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Trends and Progress in Studying Butterfly Migration
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Shawan Chowdhury1,2,3*, Myron P. Zalucki1, Tatsuya Amano1, Tomas J. Poch1, Mu-Ming Lin1,4, Atsushi
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Ohwaki5, Da-Li Lin1,6, Li Yang7, Sei-Woong Choi8, Michael Jennions9 & Richard A. Fuller1
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* Corresponding author (s.chowdhury@uqconnect.edu.au),
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ORCID: https://orcid.org/0000-0003-2936-5786
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1School of Biological Sciences, The University of Queensland 4072, Australia
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2Institute of Biodiversity, Friedrich Schiller University Jena, Jena, Germany
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3German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Leipzig, Germany
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4School of Environmental Science and Engineering, Southern University of Science and Technology.
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1088 Xueyuan Ave, Nanshan, Shenzhen, Guangdong Province, China, 518055
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5J. F. Oberlin University, 3758 Tokiwa-machi, Machida, Tokyo, 194-0294 Japan
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6Endemic Species Research Institute, Council of Agriculture, Executive Yuan. 55244 No 1, Ming-Shen
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East Rd, Jiji, Nantou, Taiwan
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7School of Life Science, Sun Yat-sen University, No. 135, Xingang Xi Road, Guangzhou, 510275, P. R.
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China
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8Department of Environmental Education, Mokpo National University, Muan 58554, Jeonnam, South
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Korea
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9Division of Ecology and Evolution, Research School of Biology, The Australian National University,
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Canberra, Australian Capital Territory 2600, Australia
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Abstract
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Several hundred butterfly species show some form of migratory behaviour. Here we identify how
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the methodologies available for studying butterfly migration have changed over time, and document
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geographic and taxonomic foci in the study of butterfly migration. We review publications on
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butterfly migration published in six languages (English, Simplified Chinese, Traditional Chinese,
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Japanese, Korean, and Spanish), summarise how migration in butterflies has been studied, explore
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geographic and taxonomic patterns in the knowledge base, and outline key future research
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directions. Using English search keywords, we found only 58 studies from Asia; however, after
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searching in local languages, we found an additional 99 relevant studies from China, Japan, and
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Taiwan. Overall, butterfly migration studies are mostly concentrated in North America and Europe,
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with only 4.6% from Africa. Most studies focus on three species: monarch (Danaus plexippus),
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painted lady (Vanessa cardui) and red admiral (Vanessa atalanta). About 62% of publications are
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focused on the monarch, with nearly 50% of migratory butterflies mentioned in no more than a
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single paper. Several research methods have been applied to ascribe migratory status and to study
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the physiology, neurobiology, and ecology of migration; however, virtually all this research is
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focused on a handful of species.
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Implications for insect conservation
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There remain hundreds of species for which we do not understand the full seasonal pattern of
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movement, flight destinations, wintering, or breeding grounds. A full understanding of movement
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ecology and migratory connectivity is needed to effectively conserve migratory butterflies.
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Keywords
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Geographic bias, literature trend, methodological advancement, migration ecology, monarch,
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taxonomic bias
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Introduction
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Migration is a widespread phenomenon among animals, often timed to exploit seasonal resource
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availability, with periodic movement from a habitat that has become unsuitable (Dingle, 2014;
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Liedvogel et al, 2011). Migration can reduce the burdens of parasitic infections and disease in a
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population by allowing individuals to escape from contaminated habitats and leave infected
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individuals behind: migratory butterflies with sub-lethal infections are less likely to migrate and/or
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are less likely to complete the journey (Bartel et al, 2011). Many migratory species are declining,
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mostly due to habitat destruction, overexploitation of resources, and climate change (Wilcove and
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Wikelski, 2008), although warming is likely to have positive effects in some locations, given the
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diveresity and abundance of some migratory Lepidoptera can also increase with the increasing
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temperature (Sparks et al, 2005, 2007).
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Conserving migratory species is particularly challenging because threats occurring at any location
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along the migratory route and at any stage of the life cycle of a migrant can impact the entire
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population. This means that a whole series of intact habitats, perhaps in different jurisdictions,
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needs to be protected (Wilcove and Wikelski, 2008). Understanding the patterns of spatial
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connectivity is central to conserving migratory species (Webster et al, 2002; Wilcove and Wikelski,
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2008; Gao et al, 2020). While significant progress has been made in characterising and
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understanding migration in birds (Faaborg et al, 2010; Robinson et al, 2010), less is known about the
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ecology and conservation of migratory butterflies, except for a few well-known migrants (e.g,
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monarch, painted lady; Chowdhury et al, 2021c). Migratory butterflies occur disproportionately in
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tropical rainforests (Chowdhury et al, 2021d), where deforestation is proceeding rapidly (Sodhi et al,
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2010). More research is needed to determine if any migratory butterflies are at acute conservation
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risk at any stage of their life cycle. Further, Chowdhury et al. (2021c) identified 13 lines of evidence
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that were used to ascribe migratory status of butterfly migrants. However, only a single line of
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evidence has been used for 92% of all diagnoses of migration in butterflies, and more than three
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lines of evidence available for only 10 species, all Pieridae or Nymphalidae. Here, we briefly review
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the history of the study of migration in butterflies, explore some of the geographic and taxonomic
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foci of that work, and outline some future research directions.
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Insects are the most speciose group on earth (Gaston et al, 1991; Stork et al, 2018), and provide key
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ecosystem functions and services, as pollinators, herbivores, predators, and decomposers (Didham
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et al, 1996; Yang and Gratton, 2014; Satterfield et al, 2020). They also occur in human-modified
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ecosystems, often as vectors of human, livestock, or plant diseases, or as herbivores that directly
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damage crops (McGeoch, 1998; Walther et al, 2002; Dingle, 2009; Reynolds et al, 2006). Every year,
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many trillions of insects migrate from one part of the world to another, often crossing international
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borders (Chapman et al, 2011). For example, nearly 3.5 trillion insects traverse the southern United
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Kingdom every year, transferring more than 3,000 tons of biomass (Hu et al, 2016).
