Skip to main content Skip to main navigation menu Skip to site footer
Responsive image
Issue: Vol. 5474 No. 4: 1 Jul. 2024
Type: Article
Published: 2024-07-01
DOI: 10.11646/zootaxa.5474.4.1
Page range: 301-354
Abstract views: 7
PDF downloaded: 0

Ancient Grasshoppers: A revision of the genus Bullacris (Orthoptera: Pneumoridae)

Department of Biodiversity and Conservation Biology; University of the Western Cape; Bellville; 7535; South Africa; Kirstenbosch Research Centre; South African National Biodiversity Institute; Newlands; 7725; South Africa; Research and Exhibitions Department; South African Museum; Iziko Museums of South Africa; P.O. Box 61; Cape Town; 8000; South Africa
Statistics in Ecology; Environment and Conservation; Department of Statistical Science; University of Cape Town; Rondebosch; 7700; South Africa
Department of Biodiversity and Conservation Biology; University of the Western Cape; Bellville; 7535; South Africa
Department of Biodiversity and Conservation Biology; University of the Western Cape; Bellville; 7535; South Africa
Orthoptera Bladder grasshoppers South Africa taxonomy morphology acoustics genetics

Abstract

The genus Bullacris in the family Pneumoridae was most recently revised by Dirsh in 1965 based on morphological comparisons between species. However, since that time, new information about the genus and the family has come to light, necessitating a revision of the genus. In addition, the species B. boschimana was originally described based on a single female specimen. Here we present and describe the male of the species for the first time. The aim of this study was to update the current species descriptions by including additional specimens and incorporating additional methods for a more comprehensive comparison. Analyses consisted of morphometric measurements from high-quality images of type specimens, existing South African museum specimens, as well as personally collected specimens. Acoustic signals are also presented and compared between species. In addition, phylogenetic analyses were conducted on the barcoding mitochondrial gene COI and two nuclear genes, namely ITS and 18S. Results show that according to morphological, acoustic and genetic data, B. discolor and B. serrata as well as B. intermedia and B. membracioides share notable similarities. Bullacris discolor and B. serrata share similar phenotypic traits, in which B. discolor can either appear uniform in colour or have a speckled variation that is very similar in appearance to B. serrata. Bullacris intermedia and B. membracioides have a 5% mitochondrial DNA pairwise distance, suggesting that they may have not be fully diverged; however, morphological analysis shows that these species are morphologically distinguishable. It is suggested that these species may have undergone spatial separation at one point; however, further investigation is required. Additional sampling across a wider geographic range is essential to clarify the relationships between B. discolor and B. serrata, as well as between B. intermedia and B. membracioides.

 

