Trends and Progress in Studying Butterfly Migration

doi:10.21203/rs.3.rs-1820553/v1

Download PDF

Systematic Review

Trends and Progress in Studying Butterfly Migration

https://doi.org/10.21203/rs.3.rs-1820553/v1

This work is licensed under a CC BY 4.0 License

Version 1

posted

You are reading this latest preprint version

Background

Several hundred butterfly species show some form of migratory behaviour. Here we identify how the methodologies available for studying butterfly migration have changed over time, and document geographic and taxonomic foci in the study of butterfly migration.

Method

We review publications on butterfly migration published in six languages [English, Simplified Chinese, Traditional Chinese, Japanese, Korean, and Spanish], summarise how migration in butterflies has been studied, explore geographic and taxonomic patterns in the knowledge base, and outline key future research directions.

Results

Using English search keywords, we found only 58 studies from Asia; however, after searching in local languages, we found an additional 99 relevant studies from China, Japan, and Taiwan. Overall, butterfly migration studies are mostly concentrated in North America and Europe, with only 4.6% from Africa. Most studies focus on three species: monarch [Danaus plexippus], painted lady [Vanessa cardui] and red admiral [Vanessa atalanta]. About 62% of publications are focused on the monarch, with nearly 50% of migratory butterflies mentioned in no more than a single paper.

Conclusions

Several research methods have been applied to ascribe migratory status and to study the physiology, neurobiology, and ecology of migration; however, virtually all this research is focused on a handful of species. There remain hundreds of species for which we do not understand the full seasonal pattern of movement, flight destinations, wintering, or breeding grounds. A full understanding of movement ecology and migratory connectivity is needed to effectively conserve migratory butterflies.

Geographic bias

insect

Lepidoptera

literature trend

methodological advancement

migration ecology

monarch

painted lady

red admiral

taxonomic bias

Migration is a widespread phenomenon among animals, often timed to exploit seasonal resource availability, with periodic movement from a habitat that has become unsuitable [1, 2]. Migration can reduce the burdens of parasitic infections and disease in a population by allowing individuals to escape from contaminated habitats and leave infected individuals behind: migratory butterflies with sub-lethal infections are less likely to migrate and/or are less likely to complete the journey [3]. Many migratory species are declining, mostly due to habitat destruction, overexploitation of resources, and climate change [4], although warming is likely to have positive effects in some locations, given the diveresity and abundance of some migratory Lepidoptera is higher in higher temperature locations [5–6].

Conserving migratory species is particularly challenging because threats occurring at any location along the migratory route and at any stage of the life cycle of a migrant can impact the entire population. This means that a whole series of intact habitats, perhaps in different jurisdictions, needs to be protected [4]. Therefore, understanding the patterns of spatial connectivity is central to conserving migratory species [4, 7–8]. While significant progress has been made in characterising and understanding migration in birds [9–10], much less is known about the ecology and conservation of migratory butterflies, excepting a few well-known migrants [e.g, monarch, painted lady; 11]. Migratory butterflies occur disproportionately in tropical rainforests [12], where deforestation is proceeding rapidly [13], and intensive research is needed to determine if a migratory butterfly is facing acute threats at a particular stage of its life cycle. Here, we briefly review the history of the study of migration in butterflies, explore some of the geographic and taxonomic foci of that work, and outline some future research directions.

Insects provide key ecosystem functions and services, as pollinators, herbivores, predators, and decomposers [14–18]. They also occur in human-modified ecosystems, often as vectors of human, livestock, or plant diseases, or as herbivores that directly damage crops [19–21]. Every year, many trillions of insects migrate from one part of the world to another, often crossing international borders [22]. For example, nearly 3.5 trillion insects traverse the southern United Kingdom every year, transferring more than 3,000 tons of biomass [23].

Although our current understanding of insect migrations is limited for most taxa, especially for pollinating insects, butterflies are, to some extent, an exception [11–12, 18, 24–26]. This might be because they are diurnal, brightly coloured, and fly relatively close to the ground, making their migration easier to detect and observe [1]. Over 3% of butterfly species [N = 568] migrate [11], but this is probably an underestimate, as only papers in English were reviewed for that study and the rate of reporting new diagnoses of migration in butterfly species does not appear to have declined between 1831 and 2020. Although studies on butterfly migration have been increasing, the literature remains scattered.

Our aims in this paper are to [i] review the history of studies on migration in butterflies, [ii] explore the geographic, taxonomic, and temporal patterns in the available studies, and [iii] outline some future research directions. Information on butterfly migration is often published in non-peer-reviewed journals [i.e, grey literature] [11], and up to one third of scientific documents related to biodiversity conservation are published in languages other than English [27]. Ignoring the non-English-language and grey literature can severely bias our understanding [28–34]. Here we compile a global knowledge base on butterfly migration from multiple sources, including peer-reviewed papers and grey literature [including web articles] that are available in English or five other languages. To identify knowledge gaps and provide a pathway to advance our understanding of butterfly migration, we analyse trends in existing studies [geographic, taxonomic, and temporal trends], describe the chronological development of how butterfly migration has been studied, and point out where further research might be fruitful.