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Although our current understanding of insect migrations is limited for most taxa, especially for
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pollinating insects, butterflies are, to some extent, an exception (Brower et al, 2006; Meitner et al,
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2004; Pierce et al, 2014; Satterfield et al, 2020; Chowdhury et al, 2021c, d). This might be because
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they are diurnal, brightly coloured, and fly relatively close to the ground, making their migration
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easier to detect and observe (Dingle, 2014). Chowdhury et al. (2021c) reported >3% of butterfly
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species (N=568) migrate, but this is probably an underestimate, as only papers in English were
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reviewed for that study and the rate of reporting new diagnoses of migration in butterfly species
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does not appear to have declined between 1831 and 2020. Although studies on butterfly migration
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have been increasing, the literature remains scattered.
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Our aims in this paper are to (i) review the history of studies on migration in butterflies, (ii) explore
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the geographic, taxonomic, and temporal patterns in the available studies, and (iii) outline some
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future research directions. Information on butterfly migration is often published in non-peer-
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reviewed journals (i.e, grey literature) (Chowdhury et al, 2021c), and up to one third of scientific
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documents related to biodiversity conservation are published in languages other than English
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(Amano et al, 2016a). Ignoring the non-English-language and grey literature can severely bias our
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understanding (Egger et al, 1997; Møller and Jennions, 2001; Jennions and Møller, 2002a, b; Amano
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and Sutherland, 2013; Amano et al, 2021; Konno et al, 2020). Here we compile a global knowledge
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base on butterfly migration from multiple sources, including peer-reviewed papers and grey
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literature (including web articles) that are available in English or five other languages. To identify
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knowledge gaps and provide a pathway to advance our understanding of butterfly migration, we
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analyse trends in existing studies (geographic, taxonomic, and temporal trends), describe the
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chronological development of how butterfly migration has been studied, and point out where
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further research might be fruitful.
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Defining butterfly migration
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Butterflies are small-bodied, usually living as adults for only a few weeks to a year (Oberhauser &
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Solenski, 2004), with the distances they travel during migrations varying greatly among species
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(Dingle, 2014). While many vertebrates migrate thousands of kilometres and individuals generally
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make the return journey, sometimes repeatedly throughout their lives, the situation is more
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complex for invertebrates (Malcolm et al, 1993; Stefanescu et al, 2013; Chapman et al, 2015;
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Malcolm and Slager, 2015; Ruiz Vargas et al, 2018; Menz et al, 2019; Chowdhury et al, 2021c).
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Butterfly migration usually entails multigenerational movement, with flights by each generation
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continuing for periods of several days to weeks (Malcolm et al, 1993; Holland et al, 2006; Nesbit et
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al, 2009; Dingle, 2014; Talavera et al, 2018). For example, North American monarch butterflies travel
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5,000-7,000 kilometres per year, but it takes 3-5 generations to complete the full annual cycle, with
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the spring migrants undertaking the bulk of journey – from the Trans Volcanic Plateau of Mountains
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in Mexico to different parts of the USA and Canada (Dingle et al, 2005; Brower et al, 2006; Malcolm,
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2018).
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It is challenging to define migration in butterflies, and several definitions have been offered
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(Chowdhury et al, 2021c). Migration encompasses phenomena at different levels of biological
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organisation (physiological, individual/behavioural, population/spatial/ecological) but is often
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characterized as a behaviour that has ecological consequences (Dingle and Drake 2007, Chapman et
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al. 2015). Perhaps one of the most useful, and the one we have employed here, remains that of
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Kennedy (1985); ‘Migratory behaviour is persistent and straightened-out movement effected by the
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animal’s own locomotory exertions or by its active embarkation on a vehicle. It depends on some
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temporary inhibition of station-keeping responses but promotes their eventual disinhibition and
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recurrence’.
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Literature search
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For the literature search, we used (i) Google Scholar (https://scholar.google.com) with the keywords:
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‘Butterfly migration’ and ‘Migratory butterflies’ and checked the first 100 pages, (ii) PubMed
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(https://pubmed.ncbi.nlm.nih.gov) with the same key words, (iii) Web of Science (Web of Science
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Core Collection; https://apps.webofknowledge.com) using the search string TS=(Butterf* AND migr*)
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with 1900-2020 as the year range, and (iv) Google (https://www.google.com) using the same
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keywords that we used for Google Scholar. When scanning relevant studies, we noticed that many
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authors published their work in local journals, especially the following four: Atalanta (Germany),
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Phegea (Belgium), Bulletin of the Allyn Museum (USA), and the Journal of the Bombay Natural
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History Society (India). Therefore, we further checked all the issues of these four journals to make
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the review more comprehensive. Similarly, Chowdhury et al. (2021c) obtained some studies from the
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South-East Asia and the Neotropical regions, including publications in non-English languages. We
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therefore conducted searches in five additional languages. Using the equivalent of ‘Butterfly
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migration’ and ‘Migratory butterflies’ we searched in Google Scholar for papers in Simplified (‘蝴蝶
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迁徙’, ‘蝶 类 迁徙’, ‘迁徙性蝴蝶’ and ‘迁徙性蝶类’’) and Traditional (‘蝴蝶 遷徙’, ‘蝶類 遷徙’, ‘遷
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徙性 蝴蝶’ and ‘遷徙性蝶類) Chinese, Japanese (‘チョウ’ ‘蝶’, ‘渡り’, ‘移動’), Korean (‘이주’ and
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‘이주성 나비’) and Spanish (‘Mariposas migratorias’ and ‘Migración de mariposas’). Because some
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of the relevant Japanese literature may not be found using the keywords, ‘蝶, 渡り’ and ‘移動’, we
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made an additional search using the keywords, ‘昆虫’ and ‘海上’.
