Davies ZG, Musche M, Conradt L (2001) Ecological and evolutionary processes at expanding range margins. Nature 411:577–581.
32. Thomas CD, Harrison S (1992) Spatial dynamics of a patchily distributed butterfly species, Journal of Animal Ecology. 61:437-446.
33. Toms A., Narayanan SP, Babu, V, Padmakumar B. Arun ND, Jaisen J, Paul M, Deepa K, Jisha K.K. Jayasooryan, J. Rajnini, C. Rathy, P.N. Sreejith, G. Christopher, Thomas A.P. (2010). Butterfly fauna of the Mahatma Gandhi University Campus, Kerala and the strategies adopted for its conservation. 3rd Asian Lepidoptera Conservation Symposium and Training Programme, 25-29 Oct. 2010, Coimbatore, India.
34. Vickery M.L. 1995. Gardens: the neglected habitat. In: Pullin A.S. (ed.), Ecology and Conservation of Butterflies. Chapman & Hall, London pp. 123–134
35. Wepprich T, Adrion JR, Ries L, Wiedmann J, Haddad NM (2019) Butterfly abundance declines over 20 years of systematic monitoring in Ohio, USA. PLoS ONE 14(7): e0216270. https://doi.org/10.1371/journal. pone.0216270.