Defining butterfly migration

Butterflies are small-bodied, usually living as adults for only a few weeks to a year [35], with the distances they travel during migrations varying greatly among species [1]. While many vertebrates migrate thousands of kilometres and individuals generally make the return journey, sometimes repeatedly throughout their lives, the situation is more complex for invertebrates [11, 36–41]. Butterfly migration usually entails multigenerational movement, with flights by each generation continuing for periods of several days to weeks [1, 37, 42–43]. For example, North American monarch butterflies travel 5,000–7,000 kilometres per year, but it takes 3–5 generations to complete the full annual cycle, with the spring migrants undertaking the bulk of journey – from the Trans Volcanic Plateau of Mountains in Mexico to different parts of the USA and Canada [24, 44–45].

It is challenging to define migration in butterflies, and several definitions have been offered [11]. Migration encompasses phenomena at different levels of biological organisation [physiological, individual/behavioural, population/spatial/ecological] but is often characterized as a behaviour that has ecological consequences [39, 46]. Perhaps one of the most useful, and the one we have employed here, remains that of Kennedy [47]; ‘Migratory behaviour is persistent and straightened-out movement effected by the animal’s own locomotory exertions or by its active embarkation on a vehicle. It depends on some temporary inhibition of station-keeping responses but promotes their eventual disinhibition and recurrence’.

Literature search

We searched [i] Google Scholar [https://scholar.google.com] with the keywords: ‘Butterfly migration’ and ‘Migratory butterflies’ and checked the first 100 pages, [ii] PubMed [https://pubmed.ncbi.nlm.nih.gov] with the same key words, [iii] Web of Science [Web of Science Core Collection; https://apps.webofknowledge.com] using the search string TS=[Butterf* AND migr*] with 1900–2020 as the year range, and [iv] Google [https://www.google.com] using the same keywords that we used for Google Scholar. When scanning relevant studies, we noticed that many authors published their work in local journals, especially the following four: Atalanta [Germany], Phegea [Belgium], Bulletin of the Allyn Museum [USA], and the Journal of the Bombay Natural History Society [India]. Therefore, we further checked all the issues of these four journals to make the review more comprehensive. Similarly, obtained some studies from the South-East Asia and the Neotropical regions, including publications in non-English languages [11]. We therefore conducted searches in five additional languages. Using the equivalent of ‘Butterfly migration’ and ‘Migratory butterflies’ we searched in Google Scholar for papers in Simplified [‘蝴蝶迁徙’, ‘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’, ‘遷徙性蝴蝶’ and ‘遷徙性蝶類] Chinese, Japanese [‘チョウ’ ‘蝶’, ‘渡り’, ‘移動’], Korean [‘이주’ and ‘이주성 나비’] and Spanish [‘Mariposas migratorias’ and ‘Migración de mariposas’]. Because some of the relevant Japanese literature may not be found using the keywords, ‘蝶, 渡り’ and ‘移動’, we made an additional search using the keywords, ‘昆虫’ and ‘海上’.

For each study, we recorded the title and year published, the subject species, geographic location, and the techniques used to establish [or discuss] migratory behaviour, as well as any information provided on parameters such as migratory behaviour, density and distance travelled. To assess geographic and taxonomic patterns, we used the locality and species information from each paper to group them into six continents [North America, South America, Europe, Africa, Asia, and Oceania].

To investigate whether interest in butterfly migration is increasing, we compared the number of papers specifically about butterfly migration to those on any aspect of butterfly biology between 1990 and 2019. Using Web of Science Core Collection [Advanced Search], we searched for papers using two keywords: ‘TS=[Butterf* AND migr*]’ for migratory butterflies, and ‘TS=[Butterf*]’ for butterflies. We only considered English-language papers, recognising that our results for this search might largely reflect patterns in North America or Europe where most English-language papers were located.

We identified 926 studies, published between 1833 and 2020, that mentioned butterfly migration in the abstract, of which 581 are in English, 246 in Spanish, 59 in Japanese, 29 in Simplified Chinese, and 11 in Traditional Chinese. The complete bibliography is provided in the Additional File section [Table S1].

While lepidopterists have been recording insect movements for centuries, interest in butterfly migration only began in earnest at the beginning of the 20th century [Fig. 1b]. Movement of millions of migratory butterflies at low altitude intrigued both professional lepidopterists and amateurs around the world, but it took a few more decades for researchers to start utilising formal scientific techniques to advance their research [Fig. 1]. For example, identification of insects flying at high altitudes based on radar echoes started in 1949 [48], and the detection of a massive locust swarm followed in 1954 [49]; however, it took more than a decade to deploy radar specifically to observe locusts. A recent review identified 13 lines of evidence [11; Y-Axis, Fig. 1a] that were used to ascribe migratory status of butterfly migrants. However, only a single line of evidence [mass movement has been used for 92% of all studies of migration in butterflies [Figure 1a].

