Revista de Biología Tropical ISSN Impreso: 0034-7744 ISSN electrónico: 2215-2075

OAI: https://revistas.ucr.ac.cr/index.php/rbt/oai
A new giant velvet worm from Costa Rica suggests absence of the genus Peripatus (Onychophora: Peripatidae) in Central America
PDF
DIGITAL APPENDIX
HTML
DIGITAL APPENDIX

Keywords

onychophoran speciation
Costa Rican biodiversity
endemism
saproxilic taxa
phylogenetics
especiación de onicóforos
biodiversidad de Costa Rica
endemismo
fauna saproxílica
filogenética

How to Cite

Barquero González, J. P., Sánchez-Vargas, S., & Morera-Brenes, B. (2020). A new giant velvet worm from Costa Rica suggests absence of the genus Peripatus (Onychophora: Peripatidae) in Central America. Revista De Biología Tropical, 68(1), 300–320. https://doi.org/10.15517/rbt.v68i1.37675

Abstract

Introduction: Neotropical onychophoran taxonomy and diversity has been poorly investigated. Recent studies have discovered problems in species classification: they have questioned the accepted genera and the actual number of species. This is true in Costa Rica, where several unidentified species have been reported. Objective: The objective of this investigation was to evaluate the occurrence of the accepted genera in this country, and to describe a new genus and species from Central America. Methods: In 2017, we collected one onychophoran in the Keköldi Indigenous Reserve in Talamanca, Limón, Costa Rica. The specimen gave birth to several offspring. Therefore, seven organisms were analyzed. Light microscopy was used to observe the gross morphology in all samples. The detailed morphology was studied in the biggest specimen with scanning electron microscopy; after that, we performed a phylogenetic analysis with the corresponding sequence of COI. Results: According to our results, a new genus and species of giant onychophoran was found. The genus was identified by its giant size, apical piece of seven scale ranks, large conical primary papillae, dorso-median furrow flanked by two-three accessory papillae, the absence of hyaline organs and a marked sexual dimorphism with respect to the number of legs. The new species presents a particular head pattern, as well as novel structures like cephalic papillae, accessory papillae with rudimentary apical pieces, and a lack of antennal chemoreceptors. Phylogenetic analysis rendered our genus as monophyletic and includes Peripatus solorzanoi, which is grouped within the Central American clade. As our species is clustered inside the Costa Rica-Panamanian group, it is not related to the Caribbean Island nor Guyanan Shield samples, home of Epiperipatus and Peripatus respectively. Therefore, we suggest that those genera do not occur in Central America, and a new genus exists: Mongeperipatus, gen. nov. Conclusion: We concluded that Costa Rica is home to a diversity of undescribed onychophorans that requires specific studies to help clarify the taxonomy and evolutionary relationships of the group to justify their protection.

https://doi.org/10.15517/rbt.v68i1.37675
PDF
DIGITAL APPENDIX
HTML
DIGITAL APPENDIX

References

Akaike, H. (1973). Maximum likelihood identification of Gaussian autoregressive moving average models. Biometrika, 60(2), 255-265.

Allwood, J., Gleeson, D., Mayer, G., Daniels, S., Beggs, J.R., & Buckley, T.R. (2010). Support for vicariant origins of the New Zealand Onychophora. Journal of Biogeography, 37(4), 669-681.

Baer, A., Hänsch, S., Mayer, G., Harrington, M.J., & Schmidt, S. (2018). Reversible supramolecular assembly of velvet worm adhesive fibers via electrostatic interactions of charged phosphoproteins. Biomacromolecules, 19(10), 4034-4043.

Barquero-González, J.P., Acosta-Chaves, V.J., Sotela, M.L., Brenes, F.V., & Morera-Brenes, B. (2016a). Evidencia fotográfica de especies desconocidas de onicóforos (Onychophora: Peripatidae) de Costa Rica. UNED Research Journal, 8(2), 139-147.

Barquero-González, J.P., Alvarado Cabrera, A., Valle-Cubero, S., Monge-Nájera, J., & Morera-Brenes, B. (2016b). The geographic distribution of Costa Rican velvet worms (Onychophora: Peripatidae). Revista de Biología Tropical, 64(4), 1401-1414.