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We retained 926 studies, published between 1833 and 2020, that mentioned butterfly migration in
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the abstract, of which 581 are in English, 246 in Spanish, 59 in Japanese, 29 in Simplified Chinese,
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and 11 in Traditional Chinese. The complete bibliography is provided in the supplementary section
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(Table S1). For each study, we recorded the title and year published, the subject species, geographic
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location, and the techniques used to establish (or discuss) migratory behaviour, as well as any
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information provided on parameters such as migratory behaviour, density and distance travelled. To
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assess geographic and taxonomic patterns, we used the locality and species information from each
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paper to group them into six continents (North America, South America, Europe, Africa, Asia, and
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Oceania).
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To investigate whether interest in butterfly migration is increasing, we compared the number of
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papers specifically about butterfly migration to those on any aspect of butterfly biology between
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1990 and 2019. Using Web of Science Core Collection (Advanced Search), we searched for papers
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using two keywords: ‘TS=(Butterf* AND migr*)’ for migratory butterflies, and ‘TS=(Butterf*)’ for
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butterflies. We only considered English-language papers, recognising that our results for this search
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might largely reflect patterns in North America or Europe where most English-language papers were
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located.
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Chronological development of studying butterfly migration
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While lepidopterists have been recording insect movements for centuries, interest in butterfly
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migration only began in earnest at the beginning of the 20th century. Movement of millions of
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migratory butterflies at low altitude intrigued both professional lepidopterists and amateurs around
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the world, but it took a few more decades for researchers to start utilising formal scientific
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techniques to advance their research (see below; Fig. 1b). Here, we summarise studies on butterfly
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migration, based largely on the English-language literature, with some inputs from key non-English-
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Language studies, to reveal how research has developed, starting with the first record of a butterfly
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migrant, the discovery of overwintering sites, then the various methods used to track individuals and
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ascertain navigation, and finally the recent development of genetic tools and analyses.
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Increasingly sophisticated methods have become available to study different aspects of butterfly
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migration (Fig. 1). The first major work on butterfly migration was by C. B. Williams, who
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summarized previous records and observations up to 1930 and listed 217 migratory butterflies from
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around the world (Williams, 1930), of which 64 were from India and Sri Lanka (Williams, 1927, 1938,
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1939a), some from the USA, Guyana, and Mexico (Williams, 1939b), and the rest from Europe, Asia
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and Australia (Williams, 1939a, 1957; Williams et al, 1942). Torben B. Larsen described 137
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migratory butterflies from tropical Africa and Asia in a series of works published between 1975 and
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2005 (Larsen, 1975, 1977, 1982, 1984, 1986, 1987, 1988a, 1988b, 1992a, 1992b, 1992c, 1995, 2004;
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Larsen et al, 2005). Major early works on the migratory butterflies of South America were published
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by William Beebe, who described migration in 68 species (Beebe, 1949a, 1949b, 1950a, 1950b,
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1951). Most of these early studies diagnosed migration on the basis of visual observations of
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directional movements.
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a) Recording butterfly migration
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Egyptian hieroglyphs dated at >3,500 years old reveal local knowledge of the lesser wanderer (also
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known as African queen, and plain tiger, Danaus chrysippus, Haynes, 2013), a known migrant (Smith,
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2014), although it is doubtful whether the hieroglyphs specifically relate to the phenomenon of
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migration. The earliest evidence of the sighting of migrating monarch butterflies was by Christopher
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Columbus in eastern Mexico (Doubleday et al, 1846; Brower, 1995). One of the earliest observations
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of mass migration in butterflies was made by Charles Darwin, on December 6, 1833, off the coast of
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Argentina (Darwin, 1839):
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“One evening, when we were about ten miles from the Bay of San Blas, vast numbers of butterflies in
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bands or flocks of countless myriads, extended as far as the eye could range. Even by the aid of a
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glass it was not possible to see a space free from butterflies.”
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On the other side of the Atlantic, in Ireland, Wolfe (1899) listed some migratory butterflies and their
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seasonal trends (Shannon, 1916). Wright (1906) was the first to note the seasonal fluctuation of
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migrations: "the substitution of the abnormal female for the normal; the temporary or permanent
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disappearance of an entire species, and the unaccountable appearance of lost or unknown species; in
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fine, the change from one state of things to another state” (Kellogg, 1907; Wright, 1906).
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b) Discovering overwintering sites
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Thaxter (1880) was the first to describe the overwintering sites of various butterflies including
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monarchs, along the California coast. “The trees were literally festooned with butterflies within an
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area of about an acre, and they were clustered so thickly that the trees seemed to be covered with
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dead leaves”. The failure to find consistent overwintering sites in the east was confusing, and it took
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nearly a century to resolve the story (Malcolm and Zalucki, 1993; Brower, 1995); an overwintering
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site of the monarch butterfly was eventually discovered in the Trans Volcanic Plateau of Mountains
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of Mexico by Kenneth and Catalina Brugger in 1975 (Urquhart and Urquhart, 1978). They were part
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of a team led by Fred Urquhart who had been working on the problem for nearly 38 years, which
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included 24 years of tagging studies. The team included interested and dedicated members of the
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public (pioneer citizen scientists). Urquhart and Urquhart hypothesized that migrants from the
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breeding areas of the Great Plains region overwinter in the western mountains of Mexico and those
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from breeding areas east of the Great Plains region overwinter in the eastern mountains (Urquhart
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and Urquhart, 1978). Later, Lincoln Brower, William Calvert and colleagues mapped the locations of
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the major overwintering sites of the eastern population atop a few mountain ranges in the centre of
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the Transverse Neovolcanic Belt of Michoacán, Mexico (Brower, 1995; Reppert and de Roode, 2018).