There is marked variation in the number of studies among continents; most English-language studies on butterfly migration were from temperate or cooler regions, or from the Northern Hemisphere [especially the USA], with far fewer from the sub/tropics, or the Southern Hemisphere [Fig. 2]. Most studies from North America were from the USA and most studies from Europe were from the UK. However, by searching in four Asian languages and Spanish, we found another 345 relevant studies, mostly on species in North America [162 Spanish-language studies], but also in South America [44 in Spanish] and Europe [37 in Spanish], and Asia [99 studies in total: 59 in Japanese, 29 in Simplified Chinese, 11 in Traditional Chinese, and 1 in Spanish, Fig. 2]. This highlights the importance of including non-English studies in literature reviews across the globe. Overall, most studies on butterfly migration were from North America [548 studies, > 50%], and only 4% [45 studies] were from Africa.

The available studies are clearly biased towards a few species; the monarch [62% of the 926 studies], painted lady [9.6%], and red admiral [5.8%] [Fig. 3]. There were only six species [monarch, painted lady, red admiral, common emigrant [Catopsilia pomona], lesser wanderer [Danaus chrysippus], and common crow [Euploea core] with more than 30 studies, and 41 species with > 10 papers [all on either pierids or nymphalids except for pea blue [Lampides boeticus, Lycaenidae], and long-tailed skipper [Urbanus proteus, Hesperiidae]]. Nearly 50% [271 species] of our recorded migratory butterfly species have not been the subject of a thorough single study but are just mentioned once in a paper. On the other hand, the monarch accounted for 62% of the studies [Fig. 3]. Being an invasive species that has spread well beyond its native range, the monarch butterfly figures prominently wherever it is present.

Studies on the monarch dominate not only in North America [nearly 85% of all studies; Fig. 2], but even in areas where monarchs do not migrate [e.g, Spain]. Elsewhere in the world, studies were biased towards other species. For example, painted lady and red admiral for Europe, lesser wanderer and monarch for Africa and Australia, and chestnut tiger [Parantica sita], and common crow for Asia [see Additional File [Table S1] for more details].

Overall, there was no significant yearly trend in the proportion of English-language peer-reviewed papers on butterfly biology that were specifically on butterfly migration [χ² = 0.14; df = 1; P = 0.7061; Generalized Linear Model with a Poisson distribution; Fig. 4a]. The proportion of papers on migratory butterflies ranged from 1–3%. On the other hand, the number of papers on monarchs has increased significantly over the past 30 years [χ² = 37.223; df = 1; P < 0.0001; Generalized Linear Model with a Poisson distribution; Fig. 4b], while the number of papers on non-monarch butterfly species has not noticeably risen. In the last few decades, the North American migratory monarch population size has declined by > 80%, starting in the 1990s [Semmens et al, 2016; Stenoien et al, 2018]; this decline of an iconic species has probably prompted more research.

Our results show that studies on butterfly migration are concentrated in relatively few regions of the world, and that only a few species have been studied in detail [monarch, painted lady and red admiral]. There was no increase in the number of publications on butterfly migration over the years; although research on the Monarch has accelerated. We showed the potential importance of non-English-language studies to better understand butterfly migration globally. Although we considered only five non-English languages in this study, future studies could consider a broader set of languages widely used for scientific studies [e.g, French, German, Italian, Polish, Portuguese, Russian, and other non-European languages]. Language restrictions might have impacted our findings. For example, if our search was expanded into German, French, and Portuguese, we might have located more studies from Europe, Africa, and South America [34]. However, given we checked two regional journals [Atalanta and Phegea; publishes studies in German and Dutch repetitively], we think that we have already captured many German and Dutch studies. Similarly, although we used rigorous literature search approaches to make the review as comprehensive as possible, may have missed relevant papers with our keyword driven search approach.

Charismatic species, especially if also threatened, often get disproportionate research, and the research using the latest techniques is often concentrated in advanced-economy countries. This sort of ‘research bias’ is quite common in biology [50], but can hamper our understanding of species ecology and conservation [51–54]. We have identified both taxonomic and geographic biases in published studies on butterfly migration in that most studies: i] cover North America and Europe, with very few from the tropics or subtropics, and ii] focus on a small number of species. To reduce bias, researchers could conduct more studies on migration in poorly studied species and regions to identify the true prevalence of migration in butterflies. For example, a recent study has shown that unlike migratory birds, seasonal movements between suitable and unsuitable habitats in migratory butterflies appears most prominent in the tropics [12]. In this review, we identify a lack of studies in the tropics, suggesting there is an under-representation of migratory species.