References

  1. Alexander, A.J. & van Staaden, M.J. (1989) Alternative sexual tactics in male bladder grasshoppers (Orthoptera, Pneumoridae). In: Bruton, M.N. (Ed.), Alternative Life-History Styles of Animals. Kluwer Academic Publishers, Dordrecht, pp. 261­–­277. https://doi.org/10.1007/978-94-009-2605-9_13
  2. Berven, K.A. & Gill, D.E. (1983) Interpreting geographic variation in life history traits. American Zoologist, 23 (1), 85–97. https://doi.org/10.1093/icb/23.1.85
  3. Bickford, D., Lohman, D.J., Sodhi, N.S., Ng, P.K.L., Meier, R., Winker, K., Ingram, K.K. & Das, I. (2007) Cryptic species as a window on diversity and conservation. Trends in Ecology and Evolution, 22 (3), 148–155. https://doi.org/10.1016/j.tree.2006.11.004
  4. Bidau, C.J., Miño, C.I., Castillo, E.R. & Martí, D.A. (2012) Effects of abiotic factors on the geographic distribution of body size variation and chromosomal polymorphism in two neotropical grasshopper species (Dichroplus: Melanoplinae: Acrididae). Psyche: A Journal of Entomology, 2012, 1–11. https://doi.org/10.1155/2012/863947
  5. Booth, C.L. (1990) Evolutionary significance of ontogenetic colour change in animals. Biological Journal of the Linnean Society, 40 (2), 125–163. https://doi.org/10.1111/j.1095-8312.1990.tb01973.x
  6. Čandek, K. & Kuntner, M. (2015) DNA barcoding gap: reliable species identification over morphological and geographical scales. Molecular Ecology Resources, 15 (2), 268–277. https://doi.org/10.1111/1755-0998.12304
  7. Castner, J.L. & Nickle, D.A. (1995) Observations on the behavior and biology of leaf-mimicking katydids (Orthoptera: Tettigoniidae: Pseudophyllinae: Pterochrozini). Journal of Orthoptera Research, 4, 93–97. https://doi.org/10.2307/3503463
  8. Center for Conservation Bioacoustics (2014) Raven Pro: Interactive Sound Analysis Software. Version 1.5. The Cornell Lab of Ornithology, Ithaca, New York. Available from: http://ravensoundsoftware.com/ (accessed 18 January 2019)
  9. Couldridge, V.C.K. & Gordon, M.L. (2015) Diel variation in signalling and signal transmission in the bladder grasshopper, Bullacris unicolor (Orthoptera; Pneumoridae). Journal of Behaviour, 152 (12–13), 1701–1718. https://doi.org/10.1163/1568539X-00003300
  10. Couldridge, V.C.K. & van Staaden, M.J. (2004) Habitat-dependent transmission of male advertisement calls in bladder grasshoppers (Orthoptera; Pneumoridae). The Journal of experimental biology, 207 (16), 2777–2786. https://doi.org/10.1242/jeb.01092
  11. Dearn, J.M. (1990) Color pattern polymorphism. In: Chapman, R.F. & Joern, A. (Eds.), Biology of grasshoppers. John Wiley & Sons, New York, New York, pp. 517–549.
  12. Dirsh, V.M. (1963) Three new genera and species of the family Pneumoridae (Orthoptera: Acridiodea). Eos, Madr, 39, 177–184.
  13. Dirsh, V.M. (1965) Revision of the family Pneumoridae (Orthoptera: Acridoidea). Bulletin of the British Museum (Natural History) Entomology, 15 (10), 325–396. https://doi.org/10.5962/bhl.part.20544
  14. Donelson, N.C. & van Staaden, M.J. (2005) Alternate tactics in male bladder grasshoppers Bullacris membracioides (Orthoptera : Pneumoridae). Behaviour, 142 (6), 761–778. https://doi.org/10.1163/1568539054729088
  15. Dyer, R.J. (2015) Is there such a thing as landscape genetics? Molecular Ecology, 24 (14), 3518–3528. https://doi.org/10.1111/mec.13249
  16. Endler, J.A. (1992) Signals, signal conditions and the direction of evolution. The American Naturalist, 139, 125–153. https://doi.org/10.1086/285308
  17. Felsenstein, J. (1985) Confidence limits on phylogenies: an approach using bootstrap. Journal of Evolution, 39 (4), 783–791. https://doi.org/10.1111/j.1558-5646.1985.tb00420.x
  18. Folmer, O., Black, M., Hoeh, W., Lutz, R. & Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3 (5), 294–299.
  19. Forrest, T.G. (1994) From Sender to Receiver: Propagation and Environmental Effects on Acoustic Signals. American Zoologist, 34 (6), 644–654. https://doi.org/10.1093/icb/34.6.644
  20. Gordon, M.L. (2017) An acoustic, genetic and morphological review of the genus Bullacris (Orthoptera; Pneumoridae). Unpublished thesis. University of the Western Cape. Available from: http://etd.uwc.ac.za/handle/11394/6119 (accessed 10 June 2024)