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Overwintering in aggregations and migration is a characteristic of many danaines (e.g, Danaus
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plexippus, lesser wanderer (Danaus chrysippus), blue tiger (Tirumala hamata); Kitching and
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Scheermeyer, 1993). During the 1960s, several researchers began to review the status of butterfly
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migration from various locations around the world (Broekhuysen, 1960; Urquhart, 1960; Brower,
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1961). Wang and Emmel (1990) described four overwintering sites of nine Danainae in remote areas
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of Taiwan and observed thousands of roosting migratory butterflies. Scheermeyer (1987) described
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a similar phenomenon in Australia. More recently, James and James (2019) described 33
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overwintering sites of monarchs from Australia. In addition, these authors described the
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movements, seasonal distributions, and breeding ranges of butterflies in their respective study
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areas.
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c) Tracking migratory butterflies
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Tracking the migratory movements of insects is challenging but becoming more efficient and
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effective. The direction of migration can be established using simple observations and/or mark-
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recapture. Levin et al. (1971) used only the angle of arrival at, and departure from, a point to define
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the flight direction of bees and butterflies. Measuring the vanishing angle is widely used to establish
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flight directions (i.e, the cardinal direction of the released specimen when it disappears from view)
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(Srygley, 2001; Srygley et al, 2006). Brussard and Ehrlich (1970) and Baker (1978) used different two-
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dimensional techniques to track butterfly movements, while Zalucki et al. (1980) used theodolites to
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identify the direction of flight in three-dimensions, although the work was limited to only 20-25 m.
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Nowadays, radio-tracking (Patterson et al, 2008; Knight et al, 2019), harmonic radar (Cant et al,
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2005; Ovaskainen et al, 2008), and even spatial population dynamics models (Hanski and Thomas,
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1994; Flockhart et al, 2015) have been used to track, record, analyse or infer movement paths.
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Nearly all these techniques are limited to describing short-range movement behaviours.
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i) Mark-release-recapture
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Mark-release-recapture procedures can identify the direction and distance a butterfly has moved
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but they are labour intensive, and recapture rates are typically very low. For monarch butterflies,
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hundreds of thousands of adults have been tagged in the summer breeding range in the last five
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decades, but only a few hundreds to thousands then recovered from overwintering sites in Mexico
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(Monarch Watch Organization, University of Kansas, https://www.monarchwatch.org/). Even so, this
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work has established the general direction of migratory flights, the connection between summer and
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wintering sites, and provided an estimate of population size and migration mortality (Taylor Jr. et al,
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2020). Fletcher (1936) first described a tagging process for butterflies: "A small patch on the upper
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surface of the right forewing is rubbed clear of scales and a small label, written in Indian ink on
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tracing paper, is attached to it with Canada balsam; the adhesive is allowed to harden and the
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butterfly then released.” This process was very time-consuming and only achievable when sample
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sizes were small. Urquhart later described an improved procedure to mark migratory butterflies
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(Urquhart, 1941, 1960; Urquhart and Urquhart, 1978). Urquhart (1941) adopted the method by
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punching a small hole through the right forewing near the base of the latter and immediately behind
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the stout radial vein, which is still widely used around the world to track butterfly migration. For
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example, Kanazawa et al. (2015) described the migration of Chestnut Tiger butterfly (Parantica sita
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niphonica) from Japan to Hong Kong using a mark-release-recapture process.
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ii) Radar studies
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Migrating insects can fly at high altitudes, up to 2,000 or 3,000 meters above the ground
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(Gatehouse, 1997; Mikkola, 2003; Chapman and Drake, 2019); however, most migration is below
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1500 meters (Drake and Reynolds, 2012). Stefanescu et al. (2013) showed that painted lady and
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other migrant Lepidoptera can take advantage of favourable winds and fly from the ground to
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altitudes over 1,000 meters; however, many butterfly migrants travel close to the ground where
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their airspeeds are higher than the wind speed, allowing them to make progress in a seasonally
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appropriate direction
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even when there is a contrary wind (Srygley and Dudley, 2008).
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Identification of insects flying at high altitudes based on radar echoes started in 1949 (Crawford,
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1949), and the detection of a massive locust swarm followed in 1954 (Rainey, 1955); however, it
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took more than a decade to deploy radar specifically to observe locusts. At the end of the 1960s,
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radar was deployed to observe insect movements in Africa and over the next few decades there was
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a surge of radar-derived information, mainly on night-flying insects including locusts and moths
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(Schaefer, 1969; Haskell, 1970; Richter et al, 1973; Vaughn, 1985; Chapman and Drake, 2019). It still
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took several years to establish migration histories for individual butterfly species (Stefanescu et al,
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2013; Chapman and Drake, 2019). With the help of radar and citizen-science data, we now know
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that high-altitude migration is common for painted lady butterflies in the UK (Satterfield et al, 2020).
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About seven million painted lady butterflies migrated from southern Europe to the UK during spring
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2009, and 14 million returned southward during fall, when they completed a 15,000-km annual
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migration requiring six generations (Stefanescu et al. 2013; Satterfield et al, 2020). However, most
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radar investigations of insect migration have been directed at species other than butterflies
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iii) Interception traps
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During the mid-1970s, Walker successfully established malaise traps as linear barriers in the Florida
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Peninsula (USA) to observe the movement of migratory butterflies. He described the northward and
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southward movements of 10 butterfly species, and showed that malaise traps can continuously and
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effectively monitor insect migration within the boundary layer (Walker, 1978). The original traps
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were made of polyester which cannot withstand strong winds and required frequent repair and
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replacement; a hardwearing-cloth trap overcame these problems. Traps could capture roughly 70%
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of passing migrants (Walker, 1985b). In the ensuing years, Walker further developed the traps and
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elucidated the full seasonal flight patterns of these migratory butterflies (Walker, 1985a, 1991, 2001;
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Walker and Lenczewski, 1989).