Although a recent review listed several hundred butterfly migrants [11], the rate of discovery of new migratory species indicates that there might yet be thousands more. Nevertheless, it is worth noting that there can be both migratory and non-migratory populations and individuals within a species [55–57]. To understand seasonal movements, it is essential to monitor across a species’ full geographic distribution, a task for which active citizen science participation is likely to be highly beneficial [12, 58–63]. For example, both amateur and professional ornithologists widely use eBird, which has transformed the availability of bird data globally [64–66]. So how can we engage citizen science in the tropics? Nowadays, iNaturalist, a citizen science project, is increasingly popular both among professional and amateur naturalists [67]. Citizen science tools, such as this, can widen the coverage of space and species in data collection; and collating and analysing the resulting data will help to identify which species are, in fact, migratory. For this reason, maximising funding and shifting research effort towards tropical regions could enable broader discovery of migration in butterflies. In many countries, funding is more readily available for insects of economic significance, such as pests and pollinators. Future studies could assess the disparity in funding amount and prioritise funding for species that are at elevated extinction risk.

Future research could focus on identifying, tracking, and understanding the navigation of butterfly migrants. Time honoured techniques such as mark-release-recapture can be used to calculate travel distances, and whether the distance and overall direction of movement is associated with changes in seasonal resources; isotopic analysis can be used to identify the origin of individuals [57, 68]; flight chamber experiments can be used to record flight duration of butterflies and differentiate migrants and non-migrants and even differences in orientation [69–71]; radars can be used in hotspot regions to determine the seasonal flow of movements [22–23, 39, 72]; female butterflies can be collected and dissected to check the status of their ovarian development [73]; genomic resources such as EST-based microarray analyses, transcriptome libraries and single nucleotide polymorphism [SNP] marker sets can be used to determine migration routes [2, 74–75]; and ecological niche and movement modelling can uncover spatial patterns of seasonal occurrence and habitat use in migratory butterflies [12, 62, 76–77].

During migratory flights, monarch butterflies adjust their flight altitude and vectors by flapping and gliding [78–79], but there is no information on whether this occurs in other migratory butterflies. Recent studies have shown that some long-distance migratory butterflies use air currents [23, 80–83] but little is known about the cost of migration, metabolism of flight fuels, or how migratory butterflies counter overheating. Moreover, there are some phenotypic differences, especially in traits linked to migration, between eastern and western monarchs, despite genetic studies indicating these populations are closely related [84]. Future studies could focus on assessing the reasons for these differences between eastern and western monarchs. Similarly, migratory butterflies can be tracked using natural markers such as cardenolides [85–86]. It would be interesting to extend this method to other Danainae butterflies that feed on Apocynaceae.

While undertaking migratory flights, migrants often cross multiple regions. This continuous movement makes them vulnerable to anthropogenic threats and complicates their conservation [12, 45, 61–62, 87–89]. Due to extensive anthropogenic pressure and human-induced climate change, insects, including butterflies, are declining worldwide [90–95]. It is notable that populations of more than half of migratory birds have declined in the last 30 years, suggesting that, in general, migratory species are at greater risk than sedentary species [96]. The few available time series analyses have shown some migratory butterfly populations to be stable, while others are declining. For example, while the North American migratory monarch population has dramatically declined in the last few decades [97–99], populations of painted lady, red admiral and clouded yellow [Colias croceus] have remained relatively stable [83, 100]. However, it should be noted that time-series data are rare for most migratory butterflies, and unavailable from most parts of the world.

To implement effective migratory species conservation, holistic analyses across the entire distribution are needed, since migrants require a chain of intact habitat [8, 88]. Ultimately, knowledge of seasonal movements, locations of stopover sites, protected area coverage, and improved knowledge of the basic biology of migration in butterflies is needed to drive successful conservation planning. Migratory butterflies perform a broad range of functions in ecosystems including transferring biomass, transporting nutrients, and influencing resource fluxes and food web structure [1, 18, 101]. If we are to conserve them effectively, migratory butterflies will need far more attention than they currently receive.

Ethics approval and consent to participate

Not applicable

Consent for publication

Not applicable

Availability of data and materials

The data that supports the findings of this study are available in the Additional File section of this article.

Competing interests

Not applicable

Funding

Not applicable

Authors' contributions

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, D.L.L, L.Y, and S.W.C. collected and summarised the data, S.C, did the analysis, everyone contributed to the analysis, S.C. wrote the paper, everyone contributed to the writing of the paper.

Acknowledgements

The corresponding author is thankful to the Australian Government, the University of Queensland, and the Centre for Biodiversity and Conservation Science for providing an International Research Training Program Fellowship.

