Advertisement

Identification “by eye”: integrative character assessment informs regional field identification of greater fritillary butterflies (Nymphalidae: Speyeria)

  • Federico RivaEmail author
  • Erin O. Campbell
  • Fionnuala Carroll
  • John H. Acorn
ORIGINAL PAPER

Abstract

The pronounced morphological variability exhibited by Speyeria butterflies can hinder the identification of these taxa, and thus presents a challenge to their management and conservation. While several studies have documented declines in American populations of Speyeria due to habitat change, the response of Canadian populations of Speyeria to widespread anthropogenic pressures remains poorly understood due to their difficult identification. Here, we assessed the utility of morphological characters recommended in regional field guides for the identification of Speyeria butterflies in Canada, focusing on three morphologically variable subspecies that inhabit boreal forests subject to widespread oil sands extraction: S. aphrodite manitoba, S. atlantis hollandi, and S. hesperis beani. We scored 159 specimens for 11 morphological characters, and complimented this data by sequencing the barcode region of the COI gene for 15 of these specimens. Our results indicate a high level of intraspecific variability in several characters, and the COI gene revealed that initial morphological identifications were incorrect. A further assessment of character reliability identified sets of morphological characters that, in combination with specimen sex and species natural history, improved subspecies identification. Notably, we found that a relatively novel field marker—in vivo eye color—consistently distinguished S. aphrodite manitoba from S. hesperis beani and S. atlantis hollandi. Our results emphasize the importance of using an integrative approach for the accurate identification of morphologically variable species, particularly in situations where molecular methods are not readily available, such as citizen science programs.

Keywords

COI gene Speyeria Morphology Species identification Citizen science 

Notes

Acknowledgments

We thank eButterfly and all of their affiliated citizen scientists for collecting, reporting, and vetting butterfly observation data used in this publication. We additionally thank F. and T. Sperling, B. Acorn, and S. Ferguson for specimen collection, and the Molecular Biology Services Unit at the University of Alberta for sequencing support. Funding for the research was provided by two Alberta Conservation Association Grant in Biodiversity to EC and FR, an NSERC Discovery Grant to Felix Sperling, and a DeWind Award from the Xerces Society to FR.

Author contributions

FR and EOC contributed equally as first authors to the manuscript; All authors designed the study and contributed to draft revisions; FR and FC collected Speyeria butterflies in the Alberta boreal forest; FC scored all specimens and prepared the data for analysis; FR and EOC conducted the analyses and prepared the R script.

Compliance with ethical standards

Conflicts of interest

The authors have no conflicts of interest to declare.

Ethical statement

This research did not involve human participants, and thus an informed consent form was not necessary. The study complies with the University of Alberta Animal Ethics Policy.

Supplementary material

10841_2019_189_MOESM1_ESM.R
Electronic supplementary material 1 (R 7 kb)
10841_2019_189_MOESM2_ESM.csv (15 kb)
Electronic supplementary material 2 (CSV 15 kb)
10841_2019_189_MOESM3_ESM.xlsx (13 kb)
Electronic supplementary material 3 (XLSX 13 kb)
10841_2019_189_MOESM4_ESM.pdf (169 kb)
Electronic supplementary material 4 (PDF 169 kb)
10841_2019_189_MOESM5_ESM.xlsx (33 kb)
Electronic supplementary material 5 (XLSX 33 kb)