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iv) Natural markers
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Natural markers can be used to ascertain the natal origins of aggregated and moving migrants. For
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example, Malcolm et al. (1989) used cardenolide fingerprints. Monarch butterfly larvae ingest
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cardenolides from their hostplant - milkweeds, which is a toxic group of chemicals. Many species of
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North American milkweeds possess different proportions of these toxins, which remain intact in
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adult individuals. By extracting these from adult butterflies and visualizing them on a thin layer
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chromatography plate, they determined the ‘cardiac glycoside fingerprint’. Adults from different
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regions ingested different milkweed species, and have unique cardiac glycoside fingerprints. Using
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this method, it became clear that about 90% of monarchs in Mexico had developed on Asclepias
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syriaca – once the most abundant milkweed host in the midwestern US (Malcolm et al, 1989). One
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limitation of this approach is that some hostplant species contain a similar range of cardiac
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glycosides and some have none (Malcolm et al, 1989; Brower, 1995).
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When insects visit flowers, pollen may become attached to their bodies and it can be used to track
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long-distance insect migrations (Mikkola, 1971; Hendrix et al, 1987). Suchan et al. (2018) collected
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butterfly samples and meta-barcoded the transferred pollen to understand the migration of the
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painted lady. They collected 47 butterflies along the Mediterranean coast of Spain in spring, then
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separated pollen from butterfly-bodies followed by meta-barcoding (Suchan et al, 2018). There was
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pollen from 157 species of plants from 23 orders, most of which are insect pollinated. Most were of
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African-Arabian origin (73%) and 19% were endemic to that region, strongly suggesting that the
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butterflies migrate northward into southern Europe from Africa in the spring (Suchan et al, 2018).
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v) Isotopic analyses
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The stable isotopes of organic tissues are related to the site where an individual develops, which can
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be used to infer the most likely natal origin of migratory butterflies (Wassenaar and Hobson, 1998;
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Flockhart et al, 2015; Stefanescu et al, 2016; Talavera et al, 2018; Reich et al, 2021). For example,
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Wassenaar and Hobson (1998) confirmed the geographic natal origins and established wintering
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roost sites of monarchs from different regions by sampling and measuring the isotopic elemental
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composition (stable hydrogen (dD) and carbon (d13C) isotope ratios) of wintering monarchs in
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Mexico. They compared 597 overwintering monarchs from 13 roosting sites and measured
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background isotope ratios in the natal sites across their breeding range over a single migration cycle.
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This revealed that all the monarchs originated from the Midwest United States, although two
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colonies showed a more northerly origin (Wassenaar and Hobson, 1998). Flockhart et al. (2013,
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2015) subsequently used the technique to study the population dynamics and movement of
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monarchs in greater detail.
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vi) Flight chambers
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Early designs of tethered flight systems started in the 1950s, but it took many years for the
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procedures to be refined sufficiently for accurate interpretation (Krogh and Weis-Fogh, 1952;
343
Kennedy and Booth, 1963, 1964; Kennedy and Ludlow, 1974; Kennedy, 1985). Flight chambers
344
eventually revealed several important features of migratory behaviour (Kennedy, 1958, 1985),
345
paving the way for detailed studies on the duration and orientation (Mouritsen et al, 2013;
346
Mouritsen and Frost, 2002; Reppert et al, 2004) of migration flights. Tethered flight provides an
347
indication of the flight propensity of the migrants making it possible to study the migratory
348
15
motivation of insects in the laboratory (Minter et al, 2018; Mouritsen, 2018) in relation to the
349
environmental conditions experienced during development. Flight simulators were a key innovation
350
as they have allowed for experiments investigating preferred headings and response to navigational
351
markers and cues.
352
353
d) Physiological evidence of migratory individuals
354
Cecil G. Johnson studied differences in life history traits between migratory and non-migratory
355
butterflies, showing that (i) migratory females start their flight before ovarian development, (ii)
356
migrants are sexually immature in some cases, (iii) migratory individuals usually gain weight as they
357
fuel up for the long journey, and (iv) they have longer forewings than non-migrant individuals
358
(Johnson, 1963, 1966, 1969). This work suggested that distinctive physiological and
359
neurophysiological factors are associated with migration, and that ovarian development can be
360
initiated, prolonged, or suppressed depending on a range of environmental conditions. Recently,
361
Stefanescu et al. (2021) showed that the painted lady fulfils the oogenesis–flight syndrome, whereby
362
the pre-reproductive period is shorter during the migration period, the mating frequency is highly
363
correlated with the host plant abundance, and that mated females can locate potential breeding
364
areas. Additionally, Dudley and Srygley (1994) showed that the airspeeds of butterflies can be
365
predicted from morphological measurements under natural conditions.