Dingle H. Migration: the biology of life on the move. Oxford University Press, USA; 2014.
Liedvogel M, Åkesson S, Bensch S. The genetics of migration on the move. Trends Ecol Evol. 2011;26:561–569.
Bartel RA, Oberhauser, KS, De Roode JC, Altizer SM. Monarch butterfly migration and parasite transmission in eastern North America. Ecology. 2011;92:342–351.
Wilcove DS, Wikelski M. Going, going, gone: is animal migration disappearing. PLoS Biol. 2008;6:e188.
Sparks TH, Roy DB, Dennis RLH. The influence of temperature on migration of Lepidoptera into Britain. Glob Change Biol. 2005;11:507–514.
Sparks TH, Dennis RL, Croxton PJ, Cade M. Increased migration of Lepidoptera linked to climate change. Eur J Entomol. 2007;104:139–143.
Webster MS, Marra PP, Haig SM, Bensch S, Holmes RT. Links between worlds: unraveling migratory connectivity. Trends Ecol Evol. 2002;17:76–83.
Gao B, Hedlund J, Reynolds DR, Zhai B, Hu G, Chapman JW. The ‘migratory connectivity’ concept, and its applicability to insect migrants. Mov Ecol. 2020;8:1–13.
Faaborg J, Holmes RT, Anders AD, Bildstein KL, Dugger KM, Gauthreaux JSA, et al. Conserving migratory land birds in the New World: Do we know enough? Ecol Appl. 2010;20:398–418.
Robinson WD, Bowlin MS, Bisson I, Shamoun-Baranes J, Thorup K, Diehl RH, et al. Integrating concepts and technologies to advance the study of bird migration. Frontiers Ecol Environ. 2010;8:354–361.
Chowdhury S, Fuller RA, Dingle H, Chapman JW, Zalucki MP. Migration in butterflies: A global overview. Biol Rev. 2021;96:1462–1483.
Chowdhury S, Zalucki MP, Amano T, Woodworth BK, Venegas-Li R, Fuller, RA. Seasonal spatial dynamics of butterfly migration. Ecol Lett. 2021;24:1814–1823.
Sodhi NS, Posa MRC, Lee TM, Bickford D, Koh LP, Brook BW. The state and conservation of Southeast Asian biodiversity. Biodivers Conserv. 2010;19:317–328.
Gaston KJ. The magnitude of global insect species richness. Conserv Biol. 1991;5:283–296.
Didham RK, Ghazoul J, Stork NE, Davis AJ. Insects in fragmented forests: a functional approach. Trends Ecol Evol. 1996;11:255–260.
Yang LH, Gratton C. Insects as drivers of ecosystem processes. Current Opinion in Insect Science. 2014;2:26–32.
Stork NE. How many species of insects and other terrestrial arthropods are there on Earth? Annu Rev Entomol. 2018;63:31–45.
Satterfield DA, Sillett TS, Chapman JW, Altizer S, Marra PP. Seasonal insect migrations: massive, influential and overlooked. Frontiers Ecol Enviorn. 2020;18:335–344.
McGeoch MA. The selection, testing and application of terrestrial insects as bioindicators. Biol Rev. 1998;73:181–201.
Walther GR, Post E, Convey P, Menzel A, Parmesan C, Beebee TJ, et al. Ecological responses to recent climate change. Nature. 2002;416:389–395.
Reynolds DR, Chapman JW, Harrington R. The migration of insect vectors of plant and animal viruses. Adv Virus Res. 2006;67:453–517.
Chapman JW, Drake VA, Reynolds DR. Recent insights from radar studies of insect flight. Annu Rev Entomol. 2011;56:337–356.
Hu G, Lim KS, Horvitz N, Clark SJ, Reynolds DR, Sapir N, Chapman JW. Mass seasonal bioflows of high-flying insect migrants. Science. 2016;354:1584–1587.
Brower LP, Fink LS, Walford P. Fueling the fall migration of the monarch butterfly. Integr Comp Biol. 2006;46:1123–1142.
Meitner C, Brower LP, Davis AK. Migration patterns and environmental effects on stopover of monarch butterflies (Lepidoptera, Nymphalidae) at Peninsula Point, Michigan. Environ Entomol. 2004;33:249–256.
Pierce AA, Zalucki MP, Bangura M, Udawatta M, Kronforst MR, Altizer S, et al. Serial founder effects and genetic differentiation during worldwide range expansion of monarch butterflies. Proc Royal Soc B. 2014; 281:20142230.
Amano T, González-Varo JP, Sutherland WJ. Languages are still a major barrier to global science. PLoS Biol. 2016a;14:e2000933.
Egger M, Zellweger-Zähner T, Schneider M, Junker C, Lengeler C, Antes G. Language bias in randomised controlled trials published in English and German. The Lancet. 1997;350:326–329.
Møller AP, Jennions MD. Testing and adjusting for publication bias. Trends Ecol Evol. 2001;16:580–586.
Jennions MD, Møller AP. Relationships fade with time: a meta-analysis of temporal trends in publication in ecology and evolution. Proc R Soc B: Biol Sci. 2002a;269:43–48.