References

  1. Acorn JH (2017) Entomological citizen science in Canada. Can Entomol.  https://doi.org/10.4039/tce.2017.48 CrossRefGoogle Scholar
  2. Acorn JH, Sheldon I (2006) Butterflies of British Columbia. Lone Pine, Edmonton, ALGoogle Scholar
  3. Bird CD, Hilchie GJ, Kondla NG et al (1995) Alberta butterflies. Alberta Public Affairs Bureau/Queens Printer, The Provincial Museum of Alberta, Edmonton, ALGoogle Scholar
  4. Breed GA, Stichter S, Crone EE (2013) Climate-driven changes in northeastern US butterfly communities. Nat Clim Chang.  https://doi.org/10.1038/nclimate1663 CrossRefGoogle Scholar
  5. Brock JP, Kaufman K, Bowers R et al (2003) Kaufman field guide to butterflies of North America. Houghton Mifflin, Oak Harbor, OHGoogle Scholar
  6. Campbell EO, Davis CS, Dupuis JR, Muirhead K, Sperling FAH (2017) Cross-platform compatibility of de novo-aligned SNPs in a non-model butterfly genus. Mol Ecol Res.  https://doi.org/10.1111/1755-0998.12695 CrossRefGoogle Scholar
  7. Caven AJ, King KC, Wiese JD, Brinley Buckley EM (2017) A descriptive analysis of Regal Fritillary (Speyeria idalia) habitat utilizing biological monitoring data along the big bend of the Platte River. J Insect Conserv, NE.  https://doi.org/10.1007/s10841-017-9968-0 CrossRefGoogle Scholar
  8. Chermock FH, Chermock RL (1940) Some new diurnal lepidoptera from the riding mountains and the sand ridge. Can Entomol, Manitoba.  https://doi.org/10.4039/Ent7281-4 CrossRefGoogle Scholar
  9. dos Passos CF, Grey LP (1947) Systemic catalogue of Speyeria (Lepidoptera, Nymphalidae) with designations of type and fixations of type localities. Am Museum Novit 404–421Google Scholar
  10. Dunford JC (2009) Taxonomic overview of the greater fritillary genus Speyeria Scudder and the atlantis-hesperis species complexes, with species accounts, type images, and relevant literature (Lepidoptera: Nymphalidae). Insecta MundiGoogle Scholar
  11. Giesy JP, Anderson JC, Wiseman SB (2010) Alberta oil sands development. Proc Natl Acad Sci USA 107:951–952.  https://doi.org/10.1073/pnas.0912880107 CrossRefPubMedGoogle Scholar
  12. Glassberg J (2001) Butterflies through binoculars: the west. Oxford University Press, OxfordGoogle Scholar
  13. Glassberg J (2017) A swift guide to butterflies of North America. Princeton University Press, PrincetonCrossRefGoogle Scholar
  14. Guppy CS, Shepard J, Royal British Columbia Museum (2001) Butterflies of British Columbia : including western Alberta, southern Yukon, the Alaska Panhandle, Washington, northern Oregon, northern Idaho, northwestern Montana. UBC Press, VancouverGoogle Scholar
  15. Hammond PC, Mccorkle DV, Bergman W (2013) Hybridization studies of genomic compatibility and phenotypic expression in the greater fritillary butterflies (Nymphalidae: Argynnini). J Lepid Soc 67:263–273.  https://doi.org/10.18473/lepi.v67i4.a3 CrossRefGoogle Scholar
  16. Hebert PDN, Cywinska A, Ball SL, DeWaard JR (2003) Biological identifications through DNA barcodes. Proc R Soc B Biol Sci.  https://doi.org/10.1098/rspb.2002.2218 CrossRefGoogle Scholar
  17. Hill RI, Ganeshan M, Wourms L et al (2018) Effectiveness of DNA barcoding in Speyeria butterflies at small geographic scales. Diversity.  https://doi.org/10.3390/d10040130 CrossRefGoogle Scholar
  18. Katoh K, Rozewicki J, Yamada KD (2017) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform.  https://doi.org/10.1093/bib/bbx108 CrossRefPubMedCentralGoogle Scholar
  19. Layberry RA, Hall PW, Lafontaine JD, Canada Institute for Scientific and Technical Information (1998) The butterflies of Canada. University of Toronto Press, TorontoCrossRefGoogle Scholar
