Published November 14, 2023 | Version v1
Journal article Open

Morphological, acoustic and genetic identification of a reproducing population of the invasive African clawed frog Xenopus laevis (Anura, Pipidae) recently discovered in Belgium

  • 1. Scientific Heritage, Royal Belgian Institute of Natural Sciences, Brussels, Belgium
  • 2. Scientific Heritage, Royal Belgian Institute of Natural Sciences, Brussels, Belgium|Royal Museum for Central Africa, Tervuren, Belgium
  • 3. Université Libre de Bruxelles, Brussels, Belgium
  • 4. Operational Directorate Natural Environment, Royal Belgian Institute of Natural Sciences, Brussels, Belgium|Scientific Heritage, Royal Belgian Institute of Natural Sciences, Brussels, Belgium
  • 5. Barcoding Facility for Organisms and Tissues of Policy Concern (BopCo), Royal Belgian Institute of Natural Sciences, Brussels, Belgium
  • 6. University of Antwerp, Antwerp, Belgium|Barcoding Facility for Organisms and Tissues of Policy Concern (BopCo), Royal Belgian Institute of Natural Sciences, Brussels, Belgium

Description

Using external morphology of adults and tadpoles, osteology from high-resolution microcomputed tomography, vocalization analysis, and DNA sequence data, the identity of a reproducing Belgian population of invasive Xenopus at the current northernmost edge of the distribution of the genus in Europe was assessed. All data concur to an identification as Xenopus (Xenopus) laevis (Daudin, 1802). Genetically it is most closely related to populations of the Cape region in South Africa. No studies on the natural history of the Belgian Xenopus population and its impact on the local environment have been made to date.

Files

ZK_article_103702.pdf

Files (12.5 MB)

Name Size Download all
md5:48e5b2ccc3512d83856f7a397f1b93d3
12.5 MB Preview Download

System files (202.9 kB)