  21. Gross, M.R. (1996) Alternative reproductive strategies and tactics: diversity within sexes. Trends in Ecology and Evolution, 11, 92–98. https://doi.org/10.1016/0169-5347(96)81050-0
  22. Hebert, P.D.N., Cywinska, A., Ball, S.L. & deWaard, J.R. (2003) Biological identifications through DNA barcodes. Proceedings of the Royal Society of London. Series B, Biological Science, 270 (1512), 313–321. https://doi.org/10.1098/rspb.2002.2218
  23. Hirtenlehner, S. & Römer, H. (2014) Selective phonotaxis of female crickets under natural outdoor conditions. Journal of comparative physiology A, 200, 239–250. https://doi.org/10.1007/s00359-014-0881-7
  24. Hubert, N. & Hanner, R. (2015) DNA Barcoding, species delineation and taxonomy: a historical perspective. DNA Barcodes, 3, 44–58. https://doi.org/10.1515/dna-2015-0006
  25. Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Meintjes, P. & Drummond, A. (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28, 1647–1649. https://doi.org/10.1093/bioinformatics/bts199
  26. Kowalski, K.N., Lakes-Harlan, R., Lehmann, G.U.C. & Strauss, J. (2014) Acoustic defence in an insect: characteristics of defensive stridulation and differences between the sexes in the tettigoniid Poecilimon ornatus (Schmidt 1850). Zoology, 117 (5), 329–336. https://doi.org/10.1016/j.zool.2014.04.007
  27. Krishnamurthy, P.K. & Francis, R.A. (2012) A critical review on the utility of DNA barcoding in biodiversity conservation. Biodiversity and Conservation, 21, 1901–1919. https://doi.org/10.1007/s10531-012-0306-2
  28. Kumar, S., Stecher, G. & Tamura, K. (2016) MEGA 7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33 (7), 1870–1874. https://doi.org/10.1093/molbev/msw054
  29. Lipscomb, D., Platnick, N. & Wheeler, Q. (2003) The intellectual content of taxonomy: a comment on DNA taxonomy. Trend in Ecology & Evolution, 18 (2), 64–66. https://doi.org/10.1016/S0169-5347(02)00060-5
  30. Manier, M.K. & Arnold, S.J. (2006) Ecological correlates of population genetic structure: a comparative approach using a vertebrate metacommunity. Proceedings of the Royal Society of London. Series B, Biological Sciences, 273 (1604), 3001–3009. https://doi.org/10.1098/rspb.2006.3678
  31. Masaki, S. (1967) Geographic variation and climate adaptation in a field cricket (Orthoptera: Gryllidae). Evolution, 21 (4), 725–741. https://doi.org/10.1111/j.1558-5646.1967.tb03430.x
  32. Miller, M.A., Pfeiffer, W. & Schwartz T. (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Proceedings of the Gateway Computing Environments workshop (GCE). New Orleans, Louisiana, pp. 1–8. https://doi.org/10.1109/GCE.2010.5676129
  33. Morton, E.S. (1975) Ecological sources of selection on avian sounds. The American Naturalist, 109 (965), 17–34. https://doi.org/10.1086/282971
  34. Mucina, L. & Rutherford, M.C. (Eds.) (2006) The vegetation of South Africa, Lesotho and Swaziland. Strelitzia. Vol. 19. South African National Biodiversity Institute, Pretoria, 817 pp.
  35. Nabours, R.K., Larson, I. & Hartwig, N. (1933) Inheritance of color patterns in the grouse locust Acrydium arenosum Burmeister (Tettigidae). Genetics, 18, 159–171. https://doi.org/10.1093/genetics/18.2.159
  36. Peralta-Rincon, J.R., Escudero, G., Edelaar, P. (2017) Phenotypic plasticity in color without molt in adult grasshoppers of the genus Sphingonotus (Acrididae: Oedipodinae). Journal of Orthoptera Research, 26 (1), 21–27. https://doi.org/10.3897/jor.26.14550
  37. Peters, R.H. (1983) The Ecological Implications of Body Size (Cambridge studies in Ecology). Cambridge University Press, Cambridge, 329 pp. https://doi.org/10.1017/CBO9780511608551
  38. Pires, A.C. & Marinoni, L. (2010) DNA barcoding and traditional taxonomy unified through Integrative Taxonomy: a view that challenges the debate questioning both methodologies. Biota Neotropica, 10 (2), 339–346. https://doi.org/10.1590/S1676-06032010000200035
  39. Rambaut, A. (2014) FigTree. Version 1.4.1. software. Institute of Evolutionary Biology, University of Edinburgh. Available from: http://tree.bio.ed.ac.uk/software/figtree/ (accessed 5 February 2018)
  40. Richards, O.W. & Waloff, N. (1954) Studies on the biology and population dynamics of British grasshoppers. Anti-locust Bulletin Vol. 17. Anti-locust Research Centre, London, 182 pp.