Jennions MD, Møller AP. Publication bias in ecology and evolution: an empirical assessment using the ‘trim and fill’ method. Biol Rev. 2002b;77:211–222.
Amano T, Espinola VB, Christie AP, Willott K, Akasaka M, Baldi A, Berthinussen A, et al. Tapping into non-English-language science for the conservation of global biodiversity. PLoS Biol. 2021;19:e3001296.
Konno K, Akasaka M, Koshida C, Katayama N, Osada N, Spake R, et al. Ignoring non-English‐language studies may bias ecological meta‐analyses. Ecol Evol. 2020;11:698–713.
Chowdhury S, Gonzalez K, Aytekin MÇK, Baek S.-Y, Bełcik M, Bertolino S, et al. Growth of non-English-language literature on biodiversity conservation. Conserv Biol. 2022 (in press).
Oberhauser KS, Solensky MJ. Monarch butterfly biology & conservation. Cornell university press, 2004, 256 pp.
Malcolm SB, Slager BH. Migration and host plant use by the southern monarch, Danaus erippus. In Monarchs in a changing world: Biology and conservation of an iconic butterfly (eds. Oberhauser KA, Nail KR, Altizer S.). Cornell University Press, Ithaca, N.Y, USA, 2015, 225–235 pp.
Malcolm SB, Zalucki MP. Biology and conservation of the Monarch butterfly. Los Angeles: Natural History Museum of Los Angeles County. 1993.
Stefanescu C, Páramo F, Åkesson S, Alarcón M, Ávila A, Brereton T, et al. Multi-generational long‐distance migration of insects: studying the painted lady butterfly in the Western Palaearctic. Ecography. 2013;36:474–486.
Chapman JW, Reynolds DR, Wilson K. (2015). Long-range seasonal migration in insects: mechanisms, evolutionary drivers and ecological consequences. Ecol Lett. 18:287–302.
Ruiz Vargas N, Rowe L, Stevens J, Armagost JE, Johnson AC, Malcolm SB. Sequential partial migration across monarch generations in Michigan. Animal Migration. 2018;5:104–114.
Menz MH, Reynolds DR, Gao B, Hu G, Chapman JW, & Wotton KR. Mechanisms and consequences of partial migration in insects. Front Ecol Evol. 2019;7:403.
Holland RA, Wikelski M, Wilcove DS. How and why do insects migrate? Science. 2006;313:794–796.
Talavera G, Bataille C, Benyamini D, Gascoigne-Pees M, Vila R. Round-trip across the Sahara: Afrotropical Painted Lady butterflies recolonize the Mediterranean in early spring. Biol Lett. 2018;14:20180274.
Dingle H, Zalucki M, Rochester W, Armijo-Prewitt T. Distribution of the monarch butterfly, Danaus plexippus (L.)(Lepidoptera: Nymphalidae), in western North America. Biol J Linn Soc. 2005;85:491–500.
Malcolm SB. Anthropogenic impacts on mortality and population viability of the monarch butterfly. Annual Review of Entomology. 2018;63:277–302.
Dingle H, Drake VA. What is migration? Bioscience. 2007;57:113–121.
Kennedy JS. Migration: behavioral and ecological. In Migration: Mechanisms and Adaptive Significance (ed. Rankin MA.). Austin, Marine Science Institute, University of Texas. 1985, p. 5–26.
Crawford A. Radar reflections in the lower atmosphere. Proc Inst Radio Eng. 1949;37:404–405.
Rainey RC. Observation of desert locust swarms by radar. Nature. 1955;175:77–78.
Di Marco M, Chapman S, Althor G, Kearney S, Besancon C, Butt N, et al. Changing trends and persisting biases in three decades of conservation science. Glob Ecol Conserv. 2017;10:32–42.
Pyšek P, Richardson DM, Pergl J, Jarošík V, Sixtova Z, Weber E. Geographical and taxonomic biases in invasion ecology. Trends Ecol Evol. 2008;23:237–244.
Jennions MD, Lortie CJ, Rosenberg MS, Rothstein HR. Publication and related biases. Handbook of Meta-analysis in Ecology and Evolution. 2013, p. 207–236.
Holman L, Head ML, Lanfear R, Jennions MD. Evidence of experimental bias in the life sciences: why we need blind data recording. PLoS Biol. 2015;13:e1002190.
Nuñez MA, Chiuffo MC, Pauchard A, Zenni RD. Making ecology really global. Trends Ecol Evol. 2021;36:766–769.
Zhan S, Zhang W, Niitepõld K, Hsu J, Haeger JF, Zalucki MP, et al. The genetics of monarch butterfly migration and warning colouration. Nature. 2014;514:317–321.
Slager BH, Malcolm SB. Evidence for partial migration in the southern monarch butterfly, Danaus erippus, in Bolivia and Argentina. Biotropica. 2015;47:355–362.
