Ray spider rush: Fast-tracking integrative taxonomy in Panama’s cloud forests

Keywords: Symphytognathoids, Neotropical Region, integrative taxonomy, DNA, Tantra gen. nov.

Abstract

Taxonomy, a pivotal scientific discipline, plays a crucial role in biodiversity assessments and conservation by defining and cataloging species and higher taxa. However, tropical regions, housing a significant portion of global biodiversity, offer challenges to traditional taxonomy, leaving a substantial part of this diversity unexplored due to limited resources. This study employs a combined approach of gross morphological sorting and DNA-based species delimitation to accelerate species identification and discovery in the orb weaving spider family Theridiosomatidae (ray spiders) within Panamanian cloud forests. Using this methodology, we navigate the taxonomic challenges posed by this species-rich family, with relatively uniform sexual organs in closely related species. Employing a semi-quantitative sampling protocol, we estimate species accumulation curves and non-parametric richness, and assess various biodiversity metrics of over 3333 specimens, resulting in an integrative taxonomic revision revealing 27 new species and a new genus. Three new species of Chthonos Coddington, 1986 are described: Chthonos dobo sp. nov. (♂♀), Chthonos kaibe sp. nov. (♂♀), Chthonos kwati sp. nov. (♂♀). Seven new species of Epeirotypus O. Pickard-Cambridge, 1894 are described: Epeirotypus bule sp. nov. (♀), Epeirotypus drune sp. nov. (♀), Epeirotypus jane sp. nov. (♀), Epeirotypus kote sp. nov. (♂♀), Epeirotypus kra sp. nov. (♂♀), Epeirotypus kwakwa sp. nov. (♂♀), Epeirotypus tain sp. nov. (♀). One new species of Naatlo Coddington, 1986 is described: Naatlo chi sp. nov. (♂♀). Two new species of Ogulnius O. Pickard-Cambridge, 1882 are described: Ogulnius zbodro sp. nov. (♂♀) and Ogulnius debonaja sp. nov. (♂♀). We describe Tantra gen. nov. based on male and female characters. Eight new species are described: Tantra bribri gen. et sp. nov. (♂♀), Tantra bugle gen. et sp. nov. (♂♀), Tantra embera gen. et sp. nov. (♂♀), Tantra kuna gen. et sp. nov. (♂♀), Tantra naso gen. et sp. nov. (♂♀), Tantra ngabe gen. et sp. nov. (♂♀), Tantra sichid gen. et sp. nov. (♀), and Tantra wounaan gen. et sp. nov. (♂♀). Tantra kullki (Dupérré & Tapia, 2017) comb. nov. is transferred from Theridiosoma O. Pickard-Cambridge, 1879. Six new species of Baalzebub Coddington, 1986 are described: Baalzebub absoguedi sp. nov. (♀), Baalzebub antomia sp. nov. (♂), Baalzebub innatuledi sp. nov. (♂♀), Baalzebub jaibana sp. nov. (♂♀), Baalzebub nele sp. nov. (♀), Baalzebub sukia sp. nov. (♂♀). The male of Baalzebub albonotatus (Petrunkevitch, 1930) and Theridiosoma goodnightorum Archer, 1953 are described for the first time. Redescriptions and illustrations of Epilineutes globosus (O. Pickard-Cambridge, 1896), Naatlo fauna (Simon, 1897), and Wendilgarda clara Keyserling, 1886 are provided. Notably, we find that gross morphology remains a reliable tool for rapid species sorting, while crude or genetic identification methods offer consistent estimates for alpha diversity. The prevalence of endemic species at mid and high elevations further underscores the importance of our findings.

References

Agnarsson I., Coddington J.A., & Kuntner M. 2013. Systematics: progress in the study of spider diversity and evolution. In: Penney D. (ed.) Spider Research in the 21st Century: Trends and Perspectives: 58–111. Siri Scientific Press, Rochdale, UK.

Altschul S., Madden T., Schäffer A., Zhang J., Zhang Z., Miller W. & Lipman D. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25 (17): 3389–3402. https://doi.org/10.1093/nar/25.17.3389

Álvarez-Padilla F., Galán-Sánchez M.A. & Salgueiro-Sepúlveda F.J. 2020. A protocol for online documentation of spider biodiversity inventories applied to a Mexican tropical wet forest (Araneae, Araneomorphae). Zootaxa 4722 (3): 241–269. https://doi.org/10.11646/zootaxa.4722.3.3

Archer A.F. 1953. Studies in the orbweaving spiders (Argiopidae). 3. American Museum Novitates 1622: 1–27.