366
367
e) Genetic analysis
368
Genetic techniques to study migration appeared in the mid-1970s, when Eanes and Koehn (1978)
369
collected monarchs from the USA and Canada and used electrophoretic alleles at six enzyme-loci as
370
genetic markers, and Wright’s F-statistics to analyse the genetic structure of the population. They
371
found significant allele frequency differences between migratory and non-migratory individuals
372
(Eanes and Koehn, 1978). In subsequent decades there was rapid improvement in the use of genetic
373
tools to uncover patterns of migratory connectivity (Sauman et al, 2005; Dingle, 2014; Zhu et al,
374
16
2008; Zhan et al, 2014; Xiafang, 2017; Freedman et al, 2021). Moreover, information about
375
expressed sequence tag resources (Zhu et al, 2008) and the monarch genome (Zhan et al, 2011) has
376
opened up the study of the genetic basis and evolutionary history of migration in monarchs, using a
377
variety of genetic markers including microsatellites (Lyons et al, 2012; Pierce et al, 2014; Pierce et al,
378
2015), and genome-wide nucleotide polymorphism (Nagano et al, 1993). Using amplified fragment
379
length polymorphism (AFLP), Brattström et al, (2010b) attempted to determine the specific
380
migratory routes of red admiral (Vanessa atalanta) in Europe. However, while there were significant
381
differences between study sites, there was no clear pattern in orientation (Brattström et al, 2008;
382
Brattström et al, 2010a,b). In 2011, MonarchBase (http://monarchbase.umassmed.edu) was
383
released to make the genome widely available (Zhan et al, 2011). Sequencing 101 Danaus genomes
384
around the world, Zhan et al. (2014) concluded that both Danaus plexippus and southern monarch
385
(D. erippus) have a common migratory ancestor.
386
387
f) Navigation
388
Migratory butterflies appear to use either a compass alone, or a map and compass (Dingle, 2014).
389
Several species of birds (Perdeck, 1958; Thorup et al, 2007; Chernetsov et al, 2008), the eastern
390
newt (Notophthalmus viridescens) (Phillips et al, 1995), the loggerhead sea turtle (Caretta caretta)
391
(Putman et al, 2011), and the spiny lobster (Panulirus argus) (Boles and Lohman, 2003) show true
392
navigation; migrating individuals know where they are heading and can compare their current
393
geographic location to the destination (Mouritsen and Frost, 2002; Gould and Gould, 2012). Other
394
migrants seem to use a vector navigation strategy (Mouritsen et al, 2013), where they do not
395
possess a map sense but orient in an inherited direction using just a compass system and a clock or
396
calendar (Gwinner and Wiltschko, 1978; Munro et al, 1993). A map sense indicates the relative
397
position of the destination from a current location, whereas a compass sense enables migrants to
398
travel in a particular direction (Guerra and Reppert, 2015).
399
400
17
It has been suggested that monarchs use both vector navigation (Calvert, 2001) and true navigation
401
(Rogg et al, 1999) to find their overwintering sites. However, whether migrant monarchs possess a
402
true map sense is debated (Mouritsen et al, 2013; Oberhauser et al, 2013). Using over five decades
403
of field data, Mouritsen et al. (2013) suggested that monarch butterflies use a vector-navigation
404
strategy (but see Oberhauser et al, 2013). Amongst the diurnal migrants (e.g, butterflies), a sun
405
compass involving skylight cues plays a key role in orientation. Here, individuals use cues such as the
406
sun’s azimuthal position and possibly daylight polarization patterns to orient, as seen in the painted
407
lady (Merlin et al, 2012; Nesbit et al, 2009; Reppert et al, 2010; Stalleicken et al, 2005). Migrating
408
monarchs use circadian clocks to adjust their directional flight throughout the day (Guilford and
409
Taylor, 2014; Reppert et al, 2010; but see Freedman et al, 2017; Ning et al, 2018). Some migrants
410
use a magnetic compass (inclination angle, polarity, and intensity) to orient (Lohmann, 2012;
411
Lohmann et al, 2012; Dreyer et al, 2018); although there is a debate as to whether southward-
412
migrating monarchs use a magnetic compass (Guerra and Reppert, 2015; Reppert et al, 2010).
413
414
Trends in migration literature
415
Although the importance of studying butterfly migration was recognised very early on (Brower,
416
1995), most research has focused on a few species, and is restricted to a limited number of regions
417
around the world (Chowdhury et al, 2021c).
418
419
a) Regional pattern
420
There is marked variation in the number of studies among continents; most English-language studies
421
on butterfly migration were from temperate or cooler regions, or from the Northern Hemisphere
422
(especially the USA), with far fewer from the sub/tropics, or the Southern Hemisphere (Fig. 2). Most
423
studies from North America were from the USA and most studies from Europe were from the UK.
424
18
However, by searching in four Asian languages and Spanish, we found another 345 relevant studies,
425
mostly on species in North America (162 Spanish-language studies), but also in South America (44 in
426
Spanish) and Europe (37 in Spanish), and Asia (99 studies in total: 59 in Japanese, 29 in Simplified
427
Chinese, 11 in Traditional Chinese, and 1 in Spanish, Fig. 2). This highlights the importance of
428
including non-English studies in literature reviews across the globe. Overall, most studies on
429
butterfly migration were from North America (548 studies, >50%), and only 4% (45 studies) were
430
from Africa.
431
432
b) Taxonomic pattern
433
The available studies are clearly biased towards a few species; the monarch (62% of the 926 studies),
434
painted lady (9.6%), and red admiral (5.8%) (Fig. 3). There were only six species (monarch, painted
435
lady, red admiral, common emigrant (Catopsilia pomona), lesser wanderer (Danaus chrysippus), and
436
common crow (Euploea core) with more than 30 studies, and 41 species with > 10 papers (all on
437
either pierids or nymphalids except for pea blue (Lampides boeticus, Lycaenidae), and long-tailed
438
skipper (Urbanus proteus, Hesperiidae)). Nearly 50% (271 species) of our recorded migratory
439
butterfly species have not been the subject of a thorough single study but are just mentioned once
440
in a paper. On the other hand, the monarch accounted for 62% of the studies (Fig. 3). Being an
441
invasive species that has spread well beyond its native range, the monarch butterfly figures
442
prominently wherever it is present.
443
444
445
Studies on the monarch dominate not only in North America (nearly 85% of all studies; Fig. 2), but
446
even in areas where monarchs do not migrate (e.g, Spain). Elsewhere in the world, studies were
447
biased towards other species. For example, painted lady and red admiral for Europe, lesser
448
19
wanderer and monarch for Africa and Australia, and chestnut tiger (Parantica sita), and common
449
crow (Euploea core) for Asia (see Supplementary Section (Table S1) for more details).