Vander Zanden HB, Chaffee CL, González-Rodríguez A, Flockhart DT, Norris DR, Wayne ML. Alternate migration strategies of eastern monarch butterflies revealed by stable isotopes. Animal Migration. 2018;5:74–83.
Boakes EH, McGowan PJ, Fuller RA, Chang-Qing D, Clark NE, O'Connor K, Mace GM. (2010). Distorted views of biodiversity: spatial and temporal bias in species occurrence data. PLoS Biol. 2010;8:e1000385.
Mason SC, Hill JK, Thomas CD, Powney GD, Fox R, Brereton, T, et al. Population variability in species can be deduced from opportunistic citizen science records: a case study using British butterflies. Insect Conserv Divers. 2018;11:131–142.
Soroye P, Ahmed N, Kerr JT. Opportunistic citizen science data transform understanding of species distributions, phenology, and diversity gradients for global change research. Glob Change Biol. 2018;24:5281–5291.
Juhász E, Gór Á, Bali D, Kerékgyártó F, Katona G, Végvári Z. Long-term temporal patterns in flight activities of a migrant diurnal butterfly. Insect Sci. 2020;28:839–849.
Chowdhury S, Braby MF, Fuller RA, Zalucki MP. Coasting along to a wider range: niche conservatism in the recent range expansion of the Tawny Coster, Acraea terpsicore (Lepidoptera: Nymphalidae). Divers Distrib. 2021a;27:402–415.
Chowdhury S, Alam S, Chowdhury SU, Rokonuzzaman M, Shahriar SA, Shome AR, et al. Butterflies are weakly protected in a mega-populated country, Bangladesh. Glob Ecol Conserv. 2021b;26:e01484.
Amano T, Lamming JD, Sutherland WJ. Spatial gaps in global biodiversity information and the role of citizen science. BioScience. 2016b;66:393–400.
Bonney R, Cooper CB, Dickinson J, Kelling S, Phillips T, Rosenberg KV, et al. Citizen science: a developing tool for expanding science knowledge and scientific literacy. BioScience. 2009;59:977–984.
Sullivan BL, Wood CL, Iliff MJ, Bonney RE, Fink D, Kelling S. eBird: A citizen-based bird observation network in the biological sciences. Biol Conserv. 2009;142:2282–2292.
Callaghan CT, Poore AG, Mesaglio T, Moles AT, Nakagawa S, Roberts C, et al. Three Frontiers for the Future of Biodiversity Research Using Citizen Science Data. BioScience. 2020;71:55–63
Wassenaar LI, Hobson KA. Natal origins of migratory monarch butterflies at wintering colonies in Mexico: new isotopic evidence. Proc Nat Acad Sci. 1998;95:15436–15439.
Mouritsen H, Frost BJ. Virtual migration in tethered flying monarch butterflies reveals their orientation mechanisms. Proc Nat Acad Sci. 2002;99:10162–10166.
Reppert SM, Zhu H, White RH. Polarized light helps monarch butterflies navigate. Curr Biol. 2004;14:155–158.
Minter M, Pearson A, Lim KS, Wilson K, Chapman JW, Jones CM. The tethered flight technique as a tool for studying life-history strategies associated with migration in insects. Ecol Entomol. 2018;43:397–411.
Stefanescu C, Ubach A, Wiklund C. Timing of mating, reproductive status and resource availability in relation to migration in the painted lady butterfly. Anim Behav. 2021;172:145–153.
Johnson CG. Physiological factors in insect migration by flight. Nature. 1963; 198:423–427.
Brattström O, Åkesson S, Bensch S. AFLP reveals cryptic population structure in migratory European red admirals (Vanessa atalanta). Ecol Entomol. 2010a;35:248–252.
Brattström O, Bensch S, Wassenaar LI, Hobson KA, Åkesson S. Understanding the migration ecology of European red admirals Vanessa atalanta using stable hydrogen isotopes. Ecography. 2010b;33:720–729.
Zalucki MP, Parry HR, Zalucki JM. Movement and egg laying in monarchs: to move or not to move, that is the equation. Austral Ecol. 2016;41:154–167.
Grant TJ, Parry HR, Zalucki MP, Bradbury SP. Predicting monarch butterfly (Danaus plexippus) movement and egg-laying with a spatially-explicit agent-based model: the role of monarch perceptual range and spatial memory. Ecol Modell. 2018;374:37–50.
Gibo DL, Pallett MJ. Soaring flight of monarch butterflies, Danaus plexippus (Lepidoptera: Danaidae), during the late summer migration in southern Ontario. Can J Zool. 1979;57:1393–1401.
Gibo DL. Some observations on soaring flight in the mourning cloak butterfly (Nymphalis antiopa L.) in southern Ontario. J N Y Entomol Soc. 1981;89:98–101.