Barquero-González, J.P., Morera-Brenes, B., & Monge-Nájera, J. (2018). The relationship between humidity, light and the activity pattern of a velvet worm, Epiperipatus sp. (Onychophora: Peripatidae), from Bahía Drake, South Pacific of Costa Rica. Brazilian Journal of Biology, 78(3), 408-413.

Barquero-González, J.P., Vega-Hidalgo, A., & Monge-Nájera, J. (2019). Feeding behavior of Costa Rican velvet worms: food hiding, parental feeding investment and ontogenetic diet shift (Onychophora: Peripatidae). UNED Research Journal, 11(2), 85-88.

Barnes, A., & Daniels, S.R. (2019). On the importance of fine-scale sampling in detecting alpha taxonomic diversity among saproxylic invertebrates: A velvet worm (Onychophora: Opisthopatus amaxhosa) template. Zoologica Scripta, 48(2), 243-262.

Bouvier, E.L. (1899). Contribution a l’histoire des Péripates Américanes. Annales de la Societé Entomologique de France, 68, 385-450.

Bouvier, E.L. (1902a). Un Péripate de Costa-Rica. Bulletin de la Société Entomologique de France, 7(15), 239-240.

Bouvier, E.L. (1902b). Peripatus biolleyi, Onychophore nouveau de Costa Rica. Bulletin de la Société Entomologique de France, 16, 258-259.

Bouvier, E.L. (1905). Monographie des Onychophores I. Annales des Sciences Naturelles, 9(2), 1-383.

Braband, A., Podsiadlowski, L., Cameron, S.L., Daniels, S., & Mayer, G. (2010a). Extensive duplication events account for multiple control regions and pseudo-genes in the mitochondrial genome of the velvet worm Metaperipatus inae (Onychophora, Peripatopsidae). Molecular Phylogenetics and Evolution, 57(1), 293-300.

Braband, A., Cameron, S.L., Podsiadlowski, L., Daniels, S.R., & Mayer, G. (2010b). The mitochondrial genome of the onychophoran Opisthopatus cinctipes (Peripatopsidae) reflects the ancestral mitochondrial gene arrangement of Panarthropoda and Ecdysozoa. Molecular Phylogenetics and Evolution, 57(1), 285-292.

Brinck, P. (1957). Onychophora, a review of South African species, with a discussion on the significance of the geographical distribution of the group. South African Animal Life, 4, 7-32.

Brito, S.V., Pereira, J.C., Ferreira, F.S., Vasconcellos, A., & Almeida, W.O. (2010). Epiperipatus cratensis sp. nov. (Onychophora: Peripatidae) from northeastern Brazil. Neotropical Biology and Conservation, 5(1), 47-52.

Briscoe, D.A., & Tait, N.N. (1995). Allozyme evidence for extensive and ancient radiations in Australian Onychophora. Zoological Journal of the Linnean Society, 114(1), 91-102.

Castresana, J. (2000). Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution, 17(4), 540-552.

Carvalho, A. (1941). Nota prévia sôbre uma nova espécie de “Peripatus” do Brasil Central. Brazilian Journal of Biology, 1(4), 447-448.

Chagas-Júnior, A., & Sampaio Costa, C. (2014). Macroperipatus ohausi: redescription and taxonomic notes on its status (Onychophora: Peripatidae). International Journal of Tropical Biology and Conservation, 62(3), 977-985.

Clark, A.H. (1913). A revision of the American species of Peripatus. Proceedings of the Biological Society of Washington, 26, 15-19.

Cockerell, T.D.A. (1908). Monographie des Onychophores by Bouvier. Science, 27, 619-621.

Concha, A., Mellado, P., Morera-Brenes, B., Costa, C., Mahadevan, L., & Monge-Nájera, J. (2015). Oscillation of the velvet worm slime jet by passive hydrodynamic instability. Nature Communications, 6, 6292.

Corrales-Ureña, Y.R., Sanchez, A., Pereira, R., Rischka, K., Kowalik, T., & Vega-Baudrit, J. (2017). Extracellular micro and nanostructures forming the velvet worm solidified adhesive secretion. Materials Research Express, 4(12), 125013.