Name Size Download all
md5:e9498e1c60cba8e5b5a556c1b01b00c0
202.9 kB Download

Linked records

Additional details

References

  • Araspin L, Martinez AS, Wagener C, Courant J, Louppe V, Padilla P, Measey J, Herrel A (2020) Rapid shifts in the temperature dependence of locomotor performance in an invasive frog, Xenopus laevis, implications for conservation. Integrative and Comparative Biology 60(2): 456–466. https://doi.org/10.1093/icb/icaa010
  • Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16(1): 37–48. https://doi.org/10.1093/oxfordjournals.molbev.a026036
  • Blackburn DC, Paluh DJ, Krone I, Roberts EM, Stanley EL, Stevens NJ (2019) The earliest fossil of the African Clawed Frog (genus Xenopus) from Sub-Saharan. Journal of Herpetology 53(2): 125–130. https://doi.org/10.1670/18-139
  • Cannatella DC, de Sá RO (1993) Xenopus laevis as a model organism. Systematic Biology 42(4): 476–507. https://doi.org/10.1093/sysbio/42.4.476
  • Cannatella DC, Trueb L (1988) Evolution of pipoid frogs: Intergeneric relationships of the aquatic frog family Pipidae (Anura). Zoological Journal of the Linnean Society 94(1): 1–38. https://doi.org/10.1111/j.1096-3642.1988.tb00880.x
  • Channing A, Rödel M-O, Channing J (2012) Tadpoles of Africa. The biology and identification of all known tadpoles in sub-Saharan Africa. Edition Chimaira, Frankfurt am Main, 402 pp.
  • Courant J, Vogt S, Marques R, Measey J, Secondi J, Rebelo R, De Villiers A, Ihlow F, De Busschere C, Backeljau T, Rödder D, Herrel A (2017) Are invasive populations characterized by a broader diet than native populations? PeerJ 5: e3250. https://doi.org/10.7717/peerj.3250
  • Courant J, Secondi J, Vollette E, Herrel A, Thirion J-M (2018a) Assessing the impacts of the invasive frog, Xenopus laevis, on amphibians in western France. Amphibia-Reptilia 39(2): 219–227. https://doi.org/10.1163/15685381-17000153
  • Courant J, Vollette E, Secondi J, Herrel A (2018b) Changes in the aquatic macroinvertebrate communities throughout the expanding range of an invasive anuran. Food Webs 17: e00098. https://doi.org/10.1016/j.fooweb.2018.e00098
  • Courant J, Secondi J, Guillemet L, Vollette E, Herrel A (2019) Rapid changes in dispersal on a small spatial scale at the range edge of an expanding population. Evolutionary Ecology 33(4): 599–612. https://doi.org/10.1007/s10682-019-09996-x
  • Daudin FM (1802) Histoire naturelle des Rainettes, des Grenouilles et des Crapauds. Levrault, Paris, 108 pp [+ pls I–XXXVIII].
  • De Busschere C, Courant J, Herrel A, Rebelo R, Rödder D, Measey GJ, Backeljau T (2016) Unequal contribution of native South African phylogeographic lineages to the invasion of the African clawed frog, Xenopus laevis, in Europe. PeerJ 4: e1659. https://doi.org/10.7717/peerj.1659
  • Delpire E, Gagnon KB, Ledford JL, Wallace JM (2011) Housing and husbandry of Xenopus laevis affect the quality of oocytes for heterologous expression studies. Journal of the American Association for Laboratory Animal Science 50(1): 46–53.
  • Deuchar EM (1972) Xenopus laevis and developmental biology. Biological Reviews 47(1): 37–112. https://doi.org/10.1111/j.1469-185X.1972.tb00970.x
  • Du Preez LH, Solomon KR, Carr JA, Giesy JP, Gross TS, Kendall RJ, Smith EE, Van der Kraak G, Weldon C (2005) Population structure of the African Clawed Frog (Xenopus laevis) in maize-growing areas with atrazine application versus non-maize-growing areas in South Africa. African Journal of Herpetology 54(1): 61–68. https://doi.org/10.1080/21564574.2005.9635518
  • Evans BJ, Greenbaum E, Kusamba C, Carter TF, Tobias ML, Mendel SA, Kelley DB (2011) Description of a new octoploid frog species (Anura: Pipidae: Xenopus) from the Democratic Republic of the Congo, with a discussion of the biogeography of African clawed frogs in the Albertine Rift. Journal of Zoology 283(4): 276–290. https://doi.org/10.1111/j.1469-7998.2010.00769.x
  • Evans BJ, Carter TF, Greenbaum E, Gvoždík V, Kelley DB, McLaughlin PJ, Pauwels OSG, Portik DM, Stanley EL, Tinsley RC, Tobias ML, Blackburn DC (2015) Genetics, morphology, advertisement calls, and historical records distinguish six new polyploid species of African clawed frog (Xenopus, Pipidae) from West and Central Africa. PLoS ONE 10(12): e0142823. https://doi.org/10.1371/journal.pone.0142823
  • Evans BJ, Gansauge M-T, Stanley EL, Furman BLS, Cauret CMS, Ofori-Boateng C, Gvoždik V, Streicher JW, Greenbaum E, Tinsley RC, Meyer M, Blackburn DC (2019) Xenopus fraseri: Mr. Fraser, where did your frog come from? PLoS ONE 14(9): e0220892. https://doi.org/10.1371/journal.pone.0220892
  • Fainsod A, Moody SA (2022) Xenopus. From basic biology to disease models in the genomic era. CRC Press, Boca Raton and Oxon, [xi +] 347 pp. https://doi.org/10.1201/9781003050230
  • 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.
  • Furman BLS, Bewick AJ, Harrison TL, Greenbaum E, Gvoždík V, Kusamba C, Evans BJ (2015) Pan-African phylogeography of a model organism, the African clawed frog 'Xenopus laevis'. Molecular Ecology 24(4): 909–925. https://doi.org/10.1111/mec.13076
  • Gombeer S, Meganck K, Vanderheyden A, Smitz N, Pauwels O, Brecko J, De Meyer M, Backeljau T (2022) Detecting Xenopus laevis in Belgium using eDNA and qPCR. In: 22nd International Conference on Aquatic Invasive Species, April 18–22, 2022, Thermae Palace Hotel, Oostende, Belgium, 42–42.
  • Goodman CM, Jongsma GFM, Hill JE, Stanley EL, Tuckett QM, Blackburn DC, Romagosa CM (2021) A case of mistaken identity: Genetic and anatomical evidence reveals the cryptic invasion of Xenopus tropicalis in central Florida. Journal of Herpetology 55(1): 62–69. https://doi.org/10.1670/20-083
  • Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16(3): 183–190.
  • Gurdon JB, Hopwood N (2000) The introduction of Xenopus laevis into developmental biology: Of empire, pregnancy testing and ribosomal genes. The International Journal of Developmental Biology 44: 43–50.
  • Hill J, Lawson KM, Tuckett QM (2017) First record of a reproducing population of the African clawed frog Xenopus laevis Daudin, 1802 in Florida (USA). BioInvasions Records 6(1): 87–94. https://doi.org/10.3391/bir.2017.6.1.14
  • Kessing BD, Croom H, Martin A, McIntosh C, McMillan WO, Palumbi S (1989) The simple fool's guide to PCR, version 1.0. Special Publication of the Department of Zoology, University of Hawaii, Honolulu, 17 pp.
  • Leininger EC, Kelley DB (2015) Evolution of courtship songs in Xenopus: Vocal pattern generation and sound production. Cytogenetic and Genome Research 145(3–4): 302–314. https://doi.org/10.1159/000433483
  • Lobos G, Measey GJ (2002) Invasive populations of Xenopus laevis (Daudin) in Chile. The Herpetological Journal 12: 163–168.
  • Lorrain-Soligon L, Secondi J (2022) Quantification of underwater calling and foraging activities in the African clawed frog Xenopus laevis. Amphibia-Reptilia 43(4): 357–367. https://doi.org/10.1163/15685381-bja10107 [Published online]
  • Mora M, Pons DJ, Peñafiel-Ricaurte A, Alvarado-Rybak M, Lebuy S, Soto-Azat C (2019) High abundance of invasive African clawed frog Xenopus laevis in Chile: Challenges for their control and updated invasive distribution. Management of Biological Invasions 10(2): 377–388. https://doi.org/10.3391/mbi.2019.10.2.11
  • Padilla P, Tallis J, Hurst J, Courant J, James RS, Herrel A (2020) Do muscle contractile properties drive differences in locomotor performance in invasive populations of Xenopus laevis in France? Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 190(6): 771–778. https://doi.org/10.1007/s00360-020-01310-4
  • Peralta-García A, Valdez-Villavicencio JH, Galina-Tessaro P (2014) African clawed frog (Xenopus laevis) in Baja California: A confirmed population and possible ongoing invasion in Mexican watersheds. The Southwestern Naturalist 59(3): 431–434. https://doi.org/10.1894/NBF-12.1
  • Porro LB, Richards CT (2017) Digital dissection of the model organism Xenopus laevis using contrast-enhanced computed tomography. Journal of Anatomy 231(2): 169–191. https://doi.org/10.1111/joa.12625
  • Robert J (2020) Experimental platform using the amphibian Xenopus laevis for research in fundamental and medical immunology. Cold Spring Harbor Protocols 247–251(7): pdb.top106625. https://doi.org/10.1101/pdb.top106625
  • Rödder D, Ihlow F, Courant J, Secondi J, Herrel A, Rebelo R, Measey GJ, Lillo F, De Villiers FA, De Busschere C, Backeljau T (2017) Global realized niche divergence in the African clawed frog Xenopus laevis. Ecology and Evolution 7(11): 4044–4058. https://doi.org/10.1002/ece3.3010
  • Rozas J, Ferrer-Mata A, Sànchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE, Sànchez-Gracia A (2017) DnaSP v6: DNA Sequence Polymorphism analysis of large datasets. Molecular Biology and Evolution 34(12): 3299–3302. https://doi.org/10.1093/molbev/msx248
  • Schoeman AL, du Preez LH, Kmentová N, Vanhove MPM (2022) A monogenean parasite reveals the widespread translocation of the African clawed frog in its native range. Journal of Applied Ecology 59(11): 2670–2687. https://doi.org/10.1111/1365-2664.14271
  • Slater BJ, Liu KJ, Kwan MD, Quarto N, Longaker MT (2009) Cranial osteogenesis and suture morphology in Xenopus laevis: A unique model system for studying craniofacial development. PLoS ONE 4(1): e3914. https://doi.org/10.1371/journal.pone.0003914
  • Tapley B, Michaels CJ, Doherty-Bone TM (2015) The tadpole of the Lake Oku clawed frog Xenopus longipes (Anura; Pipidae). Zootaxa 3981(4): 597–600. https://doi.org/10.11646/zootaxa.3981.4.10
  • Tinsley RC (1973) Studies on the ecology and systematics of a new species of clawed toad, the genus Xenopus, from western Uganda. Journal of Zoology 169(1): 1–27. https://doi.org/10.1111/j.1469-7998.1973.tb04650.x
  • Tinsley RC (1995) A new species of Xenopus (Anura: Pipidae) from the highlands of Ethiopia. Amphibia-Reptilia 16(4): 375–388. https://doi.org/10.1163/156853895X00451
  • Tinsley RC, Stott LC, Viney ME, Mable BK, Tinsley MC (2015) Extinction of an introduced warm-climate alien species, Xenopus laevis, by extreme weather events. Biological Invasions 17(11): 3183–3195. https://doi.org/10.1007/s10530-015-0944-x
  • Tobias ML, Barnard C, O'Hagan R, Horng SH, Rand M, Kelley DB (2004) Vocal communication between male Xenopus laevis. Animal Behaviour 67(2): 353–365. https://doi.org/10.1016/j.anbehav.2003.03.016
  • van Doorn L, Speybroeck J, Adriaens T, Brys R (2022) Environmental DNA sampling for African clawed frog in Flanders, Wallonia and France in 2020. Reports of the Research Institute for Nature and Forest, 6. Research Institute for Nature and Forest, Brussels, 17 pp. https://doi.org/10.21436/inbor.71707757
  • Vigny C (1979) Morphologie larvaire de 12 espèces et sous-espèces du genre Xenopus. Revue Suisse de Zoologie 86(4): 877–891. https://doi.org/10.5962/bhl.part.82345
  • Wang S, Hong Y, Measey J (2019) An established population of African clawed frogs, Xenopus laevis (Daudin, 1802), in mainland China. BioInvasions Records 8(2): 457–464. https://doi.org/10.3391/bir.2019.8.2.29
  • Zahn N, James-Zorn C, Ponferrada VG, Adams DS, Grzymkowski J, Buchholz DR, Nascone-Yoder NM, Horb M, Moody SA, Vize PD, Zorn AM (2022) Normal table of Xenopus development: A new graphical resource. Development 149(14): dev200356. https://doi.org/10.1242/dev.200356