Stefanescu C, Alarcón M, Àvila A. Migration of the painted lady butterfly, Vanessa cardui, to north-eastern Spain is aided by African wind currents. J Anim Ecolo. 2007;76:888–898.
Srygley RB, Dudley R. Optimal strategies for insects migrating in the flight boundary layer: mechanisms and consequences. Integr Comp Biol. 2008;48:119–133.
Chapman JW, Nesbit RL, Burgin LE, Reynolds DR, Smith AD, Middleton DR, Hill JK. Flight orientation behaviors promote optimal migration trajectories in high-flying insects. Science. 2010;327:682–685.
Hu G, Stefanescu C, Oliver TH, Roy DB, Brereton T, Van Swaay C, et al. Environmental drivers of annual population fluctuations in a trans-Saharan insect migrant. Proc Natl Acad Sci. 2021;118:e2102762118.
Freedman MG, de Roode JC, Forister ML, Kronforst MR, Pierce AA, Schultz CB, et al. Are eastern and western monarch butterflies distinct populations? A review of evidence for ecological, phenotypic, and genetic differentiation and implications for conservation. Conserv Sci Pract. 2021;3:e432.
Malcolm SB, Cockrell BJ, Brower LP. Cardenolide fingerprint of monarch butterflies reared on common milkweed, Asclepias syriaca L. J Chem Ecol. 1989;15:819–853.
Brower LP. Understanding and misunderstanding the migration of the monarch butterfly (Nymphalidae) in North America: 1857–1995. J Lepid Soc. 1995;49:304–385.
Martin TG, Chadès I, Arcese P, Marra PP, Possingham HP, Norris DR. Optimal conservation of migratory species. PloS One. 2007;2:e751.
Runge CA, Martin TG, Possingham HP, Willis SG, Fuller RA. Conserving mobile species. Frontiers Ecol Environ. 2014;12:395–402.
Reynolds MD, Sullivan BL, Hallstein E, Matsumoto S, Kelling S, Merrifield M, et al. Dynamic conservation for migratory species. Sci Adv. 2017;3:e1700707.
WallisDeVries MF, Baxter W, Van Vliet AJ. Beyond climate envelopes: effects of weather on regional population trends in butterflies. Oecologia. 2011;167:559–571.
Fox R. The decline of moths in Great Britain: a review of possible causes. Insect Conserv Divers. 2013;6:5–19.
Habel JC, Ulrich W, Biburger N, Seibold S, Schmitt T. Agricultural intensification drives butterfly decline. Insect Conserv Divers. 2019;12:289–295.
Hallmann CA, Sorg M, Jongejans E, Siepel H, Hofland N, Schwan H, et al. More than 75 percent decline over 27 years in total flying insect biomass in protected areas. PloS One. 2017;12:e0185809.
Sánchez-Bayo F, Wyckhuys KA. Worldwide decline of the entomofauna: A review of its drivers. Biol Conserv. 2019;232:8–27.
Wagner DL. Insect declines in the Anthropocene. Annu Rev Entomol. 2020;65:457–480.
Kirby JS, Stattersfield AJ, Butchart SH, Evans MI, Grimmett RF, Jones VR, et al. Key conservation issues for migratory land-and waterbird species on the world's major flyways. Bird Conserv Int. 2008;18:S49-S73.
Stenoien C, Nail KR, Zalucki JM, Parry H, Oberhauser KS, Zalucki MP. Monarchs in decline: a collateral landscape-level effect of modern agriculture. Insect Sci. 2018;25:528–541.
Zylstra ER, Ries L, Neupane N, Saunders SP, Ramírez MI, Rendón-Salinas E, et al. Changes in climate drive recent monarch butterfly dynamics. Nat Ecol Evol. 2021;5:1441–1452.
Semmens BX, Semmens DJ, Thogmartin WE, Wiederholt R, López-Hoffman L, Diffendorfer JE, et al. Quasi-extinction risk and population targets for the Eastern, migratory population of monarch butterflies (Danaus plexippus). Sci Rep. 2016;6:23265.
Fox R, Brereton TM, Asher J, August TA, Botham MS, Bourn NAD, et al. (2015). The State of the UK’s Butterflies. Butterfly Conservation and the Centre for Ecology & Hydrology. Wareham, Dorset; 2015, 28 pp.
Bowlin MS, Bisson IA, Shamoun-Baranes J, Reichard JD, Sapir N, Marra PP, Kunz TH, Wilcove DS, Hedenström A, Guglielmo CG, Åkesson S. Grand challenges in migration biology. Integr Comp Biol. 2010;50:261–279.

No competing interests reported.

AdditionalFile.xlsx

Download PDF

Version 1

posted

You are reading this latest preprint version

Trends and Progress in Studying Butterfly Migration

Status:

Version 1

Abstract

Background

Method

Results

Conclusions

Figures

Introduction

Methods

Defining butterfly migration

Results

Discussion

Declarations

References

Additional Declarations

Supplementary Files

Status:

Version 1