Cunha, W.T., Santos, R.C., Araripe, J., Sampaio, I., Schneider, H., & Rêgo, P.S. (2017). Molecular analyses reveal the occurrence of three new sympatric lineages of velvet worms (Onychophora: Peripatidae) in the eastern Amazon basin. Genetics and Molecular Biology, 40(1), 147-152.

Daniels, S.R. (2011). Genetic variation in the Critically Endangered velvet worm Opisthopatus roseus (Onychophora: Peripatopsidae). African Zoology, 46(2), 419-424.

Daniels, S.R., Picker, M.D., Cowlin, R.M., & Hamer, M.L. (2009). Unravelling evolutionary lineages among South African velvet worms (Onychophora: Peripatopsis) provides evidence for widespread cryptic speciation. Biological Journal of the Linnean Society, 97(1), 200-216.

Daniels, S.R., & Ruhberg, H. (2010). Molecular and morphological variation in a South African velvet worm Peripatopsis moseleyi (Onychophora, Peripatopsidae): evidence for cryptic speciation. Journal of Zoology, 282(3), 171-179.

Daniels, S.R., McDonald, D.E., & Picker, M.D. (2013). Evolutionary insight into the Peripatopsis balfouri sensu lato species complex (Onychophora: Peripatopsidae) reveals novel lineages and zoogeographic patterning. Zoologica Scripta, 42(6), 656-674.

Daniels, S.R., Dambire, C., Klaus, S., & Sharma, P.P. (2016). Unmasking alpha diversity, cladogenesis and biogeographical patterning in an ancient panarthropod lineage (Onychophora: Peripatopsidae: Opisthopatus cinctipes) with the description of five novel species. Cladistics, 32(5), 506-537.

Dzik, J., & Krumbiegel, G. (1989). The oldest onychophoran, Xenusion - a link connecting phyla. Lethaia, 22, 169-181.

Evans, R. (1901). On two new species of Onychophora from the Siamese Malay States. Quarterly Journal of Microscopical Science, 44, 473-538.

Fuhrmann, O. (1913). Quelques nouveaux Péripates américains. Mémoires de la Société Neuchâteloise des Sciences Naturelles, 5, 176-192.

Garwood, R.J., Edgecombe, G.D., Charbonnier, S., Chabard, D., Sotty, D., & Giribet, G. (2016). Carboniferous Onychophora from Montceau les Mines, France, and onychophoran terrestrialization. Invertebrate Biology, 135(3), 179-190.

Giribet, G., Buckman-Young, R.S., Costa, C.S., Baker, C.M., Benavides, L.R., Branstetter, M.G., & Pinto-da-Rocha, R. (2018). The ‘Peripatos’ in Eurogondwana?–Lack of evidence that south-east Asian onychophorans walked through Europe. Invertebrate Systematics, 32(4), 840-863.

Gleeson, D.M., & Ruhberg, H. (2010). Phylum Onychophora–velvet worms, peripatus. New Zealand Inventory of Biodiversity: Kingdom Animalia, 2, 36-39.

Guilding, L. (1826). Mollusca Carribbeana. The Zoological Journal, 2, 437-449.

Haritos, V.S., Niranjane, A., Weisman, S., Trueman, H.E., Sriskantha, A., & Sutherland, T.D. (2010). Harnessing disorder: onychophorans use highly unstructured proteins, not silks, for prey capture. Proceedings of the Royal Society of London B: Biological Sciences, 277(1698), 3255-3263.

Holdridge, L.R. (1967). Life zone ecology. San José, Costa Rica: Centro Científico Tropical.

Katoh, K., Kuma, K., Toh, H., & Miyata, T. (2005). MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Research, 33, 511-518.

Kemp, S. (1913). Preliminary note on a new genus of Onychophora from the N. E. frontier of India. Records of the Indian Museum, 9, 241-242.

von Kennel, J. (1883). Entwicklungsgeschichte von Peripatus. Zoologischer. Anzeiger, 6(150), 531-537.

Kuraku, S., Zmasek, C.M., Nishimura, O., & Katoh, K. (2013). aLeaves facilitates on-demand exploration of metazoan gene family trees on MAFFT sequence alignment server with enhanced interactivity. Nucleic Acids Research, 41, W22-W28.