Astrin J.J., Huber B.A., Misof B. & Klütsch C.F.C. 2006. Molecular taxonomy in pholcid spiders (Pholcidae, Araneae): evaluation of species identification methods using CO1 and 16S rRNA. Zoologica Scripta 35 (5): 441–457. https://doi.org/10.1111/j.1463-6409.2006.00239.x

Baert L. 2014. New spider species (Araneae) from the Galápagos Islands (Ecuador). Bulletin de la Société royale belge d’Entomologie/Bulletin van de Koninklijke Belgische Vereniging voor Entomologie 149: 263–271.

Ballarin F., Yamasaki T. & Su Y.C. 2021. A survey on poorly known rainforest litter-dwelling spiders of Orchid Island (Lanyu, Taiwan) with the description of a new species (Araneae: Linyphiidae, Tetrablemmidae, and Theridiosomatidae). Zootaxa 4927 (2): 197–208. https://doi.org/10.11646/zootaxa.4927.2.2

Balslev H. 1988. Distribution patterns of Ecuadorean plant species. Taxon 37: 567–577. https://doi.org/10.2307/1221100

Bond J.E., Godwin R.L., Colby J.D., Newton L.G., Zahnle X.J., Agnarsson I., Hamilton C.A. & Kuntner M. 2022. Improving taxonomic practices and enhancing its extensibility—An example from araneology. Diversity 14 (1): 5. https://doi.org/10.3390/d14010005

Britton T., Anderson C.L., Jacquet D., Lundqvist S. & Bremer K. 2007. Estimating divergence times in large phylogenetic trees. Systematic Biology 56: 741–752. https://doi.org/10.1080/10635150701613783

Burnham K.P. & Overton W.S. 1978. Estimation of the size of a closed population when capture probabilities vary among animals. Biometrika 65: 623–633. https://doi.org/10.2307/2335915

Burnham K.P. & Overton W.S. 1979. Robust estimation of population size when capture probabilities vary among animals. Ecology 60: 927–936. https://doi.org/10.2307/1936861

Cao X., Liu J., Chen J., Zheng G., Kuntner M. & Agnarsson I. 2016. Rapid dissemination of taxonomic discoveries based on DNA barcoding and morphology. Scientific Reports 6: 37066. https://doi.org/10.1038/srep37066

de Carvalho M.R., Bockmann F.A., Amorim D.S., de Vivo M., de Toledo-Piza M., Menezes N.A., de Figueiredo J.L., Castro R.M.C., Gill A.C., Mceachran J.D., Compagno L.J.V., Schelly R.C., Britz R., Lundberg J.G., Vari R.P. & Nelson G. 2005. Revisiting the taxonomic impediment. Science 307: 353–4. https://doi.org/10.1126/science.307.5708.353b

de Carvalho M.R., Bockmann F.A., Amorim D.S., Brandão C.R.F., de Vivo M., de Figueiredo J.L., Bristki H.A., de Pinna M.C.C., Menezes N.A., Maques F.P.L., Papavero N., Cancello E.M., Crisci J.V., Mceachran J.D., Schelly R.C., Lundberg J.G., Gill A.C., Britz R., Wheeler Q.D., Stiassny M.L., Parenti L.R., Page L.M., Wheeler W.C., Faivovich J., Vari R.P., Grande L., Humphries C.J., DeSalle R., Ebach M.C. & Nelson G.J. 2007. Taxonomic impediment or impediment to taxonomy? A commentary on systematics and the cybertaxonomic-automation paradigm. Evolutionary Biology 34: 140–143. https://doi.org/10.1007/s11692-007-9011-6

Castalanelli M.A., Teale R., Rix M.G., Kennington W.J. & Harvey M.S. 2014. Barcoding of mygalomorph spiders (Araneae: Mygalomorphae) in the Pilbara bioregion of Western Australia reveals a highly diverse biota. Invertebrate Systematics 28 (4): 375–385. https://doi.org/10.1071/IS13058

Chamberlin R.V. & Ivie W. 1944. Spiders of the Georgia region of North America. Bulletin of the University of Utah 35 (9): 1–267. https://doi.org/10.1093/aesa/38.2.167

Chao A. 1984. Non-parametric estimation of the number of classes in a population. Scandanavian Journal of Statistics 11: 265–270.