450
451
c) Publication trends
452
Overall, there was no significant yearly trend in the number of English-language peer-reviewed
453
papers on butterfly biology in general and those specifically on butterfly migration (χ² = 0.14; df = 1;
454
P = 0.7061; Generalized Linear Model with a Poisson distribution; Fig. 4a). The proportion of papers
455
on migratory butterflies ranged from 1-3%. On the other hand, the number of papers on monarchs
456
has increased significantly over the past 30 years (χ² = 37.223; df = 1; P < 0.00001; Generalized Linear
457
Model with a Poisson distribution; Fig. 4b), while the number of papers on non-monarch butterfly
458
species has not noticeably risen. In the last few decades, the North American migratory monarch
459
population size has declined by > 80%, starting in the 1990s (Semmens et al, 2016; Stenoien et al,
460
2018); this decline of an iconic species has probably prompted more research.
461
462
Conclusions and future directions
463
Our results show that studies on butterfly migration are concentrated in relatively few regions of the
464
world, and that only a few species have been studied in detail (monarch, painted lady and red
465
admiral). There was no increase in the number of publications on butterfly migration over the years;
466
although research on the Monarch has accelerated. We showed the potential importance of non-
467
English-language studies to better understand butterfly migration globally. Of course, there are
468
thousands of languages globally, and here, we considered only five non-English languages. Future
469
studies could consider a broader set of languages widely used for scientific studies (e.g, French,
470
German, Italian, Polish, Portuguese, Russian, and other non-European languages). Language
471
restrictions might have impacted our findings. For example, if our search was expanded into
472
20
German, French, and Portuguese, we might have located more studies from Europe, Africa, and
473
South America (Chowdhury et al, 2022). However, given we checked two regional journals (Atalanta
474
and Phegea; publishes studies in German and Dutch repetitively), we think that we have already
475
captured many German and Dutch studies. Similarly, although we used rigorous literature search
476
approaches to make the review as comprehensive as possible, it is inevitable that we missed
477
relevant papers with our keyword driven search approach. There is, however, no reason to believe
478
that this would introduce a systematic bias that would affect our overall conclusion.
479
Charismatic species, especially if also threatened, often get disproportionate research, and the
480
research using the latest techniques is often concentrated in advanced-economy countries. This sort
481
of ‘research bias’ is quite common in biology (Di Marco et al, 2017), but can hamper our
482
understanding of species ecology and conservation (Pyšek et al, 2008; Jennions et al, 2013; Holman
483
et al, 2015; Nuñez et al, 2021). We have identified both taxonomic and geographic biases in
484
published studies on butterfly migration in that most studies: i) cover North America and Europe,
485
with very few from the tropics or subtropics, and ii) focus on a small number of species. To reduce
486
bias, researchers could conduct more studies on migration in poorly studied species and regions to
487
identify the true prevalence of migration in butterflies. For example, a recent study has shown that
488
unlike migratory birds, seasonal movements between suitable and unsuitable habitats in migratory
489
butterflies appears most prominent in the tropics (Chowdhury et al, 2021d). In this review, we
490
identify a lack of studies in the tropics, suggesting there is an under-representation of migratory
491
species.
492
Although a recent review listed several hundred butterfly migrants (Chowdhury et al, 2021c), the
493
rate of discovery of new migratory species indicates that there might yet be thousands more.
494
Nevertheless, it is worth noting that there can be both migratory and non-migratory populations and
495
individuals within a species (Zhan et al, 2014; Slager and Malcolm, 2015; Vander Zanden et al, 2018).
496
To understand seasonal movements, it is essential to monitor across a species’ full geographic
497
21
distribution, a task for which active citizen science participation is likely to be highly beneficial
498
(Boakes et al, 2010; Mason et al, 2018; Soroye et al, 2018; Lloyd et al, 2020; Juhász et al, 2020;
499
Chowdhury et al, 2021a,b,d). For example, both amateur and professional ornithologists widely use
500
eBird, which has transformed the availability of bird data globally (Bonney et al, 2009; Sullivan et al,
501
2009; Amano et al, 2016b). So how can we engage citizen science in the tropics? Nowadays,
502
iNaturalist, a citizen science project, is increasingly popular both among professional and amateur
503
naturalists (Callaghan et al, 2020). Citizen science tools, such as this, can widen the coverage of
504
space and species in data collection; and collating and analysing the resulting data will help to
505
identify which species are, in fact, migratory. For this reason, maximising funding and shifting
506
research effort towards tropical regions could enable broader discovery of migration in butterflies.
507
In many countries, funding is more readily available for insects of economic significance, such as
508
pests and pollinators. Future studies could assess the disparity in funding amount and prioritise
509
funding for species that are at elevated extinction risk.
510
Future research could focus on identifying, tracking, and understanding the navigation of butterfly
511
migrants. Time honoured techniques such as mark-release-recapture can be used to calculate travel
512
distances, and whether the distance and overall direction of movement is associated with changes in
513
seasonal resources; isotopic analysis can be used to identify the origin of individuals (Vander Zanden
514
et al, 2018; Wassenaar and Hobson, 1998); flight chamber experiments can be used to record flight
515
duration of butterflies and differentiate migrants and non-migrants and even differences in
516
orientation (Mouritsen and Frost, 2002; Reppert et al, 2004; Minter et al, 2018); radars can be used
517
in hotspot regions to determine the seasonal flow of movements (Chapman et al, 2011; Chapman et
518
al, 2015; Hu et al, 2016; Stefanescu et al, 2021); female butterflies can be collected and dissected to
519
check the status of their ovarian development (Johnson, 1963); genomic resources such as EST-
520
based microarray analyses, transcriptome libraries and single nucleotide polymorphism (SNP)
521
marker sets can be used to determine migration routes (Brattström et al, 2010a; Brattström et al,
522
2010b; Liedvogel et al, 2011); and ecological niche and movement modelling can uncover spatial
523
22
patterns of seasonal occurrence and habitat use in migratory butterflies (Zalucki et al. 2016; Grant et
524
al, 2018; Chowdhury et al, 2021a, d).