Lacorte, G.A., Oliveira, I.S., & Fonseca, C.G. (2011). Population structure and demographic inferences concerning the endangered onychophoran species Epiperipatus acacioi (Onychophora: Peripatidae). Genetics and Molecular Research, 10(4), 2775-2785.

Lavallard, R., & Campiglia, S. (1975). Contribution a la biologie de Peripatus acacioi Marcus et Marcus (Onychophore). V. Etude des Naissances dans un elevage de laboratiore. Zoologischer Anzeiger, 195, 338-350.

Marcus, E., & Marcus, E. (1955). A new Peripatus from Minas Gerais, Brazil. Anais da Academia Brasileira de Ciencias, 27, 189-193.

Mayer, G. (2007). Metaperipatus inae sp. nov. (Onychophora: Peripatopsidae) from Chile with a novel ovarian type and dermal insemination. Zootaxa, 1440(1), 21-37.

Miller, M.A., Pfeiffer, W., & Schwartz, T. (2010). Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Gateway Computing Environments Workshop, 1-8.

Monge-Nájera, J. (1994). Reproductive trends, habitat type and body characteristics in velvet worms (Onychophora). Revista de Biología Tropical, 42(3), 611-622.

Monge-Nájera, J. (1995). Phylogeny, biogeography and reproductive trends in the Onychophora. Zoological Journal of the Linnean Society, 114(1), 21-60.

Monge-Nájera, J. (1996). Jurassic–Pliocene biogeography: testing a model with velvet worm (Onychophora) vicariance. International Journal of Tropical Biology and Conservation, 44(1), 147-152.

Monge-Nájera, J. (2017). The power of short lectures to improve support for biodiversity conservation of unpopular organisms: an experiment with worms. UNED Research Journal, 9(1), 145-150.

Monge-Nájera, J. (2018). City Worms (Onychophora): why do fragile invertebrates from an ancient lineage live in heavily urbanized areas? UNED Research Journal, 10(1), 91-94.

Monge-Nájera, J., Barrientos, Z., & Aguilar, F. (1993). Behavior of Epiperipatus biolleyi (Onychophora: Peripatidae) under laboratory conditions. Revista de Biología Tropical, 41(3A), 689-696.

Monge-Nájera, J. & Morera-Brenes, B. (2015). Velvet Worms (Onychophora) in Folklore and Art: Geographic Pattern, Types of Cultural Reference and Public Perception. British Journal of Education, Society & Behavioural Science, 10(3), 1-9.

Mora, M., Herrera, A., & León, P. (1996). The genome of Epiperipatus biolleyi (Peripatidae), a Costa Rican onychophoran. Revista de Biología Tropical, 44(1), 153-157.

Morera-Brenes, B., & León, M.D. (1986). Description of Macroperipatus valerioi n. sp. from Costa Rica, and comments on the genus Macroperipatus (Onychophora: Peripatidae). Revista de Biología Tropical, 34(2), 277-282.

Morera Brenes, B., Monge-Nájera, J., & Sáenz, R. (1988). Parturition in Onychophorans: New Record and a Review. Brenesia, 29, 15-20.

Morera-Brenes, B., & Monge-Nájera, J. (1990). Epiperipatus hilkae, n. sp. from Costa Rica (Onychophora: Peripatidae). Revista de Biología Tropical, 38(2B), 449-456.

Morera-Brenes, B., & Monge-Nájera, J. (2010). A new giant species of placented worm and the mechanism by which onychophorans weave their nets (Onychophora: Peripatidae). Revista de Biología Tropical, 58(4), 1127-1142.

Murienne, J., Daniels, S.R., Buckley, T.R., Mayer, G., & Giribet, G. (2014). A living fossil tale of Pangaean biogeography. Proceedings of the Royal Society of London B: Biological Sciences, 281(1775), 20132648.

Myburgh, A.M., & Daniels, S.R. (2015). Exploring the impact of habitat size on phylogeographic patterning in the Overberg velvet worm Peripatopsis overbergiensis (Onychophora: Peripatopsidae). Journal of Heredity, 106(3), 296-305.