Chao A. 1987. Estimating the population size for capture-recapture data with unequal catchability. Biometrics 43: 783–791. https://doi.org/10.2307/2531532

Chao A., Chazdon R.L., Colwell R.K. & Shen T. 2005. Capítulo 7. Un nuevo método estadístico para la evaluación de la similitud en la composición de especies con datos de incidencia y abundancia. In: Halffter G., Soberón J., Koleff P. & Melic A. (eds) Sobre Diversidad Biológica: El significado de las diversidades alfa, beta y gamma. m3m: Monografías Tercer Milenio, 4, Sociedad Entomológica Aragonesa, Zaragoza, Spain.

Chazdon R.L., Colwell R.K., Denslow J.S. & Guariguata M.R. 1998. Statistical methods for estimating species richness of woody regeneration in primary and secondary rain forests of NE Costa Rica. In: Dallmeier F. & Comiskey J.A. (eds) Forest Biodiversity Research, Monitoring and Modeling: Conceptual Background and Old World Case Studies: 285–309. Parthenon Publishing, Paris.

Clement M., Posada D. & Crandall K.A. 2000. TCS: a computer program to estimate gene genealogies. Molecular Ecology 9: 1657–1659. https://doi.org/10.1046/j.1365-294x.2000.01020.x

Clerck C. 1757. Aranei Svecici. Svenska spindlar, uti sina hufvud-slågter indelte samt under några och sextio särskildte arter beskrefne och med illuminerade figurer uplyste. Laurentius Salvius, Stockholmiae [= Stockholm]. https://doi.org/10.5962/bhl.title.119890

Coddington J.A. 1986. The genera of the spider family Theridiosomatidae. Smithsonian Contribution to Zoology 422: 1–96. https://doi.org/10.5479/si.00810282.422

Coddington J.A. & Valerio C.G. 1980. Observations on the web and behavior of Wendilgarda spiders (Araneae: Theridiosomatidae). Psyche 87 (1–2): 93–105. https://doi.org/10.1155/1980/69153

Coddington J.A., Griswold C.E., Dávila D.S., Peñaranda E. & Larcher S.F. 1991. Designing and testing sampling protocols to estimate biodiversity in tropical ecosystems. In: Dudley E.C. (ed.) The Unity of Evolutionary Biology: Proceedings of the Fourth International Congress of Systematics and Evolutionary Biology: 44–60. Discorides Press, Portland, Oregon, USA.

Coddington J.A., Young L.H. & Coyle F.A. 1996. Estimating spider species richness in a southern Appalachian cove hardwood forest. The Journal of Arachnology 24: 111–128.

Coddington J.A., Agnarsson I., Miller J.A., Kunter M. & Hormiga G. 2009. Undersampling bias: the null hypothesis for singleton species in tropical arthropod surveys. Journal of Animal Ecology 78 (3): 573–584. https://doi.org/10.1111/j.1365-2656.2009.01525.x

Coddington J.A., Agnarsson I., Cheng R.C., Čandek K., Driskell A., Frick H., Gregorič M., Kostanjšek R., Kropf C., Kweskin M., Lokovšek T., Pipan M., Vidergar N. & Kuntner M. 2016. DNA barcode data accurately assign higher spider taxa. PeerJ 4: e2201. https://doi.org/10.7717/peerj.2201

Colwell R.K. 2004. EstimateS: statistical estimation of species richness and shared species from samples (software and user’s guide). Ver. 9.1. Available from https://www.robertkcolwell.org/pages/1407 [accessed 19 Mar. 2023].

Colwell R.K. & Coddington J.A. 1994. Estimating terrestrial biodiversity through extrapolation. Philosophical Transactions of the Royal Society of London B – Biological Sciences 345: 101–118. https://doi.org/10.1098/rstb.1994.0091

Colwell R.K., Mao C.X. & Chang J. 2005. Capítulo 6. Interpolando, extrapolando y comparando las curvas de acumulación de especies basadas en su incidencia. In: Halffter G., Soberón J., Koleff P. & Melic A. (eds) Sobre Diversidad Biológica: El significado de las diversidades alfa, beta y gamma. m3m: Monografías Tercer Milenio, 4, Sociedad Entomológica Aragonesa, Zaragoza, España.