  20. Maddison WP, Maddison DR (2018) Mesquite: a modular system for evolutionary analysisGoogle Scholar
  21. McHugh A, Bierzychudek P, Greever C et al (2013) A molecular phylogenetic analysis of Speyeria and its implications for the management of the threatened Speyeria zerene hippolyta. J Insect Conserv.  https://doi.org/10.1007/s10841-013-9605-5 CrossRefGoogle Scholar
  22. Moeck AH (1975) Geographic variability in Speyeria: comments, records, and description of a new subspecies. Entomological Reprint Specialists, Los AngelesGoogle Scholar
  23. Nielsen SE, Boyce MS, Stenhouse GB (2004) Grizzly bears and forestry: I. Selection of clearcuts by grizzly bears in west-central Alberta, Canada. For Ecol Manage.  https://doi.org/10.1016/j.foreco.2004.04.014 CrossRefGoogle Scholar
  24. Pelham JP (2012) A catalogue of the butterflies of the United States and Canada, with a complete bibliography of the descriptive and systematic literature. J Res Lepid 40:1–658Google Scholar
  25. R Core Team (2017) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
  26. Ríos-Saldaña CA, Delibes-Mateos M, Ferreira CC (2018) Are fieldwork studies being relegated to second place in conservation science? Glob Ecol Conserv.  https://doi.org/10.1016/j.gecco.2018.e00389 CrossRefGoogle Scholar
  27. Riva F, Acorn JH, Nielsen SE (2018a) Localized disturbances from oil sands developments increase butterfly diversity and abundance in Alberta’s boreal forests. Biol Conserv 217:173–180.  https://doi.org/10.1016/j.biocon.2017.10.022 CrossRefGoogle Scholar
  28. Riva F, Acorn JH, Nielsen SE (2018b) Narrow anthropogenic corridors direct the movement of a generalist boreal butterfly. Biol Lett.  https://doi.org/10.1098/rsbl.2017.0770 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Riva F, Pinzon J, Acorn JH, Nielsen SE (2019) Composite effects of cutlines and wildfire result in fire refuges for plants and butterflies in boreal treed peatlands. Ecosystems.  https://doi.org/10.1007/s10021-019-00417-2 CrossRefGoogle Scholar
  30. Shuey J, Jacquart E, Orr S et al (2016) Landscape-scale response to local habitat restoration in the regal fritillary butterfly (Speyeria idalia) (Lepidoptera: Nymphalidae). J Insect Conserv.  https://doi.org/10.1007/s10841-016-9908-4 CrossRefGoogle Scholar
  31. Soroye P, Ahmed N, Kerr JT (2018) Opportunistic citizen science data transform understanding of species distributions, phenology, and diversity gradients for global change research. Glob Chang Biol.  https://doi.org/10.1111/gcb.14358 CrossRefPubMedGoogle Scholar
  32. Soulé ME (1985) What is conservation biology? Bioscience 35:727–734.  https://doi.org/10.1016/0169-5347(87)90031-0 CrossRefGoogle Scholar
  33. Swengel SR, Schlicht D, Olsen F, Swengel AB (2011) Declines of prairie butterflies in the midwestern USA. J Insect Conserv 15:327–339.  https://doi.org/10.1007/s10841-010-9323-1 CrossRefGoogle Scholar
  34. Williams BL (2002) Conservation genetics, extinction, and taxonomic status: a case history of the regal fritillary. Conserv Biol.  https://doi.org/10.1046/j.1523-1739.2002.00147.x CrossRefGoogle Scholar
  35. Williams BL, Brawn JD, Paige KN (2003) Landscape scale genetic effects of habitat fragmentation on a high gene flow species: Speyeria idalia (Nymphalidae). Mol Ecol 12:11–20.  https://doi.org/10.1046/j.1365-294X.2003.01700.x CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of Renewable ResourcesUniversity of AlbertaEdmontonCanada
  2. 2.Department of Biological SciencesUniversity of AlbertaEdmontonCanada

Personalised recommendations