Oliveira, I.D.S., & Wieloch, A.H. (2005). Macroperipatus machadoi sp. n. (Onychophora: Peripatidae) da floresta atlântica de Minas Gerais, Brasil. Lundiana, 6(supplement), 61-66.

Oliveira, I.S, Wieloch, A.H., & Mayer, G. (2010). Revised taxonomy and redescription of two species of the Peripatidae (Onychophora) from Brazil: a step towards consistent terminology of morphological characters. Zootaxa, 2493, 16-34.

Oliveira, I.S., Lacorte, G.A., Fonseca, C.G., Wieloch, A.H., & Mayer, G. (2011). Cryptic speciation in Brazilian Epiperipatus (Onychophora: Peripatidae) reveals an underestimated diversity among the peripatid velvet worms. Plos One, 6(6), e19973.

Oliveira, I.S., Franke, F.A., Hering, L., Schaffer, S., Rowell, D.M., Weck-Heimann, A., … Mayer, G. (2012a). Unexplored character diversity in Onychophora (velvet worms): a comparative study of three peripatid species. PloS One, 7(12), e51220.

Oliveira, I.S., Read, V.S.J., & Mayer, G. (2012b). A world checklist of Onychophora (velvet worms), with notes on nomenclature and status of names. ZooKeys, 211, 1-70.

Oliveira, I.S., Schaffer, S., Kvartalnov, P.V., Galoyan, E.A., Plako, I.V., Weck-Heimann, A., Geissler, P., Ruhberg, H., & Mayer, G. (2013). A new species of Eoperipatus (Onychophora) from Vietnam reveals novel morphological characters for the South-East Asian Peripatidae. Zoologischer Anzeiger-A Journal of Comparative Zoology, 252(4), 495-510.

Oliveira, I.S., Lacorte, G.A., Weck-Heimann, A., Cordeiro, L.M., Wieloch, A.H., & Mayer, G. (2014). A new and critically endangered species and genus of Onychophora (Peripatidae) from the Brazilian savannah–a vulnerable biodiversity hotspot. Systematics and Biodiversity, 13(3), 211-233.

Oliveira, I.S., Bai, M., Jahn, H., Gross, V., Martin, C., Hammel, J.U., … Mayer, G. (2016). Earliest onychophoran in amber reveals Gondwanan migration patterns. Current Biology, 26(19), 2594-2601.

Oliveira, I.S., Ruhberg, H., Rowell, D.M., & Mayer, G. (2018). Revision of Tasmanian viviparous velvet worms (Onychophora: Peripatopsidae) with descriptions of two new species. Invertebrate Systematics, 32(4), 909-932.

Peck, S.B. (1975). A Review of the New World Onychophora with the Description of a New Cavernicolous Genus and Species from Jamaica. Psyche: A Journal of Entomology, 82(3-4), 341-358.

Picado, C. (1911). Sur un habitat nouveau des Peripatus. Bulletin du Musée National d’Histoire Naturelle, Paris, 17, 415-416.

Podsiadlowski, L., Braband, A., & Mayer, G. (2008). The complete mitochondrial genome of the onychophoran Epiperipatus biolleyi reveals a unique transfer RNA set and provides further support for the Ecdysozoa hypothesis. Molecular Biology and Evolution, 25(1), 42-51.

Posada, D. (2008). jModelTest: phylogenetic model averaging. Molecular Biology and Evolution, 25(7), 1253-1256.

Rambaut, A., Drummond, A.J., Xie, D., Baele, G., & Suchard, M.A. (2018). Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology, 67(5), 901-904.

Read, V.S.J. (1985). The ecology of Macroperipatus torquatus (Kennel) with special reference to feeding and a taxonomic review (Doctoral dissertation). University of Wales, United Kingdom.

Read, V.S.J. (1988a). The application of scanning electron microscopy to the systematics of the neotropical Peripatidae (Onychophora). Zoological Journal of the Linnean Society, 93(3), 187-223.

Read, V.S.J. (1988b). The Onychophora of Trinidad, Tobago and the Lesser Antilles. Zoological Journal of the Linnean Society, 93(3), 225-257.

Reinhard, J., & Rowell, D.M. (2005). Social behaviour in an Australian velvet worm, Euperipatoides rowelli (Onychophora: Peripatopsidae). Journal of Zoology, 267(1), 1-7.