Cotoras D.D., Suenaga M. & Mikheyev A.S. 2021. Intraspecific niche partition without speciation: individual level web polymorphism within a single island spider population. Proceedings of the Royal Society B – Biological Sciences 288: 20203138.20203138. http://doi.org/10.1098/rspb.2020.3138

Dayrat B. 2005. Towards integrative taxonomy. Biological Journal of the Linnean Society 85: 407–15. https://doi.org/10.1111/j.1095-8312.2005.00503.x

Deltshev C. 2000. The endemic spiders (Araneae) of the Balkan Peninsula. Ekológia (Bratislava) 19 (3): 59–65.

Dupérré N. & Tapia E. 2017. On some minuscule spiders (Araneae: Theridiosomatidae, Symphytognathidae) from the Chocó region of Ecuador with the description of ten new species. Zootaxa 4341 (3): 375–399. https://doi.org/10.11646/zootaxa.4341.3.3

Ezard T., Fujisawa T. & Barraclough T. 2009. ‘Splits: SPecies’ limits by threshold statistics. R Package Ver. 1.0. Available from http://r-forge.r-project.org/projects/splits [accessed 19 Mar. 2023].

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 Biotechnology 3 (5): 294–299.

Fontaine B., Perrard A. & Bouchet P. 2012. 21 years of shelf life between discovery and description of new species. Current Biology 22 (22): R943–R944. https://doi.org/10.1016/j.cub.2012.10.029

Fujisawa T. & Barraclough T.G. 2013. Delimiting species using single-locus data and the generalized mixed Yule coalescent approach: a revised method and evaluation on simulated data sets. Systematic Biology 62 (5): 707–724. https://doi.org/10.1093/sysbio/syt033

Godfray H.C.J. 2002. Challenges for taxonomy. Nature 417 (6884): 17–19. https://doi.org/10.1038/417017a

Godfray H.C.J. 2007. Linnaeus in the information age. Nature 446 (7133): 259–260. https://doi.org/10.1038/446259a

Godfray H.C.J., Mayo S.J. & Scoble M.J. 2008. Pragmatism and rigour can coexist in taxonomy. Evolutionary Biology 35: 309–311. https://doi.org/10.1007/s11692-008-9041-8

Guevara J. & Avilés L. 2009. Elevational changes in the composition of insects and other terrestrial arthropods at tropical latitudes: a comparison of multiple sampling methods and social spider diets. Insect Conservation and Diversity 2: 142–152. https://doi.org/10.1111/j.1752-4598.2008.00043.x

Hall T.A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Serie 41: 95–98.

Hebert P.D.N., Cywinska A., Ball S.L. & deWaard J.R. 2003a. Biological identification through DNA barcodes. Proceedings of the Royal Society of London B – Biological Sciences 270: 313–321. https://doi.org/10.1098/rspb.2002.2218

Hebert P.D.N., Ratnasingham S. & deWaard J.R. 2003b. Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society of London B – Biological Sciences 270 (Supplement 1): S96–9. https://doi.org/10.1098/rsbl.2003.0025

Hebert P.D.N., Penton E.H., Burns J.M., Janzen D.H. & Hallwachs W. 2004. Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. PNAS 101 (41): 14812–14817. https://doi.org/10.1073/pnas.0406166101

Hickman V.V. 1931. A new family of spiders. Proceedings of the Zoological Society of London (B) 101 (4): 1321–1328. https://doi.org/10.1111/j.1096-3642.1931.tb01063.x

Ivanova N.V. & Grainger C.M. 2007. CCDB Protocols, COI Amplification. Available from https://ccdb.ca/site/wp-content/uploads/2016/09/CCDB_Amplification.pdf [accessed 19 Mar. 2023].