525
During migratory flights, monarch butterflies adjust their flight altitude and vectors by flapping and
526
gliding (Gibo & Pallett, 1979; Gibo, 1981), but there is no information on whether this occurs in
527
other migratory butterflies. Recent studies have shown that some long-distance migratory
528
butterflies use air currents (Stefanescu et al, 2007; Srygley & Dudley, 2008; Chapman et al, 2010; Hu
529
et al, 2016, 2021) but little is known about the cost of migration, metabolism of flight fuels, or how
530
migratory butterflies counter overheating. Moreover, there are some phenotypic differences,
531
especially in traits linked to migration, between eastern and western monarchs, despite genetic
532
studies indicating these populations are closely related (Freedman et al, 2021). Future studies could
533
focus on assessing the reasons for these differences between eastern and western monarchs.
534
Similarly, migratory butterflies can be tracked using natural markers such as cardenolides (Malcolm
535
et al, 1989; Brower, 1995). It would be interesting to extend this method to other Danainae
536
butterflies that feed on Apocynaceae.
537
While undertaking migratory flights, migrants often cross multiple regions. This continuous
538
movement makes them vulnerable to anthropogenic threats and complicates their conservation
539
(Martin et al, 2007; Runge et al, 2014; Reynolds et al, 2017; Malcolm, 2018; Chowdhury et al,
540
2021a,d; Juhász et al, 2020). Due to extensive anthropogenic pressure and human-induced climate
541
change, insects, including butterflies, are declining worldwide (WallisDeVries et al, 2011; Fox, 2013;
542
Hallmann et al, 2017; Habel et al, 2019; Sánchez-Bayo and Wyckhuys, 2019; Wagner, 2020). It is
543
notable that populations of more than half of migratory birds have declined in the last 30 years,
544
suggesting that, in general, migratory species are at greater risk than sedentary species (Kirby et al,
545
2008). The few available time series analyses have shown some migratory butterfly populations to
546
be stable, while others are declining. For example, while the North American migratory monarch
547
population has dramatically declined in the last few decades (Stenoien et al, 2016; Zylstra et al,
548
23
2021), populations of painted lady, red admiral and clouded yellow (Colias croceus) have remained
549
relatively stable (Fox et al, 2015; Hu et al, 2021). However, it should be noted that time-series data
550
are rare for most migratory butterflies, and unavailable from most parts of the world.
551
According to the Goal-2 of the post-2020 biodiversity framework, area-based conservation measures
552
and ecosystem-based approaches (“nature-based solutions”) are crucial to halt ongoing biodiversity
553
decline (Convention on Biological Diversity, 2020). Protected areas and other conserved areas have,
554
and will continue to be, a significant global tool to conserve threatened and endemic biodiversity
555
(Watson et al, 2014). However, there is no global assessments on protected area performance for
556
migratory butterfly conservation. Future studies could conduct such a gap analysis to assess whether
557
the current protected area networks are adequate to conserve migratory butterflies. This could lead
558
to new protected areas using spatial prioritization approaches to meet the post-2020 global
559
biodiversity framework targets. Future studies could also investigate whether protected areas better
560
help migratory butterfly populations to persist over time. Here, incorporating butterflies in the
561
monitoring plan of protected areas, creating baseline databases and using them for future
562
assessments will help us to assess the effectiveness of protected areas.
563
To implement effective migratory species conservation, holistic analyses across the entire
564
distribution are needed, since migrants require a chain of intact habitat (Runge et al, 2014; Gao et al,
565
2020). Ultimately, knowledge of seasonal movements, locations of stopover sites, protected area
566
coverage, and improved knowledge of the basic biology of migration in butterflies is needed to drive
567
successful conservation planning. Migratory butterflies perform a broad range of functions in
568
ecosystems including transferring biomass, transporting nutrients, and influencing resource fluxes
569
and food web structure (Bowlin et al, 2010; Dingle, 2014; Satterfield et al, 2020). If we are to
570
conserve them effectively, migratory butterflies will need far more attention than they currently
571
receive.
572
573
24
Statements and Declarations
574
The author has no conflicts of interest to declare.
575
576
Data Availability
577
The data that supports the findings of this study are available in the supplementary material of this
578
article.
579
580
Acknowledgement
581
The corresponding author is thankful to the Australian Government, the University of Queensland,
582
and the Centre for Biodiversity and Conservation Science for providing an International Research
583
Training Program Fellowship.
584
585
Author contributions
586
S.C. conceptualized the idea, S.C, M.P.Z, T.A. and R.A.F developed the method, S.C, T.J.P, M.M.L, A.O,
587
D.L.L, L.Y, and S.W.C. collected and summarised the data, S.C, did the analysis, everyone contributed
588
to the analysis, S.C. wrote the paper, everyone contributed to the writing of the paper.
589
590
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List of Figures
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Fig. 1 a) Chronological progression of different methodological approaches to studying butterfly
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migration (PE = population evidence), where the colour bar is representing the number of studies. b)
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Chronological development of key methods to diagnose migration in butterflies, where
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Fig. 2 The number of butterfly migration studies by language from each continent.
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Fig. 3 The number of butterfly migration studies in each continent for three different butterfly
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Fig. 4 Temporal trends in peer-reviewed English-language papers on butterfly migration. (a) Yearly
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48
Fig. 1
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49
Fig. 2
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1079
50
Fig. 3
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51
Fig. 4
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