Reid, A.L. (1996). Review of the Peripatopsidae (Onychophora) in Australia, with comments on peripatopsid relationships. Invertebrate Systematics, 10(4), 663-936.

Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D.L., Darling, A., Höhna, S., … 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.

Rota-Stabelli, O., Kayal, E., Gleeson, D., Daub, J., Boore, J.L., Telford, M.J., Pisani, D., Blaxter, M., & Lavrov, D.V. (2010). Ecdysozoan mitogenomics: evidence for a common origin of the legged invertebrates, the Panarthropoda. Genome Biology and Evolution, 2, 425-440.

Ruhberg, H. (1985). Die Peripatopsidae (Onychophora), Systematik, Ökologie, Chorologie und phylogenetische Aspekte. Zoologica, 137, 1-184.

Ruhberg, H., & Hamer, M.L. (2005). A new species of Opisthopatus Purcell, 1899 (Onychophora: Peripatopsidae) from KwaZulu-Natal, South Africa. Zootaxa, 1039(1), 27-38.

Ruhberg, H., & Daniels, S.R. (2013). Morphological assessment supports the recognition of four novel species in the widely distributed velvet worm Peripatopsis moseleyi sensu lato (Onychophora: Peripatopsidae). Invertebrate Systematics, 27(2), 131-145.

Sampaio-Costa, C., Chagas-Junior, A., & Baptista, R.L. (2009). Brazilian species of Onychophora with notes on their taxonomy and distribution. Zoologia, 26(3), 553-561.

Sampaio-Costa, C. (2016). Sistemática e análise filogenética de Epiperipatus Clark, 1913 baseada em dados moleculares e morfológicos (Onychophora: Peripatidae) (Doctoral dissertation). Universidade de São Paulo, Brasil.

Sampaio-Costa, C., Chagas-Junior, A., & Pinto-da-Rocha, R. (2018). Redescription of Epiperipatus edwardsii, and descriptions of five new species of Epiperipatus from Brazil (Onychophora: Peripatidae). Zoologia, 35, 1-15.

Sato, S., Buckman-Young, R.S., Harvey, M.S., & Giribet, G. (2018). Cryptic speciation in a biodiversity hotspot: multilocus molecular data reveal new velvet worm species from Western Australia (Onychophora: Peripatopsidae: Kumbadjena). Invertebrate Systematics, 32(6), 1249-1264.

Schmarda, L.K. (1871). I. Ordnung. Malacopoda Blainville. Onychophora. Grube. Zoologie, 1(2), 74-76.

Sedgwick, A. (1888). A monograph on the species and distribution of the genus Peripatus (Guilding). Quarterly Journal of Microscopical Science, 28, 431-493.

Trewick, S. (1998). Sympatric cryptic species in New Zealand Onychophora. Biological Journal of the Linnean Society, 63(3), 307-329.

Trewick, S.A. (1999). Molecular diversity of Dunedin Peripatus (Onychophora: Peripatopsidae). New Zealand Journal of Zoology, 26(4), 381-393.

Trewick, S.A. (2000). Mitochondrial DNA sequences support allozyme evidence for cryptic radiation of New Zealand Peripatoides (Onychophora). Molecular Ecology, 9(3), 269-281.

Vaidya, G., Lohman, D.J., & Meier, R. (2011). SequenceMatrix: concatenation software for the fast assembly of multigene datasets with character set and codon information. Cladistics, 27(2), 171-180.

Zilch, A. (1954). Onychophoren aus El Salvador. Senckenbergiana Biologica, 35, 147-150.

Zitani, N.M., Thorn, R.G., Hoyle, M., Schulz, J.M., Steipe, T., Ruiz, Y.B., Sarquis-Adamson, Y., & Wishart, A.E. (2018). An Onychophoran and Its Putative Lepidopteran Mimic in the Arboreal Bryosphere of an Ecuadorian Cloud Forest. American Entomologist, 64(2), 94-101.

Comments

Creative Commons License

This work is licensed under a Creative Commons Attribution 4.0 International License.

Copyright (c) 2020 José Pablo Barquero González

Downloads

Download data is not yet available.