Ivanova N.V., deWaard J. & Hebert P.D.N. 2006. An inexpensive, automation-friendly protocol for recovering high-quality DNA. Molecular Ecology Notes 6: 998–1002. https://doi.org/10.1111/j.1471-8286.2006.01428.x

Janzen D.H., Hallwachs W., Blandin P., Burns J.M., Cadiou J.M., Chacon I., Dapkey T., Deans A.R., Epstein M.E., Espinoza B., Franclemont J.G., Haber W.A., Hajibabaei M., Hall J.P.W., Hebert P.D.N., Gauld I.D., Harvey D.J., Hausmann A., Kitching I.J., Lafontaine D., Landry J., Lemaire C., Miller J.Y., Miller J.S., Miller L., Miller S.E., Montero J., Munroe E., Green S.R., Ratnasingham S., Rawlins J.E., Robbins R.K., Rodriguez J.J., Rougerie R., Sharkey M.J., Smith M.A., Solis M.A., Sullivan J.B., Thiaucourt P., Wahl D.B., Weller S.J., Whitfield J.B., Willmott K.R., Wood D.M., Woodley N.E. & Wilson J.J. 2009. Integration of DNA barcoding into an ongoing inventory of complex tropical biodiversity. Molecular Ecology Resources 9: 1–26. https://doi.org/10.1111/j.1755-0998.2009.02628.x

Keyserling E. 1886. Die Spinnen Amerikas. Theridiidae. Verlag von Bauer & Raspe (E. Küster), Nürnberg. https://doi.org/10.5962/bhl.title.64832

Khmelik V.V., Kozub D. & Glazunov A. 2006. Helicon Focus. Ver. 3.10.3. and 4.01. Available from https://www.heliconsoft.com/heliconsoft-products/helicon-focus/ [accessed 19 Mar. 2023].

Koch L. 1877. Verzeichniss der bei Nürnberg bis jetzt beobachteten Arachniden (mit Ausschluss der Ixodiden und Acariden) und Beschreibungen von neuen, hier vorkommenden Arten. Abhandlungen der Naturhistorischen Gesellschaft zu Nürnberg 6: 113–198.

Kulkarni S., Wood H., Lloyd M. & Hormiga G. 2020. Spider-specific probe set for ultraconserved elements offers new perspectives on the evolutionary history of spiders (Arachnida, Araneae). Molecular Ecology Resources 20 (1): 185–203. https://doi.org/10.1111/1755-0998.13099

Kulkarni S., Wood H.M. & Hormiga G. 2023. Phylogenomics illuminates the evolution of orb webs, respiratory systems and the biogeographic history of the world’s smallest orb-weaving spiders (Araneae, Araneoidea, Symphytognathoids). Molecular Phylogenetics and Evolution 186: e107855. https://doi.org/10.1016/j.ympev.2023.107855

Labarque F.M. & Griswold C.E. 2014. New ray spiders from Southeast Asia: The new Philippine genus Tagalogonia gen. nov. and continental genus Coddingtonia Miller, Griswold & Yin, 2009 (Araneae: Theridiosomatidae), with comments on their intergeneric relationships. In: William C. & Gosliner T. (eds) The Coral Triangle: The 2011 Hearts Philippine Biodiversity Expedition: 407–426. California Academy of Sciences, San Francisco, California.

Lamarck J.B.P.A. 1801. Système des animaux sans vertèbres. Paris, l’auteur. https://doi.org/10.5962/bhl.title.14255

Librado P. & Rozas J. 2009. DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451–1452. https://doi.org/10.1093/bioinformatics/btp187

Lopardo L. & Hormiga G. 2015. Out of the twilight zone: phylogeny and evolutionary morphology of the orb-weaving spider family Mysmenidae, with a focus on spinneret spigot morphology in symphytognathoids (Araneae, Araneoidea). Zoological Journal of the Linnean Society 173: 527–786. https://doi.org/10.1111/zoj.12199

Lopardo L. & Uhl G. 2014. Testing mitochondrial marker efficacy for DNA barcoding in spiders: a test case using the dwarf spider genus Oedothorax (Araneae : Linyphiidae : Erigoninae). Invertebrate Systematics 28: 501–521. https://doi.org/10.1071/IS14017

Lopardo L., Giribet G. & Hormiga G. 2010. Morphology to the rescue: molecular data and the signal of morphological characters in combined phylogenetic analyses—a case study on mysmenid spiders (Araneae, Mysmenidae), with comments on the evolution of web architecture. Cladistics 27: 278–330. https://doi.org/10.1111/j.1096-0031.2010.00332.x

Lopez A. & Emerit M. 1986. Wendilgarda mustelina arnouxi n. ssp et la glande labio-sternale des Theridiosomatidae (Araneae). Mémoires de Biospéologie 12: 67–76.