  41. Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D.L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M.A. & Huelsenbeck, J.P. (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61 (3), 539–542. https://doi.org/10.1093/sysbio/sys029
  42. Rowell, C.H.F. (1971) The variable coloration of the acridoid grasshoppers. Advances in Insect Physiology, 8, 145–198. https://doi.org/10.1016/S0065-2806(08)60197-6
  43. Roy, L., Dowling, A.P.G., Chauve, C.M. & Buronfosse, T. (2008) Delimiting species boundaries within Dermanyssus Dugès, 1834 (Acari: Dermanyssidae) using a total evidence approach. Molecular Phylogenetics and Evolution, 50, 446–470. https://doi.org/10.1016/j.ympev.2008.11.012
  44. Rubinoff, D. (2006) DNA Barcoding Evolves into the Familiar. Society for Conservation Biology, 20 (5), 1548–1549. https://doi.org/10.1111/j.1523-1739.2006.00542.x
  45. Rubtzov, I.A. (1935) Phase variation in non-swarming grasshoppers. Bulletin of Entomological Research, 26 (4), 499–520. https://doi.org/10.1017/S0007485300036841
  46. Sathyan, R., Engelbrecht, A.D. & Couldridge, V.C.K. (2017) Morphological, acoustic and genetic divergence in the bladder grasshopper Bullacris unicolor. Ethology, Ecology and Evolution, 29 (6), 552–573. https://doi.org/10.1080/03949370.2017.1287915
  47. Schindelin, J., Rueden, C.T. & Hiner, M.C. (2015) The ImageJ ecosystem: An open platform for biomedical image analysis. Molecular Reproduction and Development, 82 (7–8), 518–529. https://doi.org/10.1002/mrd.22489
  48. Scotland, R.W., Olmstead, R.G. & Bennett, J.R. (2003) Phylogeny reconstruction: The role of morphology. Systematic Biology, 52 (4), 539–548. https://doi.org/10.1080/10635150309309
  49. Song, H., Amédégnato, C., Cigliano, M.M., Desutter-Grandcolas, L., Heads, S.W., Huang, Y., Otte, D. & Whiting, M.F. (2015) 300 million years of diversification: elucidating the patterns of orthopteran evolution based on comprehensive taxon and gene sampling. Cladistics, 31 (6), 621–651. https://doi.org/10.1111/cla.12116
  50. Song, H., Foquet, B., Mariño-Pérez, R. & Woller, D.A. (2017) Phylogeny of locusts and grasshoppers reveals complex evolution of density-dependent phenotypic plasticity. Scientific Reports, 7, 6606. https://doi.org/10.1038/s41598-017-07105-y
  51. Stamatakis, A. (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 22 (21), 2688–2690. https://doi.org/10.1093/bioinformatics/btl446
  52. Tautz, D., Arctander, P., Minelli, A., Thomas, R.H. & Vogler, A.P. (2002) DNA points the way ahead in taxonomy. Nature, 418, 479. https://doi.org/10.1038/418479a
  53. Tautz, D., Arctander, P., Minelli, A., Thomas, R.H. & Vogler, A.P. (2003) A plea for DNA taxonomy. Trends in Ecology & Evolution, 18 (2), 71–74. https://doi.org/10.1016/S0169-5347(02)00041-1
  54. Trewick, S.A. (2008) DNA Barcoding is not enough: mismatch of taxonomy and genealogy in New Zealand grasshoppers (Orthoptera: Acrididae). Cladistics, 24, 240–254. https://doi.org/10.1111/j.1096-0031.2007.00174.x
  55. Whitman, D.W. & Agrawal, A.A. (2009) What is phenotypic plasticity and why is it important? In: Whitman, D. W. & Ananthakrishman, T. N. (Eds.), Phenotypic Plasticity of Insects. Science Publishers, Washington, pp. 1–63.
  56. Whitney, J.E., Gido, K.B. & Propst, D. (2014) Factors associated with the success of native and non-native species in an unfragmented arid-land riverscape. Canadian Journal of Fisheries and Aquatic Sciences, 71 (8), 1134–1145. https://doi.org/10.1139/cjfas-2014-0153
  57. Wilkins, M.R., Seddon, N. & Safran, R.J. (2013) Evolutionary divergence in acoustic signals: causes and consequences. Trends in Ecology & Evolution, 28 (3), 156–166. https://doi.org/10.1016/j.tree.2012.10.002
  58. Will, K.W. & Rubinoff, D. (2004) Myth of the Molecule: DNA barcodes for species cannot replace morphology for identification and classification. Cladistics, 20 (1), 47–55. https://doi.org/10.1111/j.1096–0031.2003.00008.x
  59. Will, K.W., Mishler, B.D. & Wheeler, Q.D. (2005) The Perils of DNA Barcoding and the Need for Integrative taxonomy. Systematic Biology, 54 (5), 844–851. https://doi.org/10.1080/10635150500354878