Meier R., Blaimer B.B., Buenaventura E., Hartop E., Srivathsan A. & Yeo D. 2021. A re-analysis of the data in Sharkey et al.’s (2021) minimalist revision reveals that BINs do not deserve names, but BOLD Systems needs a stronger commitment to open science. Cladistics 38 (2): 264–275. https://doi.org/10.1111/cla.12489

Messing J. 1983. [2] New M13 vectors for cloning. Methods in Enzymology 101: 20–78. https://doi.org/10.1016/0076-6879(83)01005-8

Miller J.A., Griswold C.E. & Yin C.M. 2009. The symphytognathoid spiders of the Gaoligongshan, Yunnan, China (Araneae, Araneoidea): Systematics and diversity of micro-orbweavers. ZooKeys 11: 9–195. https://doi.org/10.3897/zookeys.11.160

Miller J.A., Miller J.H., Pham D.S. & Beentjes K.K. 2014. Cyberdiversity: improving the informatic value of diverse tropical arthropod inventories. PLoS One 9 (12): e115750. https://doi.org/10.1371/journal.pone.0115750

Miller M.A., Pfeiffer W. & Schwartz T. 2010. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: IEEE Proceedings of the Gateway Computing Environments Workshop (GCE): 1–8. New Orleans, LA. https://doi.org/10.1109/GCE.2010.5676129

Monaghan M.T., Wild R., Elliot M., Fujisawa T., Balke M., Inward D.J.G., Lees D.C., Ranaivosolo R., Eggleton P., Barraclough T.G. & Vogler A.P. 2009. Accelerated species inventory on Madagascar using coalescent-based models of species delineation. Systematic Biology 58 (3): 298–311. https://doi.org/10.1093/sysbio/syp027

Myers N., Mittermeier R.A., Mittermeier C.G., da Fonseca G.A.B. & Kent J. 2000. Biodiversity hotspots for conservation priorities. Nature 403: 853–858. https://doi.org/10.1038/35002501

Nogueira A., Pinto-da-Rocha R. & Brescovit A. 2006. Comunidade de aranhas orbitelas (Arachnida, Araneae) na região da Reserva Florestal do Morro Grande, Cotia, São Paulo, Brasil. Biota Neotropica 6: 1–24.

Oh J.H., Kim S. & Lee S. 2022. DNA barcodes reveal population-dependent cryptic diversity and various cases of sympatry of Korean leptonetid spiders (Araneae: Leptonetidae). Scientific Reports 12 (1): 1–16. https://doi.org/10.1038/s41598-022-18666-y

Oliver I. & Beattie A.J. 1996. Invertebrate morphospecies as surrogates for species: A case study. Conservation Biology 10 (1): 99–109. https://doi.org/10.1046/j.1523-1739.1996.10010099.x

Olson D.M. 1994. The distribution of leaf litter invertebrates along a Neotropical altitudinal gradient. Journal of Tropical Ecology 10 (2): 129–150. https://doi.org/10.1017/S0266467400007793

Padial J., Castroviejo-Fisher S., Kohler J., Vila C., Chaparro J. & De la Riva I. 2009. Deciphering the products of evolution at the species level: the need for an integrative taxonomy. Zoologica Scripta 38: 431–447. https://doi.org/10.1111/j.1463-6409.2008.00381.x

Paradis E., Claude J. & Strimmer K. 2004. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20: 289–290. https://doi.org/10.1093/bioinformatics/btg412

Petrunkevitch, A. 1928. Systema Aranearum. Transactions of the Connecticut Academy of Arts and Sciences 29: 1–270.

Petrunkevitch A. 1930. The spiders of Porto Rico. Part two. Transactions of the Connecticut Academy of Arts and Sciences 30: 159–356.

Pickard-Cambridge F.O.1902. Arachnida - Araneida and Opiliones. Biologia Centrali-Americana, Zoology, London 2: 313–424.

Pickard-Cambridge O. 1879. On some new and rare British spiders, with characters of a new genus. Annals and Magazine of Natural History (5) 4 (21): 190–215. https://doi.org/10.1080/00222937908679818

Pickard-Cambridge O. 1882. On new genera and species of Araneidea. Proceedings of the Zoological Society of London 50 (3): 423–442. https://doi.org/10.1111/j.1096-3642.1882.tb02749.x

Pickard-Cambridge O. 1894. Arachnida. Araneida. Biologia Centrali-Americana, Zoology, London 1: 121–144.

Pickard-Cambridge O. 1896. Arachnida. Araneida. Biologia Centrali-Americana, Zoology, London 1: 161–224.

Planas E., Fernández-Montraveta C. & Ribera C. 2013. Molecular systematics of the wolf spider genus Lycosa (Araneae: Lycosidae) in the Western Mediterranean Basin. Molecular Phylogenetics and Evolution 67 (2): 414–428. https://doi.org/10.1016/j.ympev.2013.02.006

Pons J., Barraclough T.G., Gomez-Zurita J., Cardoso A., Duran D.P., Hazell S., Kamoun S., Sumlin W.D. & Vogler A.P. 2006. Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Systematic Biology 55: 595–609. https://doi.org/10.1080/10635150600852011

Posada D. 2004. Collapse: Describing Haplotypes from Sequence Alignments. Ver. 1.2. University of Vigo, Vigo, Spain. Available from https://www.softpedia.com/get/Science-CAD/Collapse.shtml [accessed 19 Mar. 2023].

Powell J.R., Monaghan M.T., Öpik M. & Rillig M.C. 2011. Evolutionary criteria outperform operational approaches in producing ecologically relevant fungal species inventories. Molecular Ecology 20 (3): 655–666. https://doi.org/10.1111/j.1365-294X.2010.04964.x

Rambaut A. 2006–2014. Tree Figure Drawing Tool. Ver. 1.4. Institute of Evolutionary Biology, University of Edinburgh. Available from http://tree.bio.ed.ac.uk/ [accessed 19 Mar. 2023].

Ratnasingham S. & Hebert P.D.N. 2007. BOLD: The Barcode of Life Data System (www.barcodinglife.org). Molecular Ecology Notes 7: 355–364. https://doi.org/10.1111/j.1471-8286.2007.01678.x

Ricetti J. & Bonaldo A. 2008. Diversidade e estimativas de riqueza de aranhas em quatro fitofisionomias na Serra do Cachimbo, Pará, Brasil. Iheringia, Série Zoologia 98: 88–99. https://doi.org/10.1590/S0073-47212008000100013

Rivera-Quiroz F.A. & Álvarez-Padilla F. 2023. Integration or minimalism: twenty-one new species of ghost spiders (Anyphaenidae: Anyphaena) from Mexico. European Journal of Taxonomy 865: 1–94. https://doi.org/10.5852/ejt.2023.865.2097

Rodrigues E.N.L. & Ott R. 2005. Nova espécie de Theridiosoma (Araneae, Theridiosomatidae) do sul do Brasil. Iheringia, Série Zoologia, Porto Alegre 95 (1): 79–81. https://doi.org/10.1590/S0073-47212005000100011

Saaristo M.I. 1996. Theridiosomatid spiders of the granitic islands of Seychelles (Araneae, Theridiosomatidae). Phelsuma 4: 48–52.

Saaristo M.I. 2010. Araneae. In: Gerlach J. & Marusik Y.M. (eds) Arachnida and Myriapoda of the Seychelles Islands: 8–306. Siri Scientific Press, Manchester.

Sanger F., Nicklen S. & Coulson A.R. 1977. DNA sequencing with chain-terminating inhibitors. PNAS 74 (12): 5463–5467. https://doi.org/10.1073/pnas.74.12.5463

Scharff N., Coddington J.A., Griswold C.E., Hormiga G. & De Place Bjorn P. 2003. When to quit? Estimating spider species richness in a northern European deciduous forest. Journal of Arachnology 31: 246–273. https://doi.org/10.1636/0161-8202(2003)031[0246:WTQESS]2.0.CO;2

Sharkey M.J., Janzen D.H., Hallwachs W., Chapman E.G., Smith M.A., Dapkey T., Brown A., Ratnasingham S., Naik S., Manjunath R., Perez K., Milton M., Hebert P., Shaw S.R., Kittel R.N., Solis M.A., Metz M.A., Goldstein P.Z., Brown J.W., Quicke D.L.J., Achterberg C.V., Brown B.V. & Burns J.M. 2021. Minimalist revision and description of 403 new species in 11 subfamilies of Costa Rican braconid parasitoid wasps, including host records for 219 species. ZooKeys 1013: 1–665. https://doi.org/10.3897/zookeys.1013.55600

Simon E. 1881. Les arachnides de France. Tome cinquième, première partie. Roret, Paris.

Simon E. 1895. Histoire naturelle des araignées. Deuxième édition, tome premier. Roret, Paris, 761–1084. https://doi.org/10.5962/bhl.title.51973

Simon E. 1897. Études arachnologiques. 27e Mémoire. XLII. Descriptions d’espèces nouvelles de l’ordre des Araneae. Annales de la Société entomologique de France 65: 465–510.

Simon E. 1898. On the spiders of the island of St Vincent. Part III. Proceedings of the Zoological Society of London 65 (4): 860–890. https://doi.org/10.1111/j.1096-3642.1898.tb01390.x

Sørensen L.L., Coddington J.A. & Scharff N. 2002. Inventorying and estimating subcanopy spider diversity using semiquantitative sampling methods in an Afromontane forest. Environmental Entomology 31: 319–330. https://doi.org/10.1603/0046-225X-31.2.319

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

Stamatakis A. 2014. RAxML Version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30 (9): 1312–1313. https://doi.org/10.1093/bioinformatics/btu033

Stamatakis A., Hoover P. & Rougemont J. 2008. A rapid bootstrap algorithm for the RAxML web-servers. Systematic Biology 57 (5): 758–771. https://doi.org/10.1080/10635150802429642

Stevens G.C. 1989. The latitudinal gradient in geographical range: how so many species coexist in the tropics. American Naturalist 133: 240–256. https://doi.org/10.1086/284913

Suzuki Y., Serita R. & Hiramatsu T. 2020. Japanese spiders of the genus Theridiosoma (Araneae: Theridiosomatidae) with the description of four new species. Acta Arachnologica 69 (2): 133–150. https://doi.org/10.2476/asjaa.69.133

Suzuki Y., Hiramatsu T. & Tatsuta H. 2022. Two new species and a new genus of ray spiders (Araneae, Theridiosomatidae) from the Ryukyu Islands, southwest Japan, with notes on their natural history. ZooKeys 1109: 76–101. https://doi.org/10.3897/zookeys.1109.83807

Talavera G., Dincă V. & Vila R. 2013. Factors affecting species delimitations with the GMYC model: insights from a butterfly survey. Methods in Ecology and Evolution 4 (12): 1101–1110. https://doi.org/10.1111/2041-210X.12107

Taylor R.W. 1983. Descriptive taxonomy: past, present, and future. In: Highley E. & Taylor R.W. (eds) Australian Systematic Entomology: A Bicentenary Perspective: 93–134. CSIRO, Melbourne.

Van der Werff H. & Consiglio T. 2004. Distribution and conservation significance of endemic species of flowering plants in Peru. Biodiversity and Conservation 13: 1699–1713. https://doi.org/10.1023/B:BIOC.0000029334.69717.f0

Víquez C. 2020. Aracnofauna (Arachnida) de la Isla del Coco, Costa Rica, con la descripción de tres nuevas especies. Revista de Biología Tropical 68 (1): S115–S143. https://doi.org/10.15517/rbt.v68iS1.41174

Wang Q., Li S., Wang R. & Paquin P. 2008. Phylogeographic analysis of Pimoidae (Arachnida: Araneae) inferred from mitochondrial cytochrome c oxidase subunit I and nuclear 28S rRNA gene regions. Journal of Zoological Systematics and Evolutionary Research 46 (2): 96–104. https://doi.org/10.1111/j.1439-0469.2007.00441.x

Wheeler Q.D. 2004. Taxonomic triage and the poverty of phylogeny. Philosophical Transactions of the Royal Society B – Biological Sciences 359: 571–583. https://doi.org/10.1098/rstb.2003.1452

Wheeler Q.D. 2008. The New Taxonomy. CRC Press, Boca Raton, Florida.

Wheeler Q.D. 2023. Species, Science and Society: The Role of Systematic Biology. Taylor & Francis.

Whittaker R.H. 1952. A study of summer foliage insect communities in the Great Smoky Mountains. Ecological Monographs 22: 1–44. https://doi.org/10.2307/1948527

Wienskoski E. 2010. The genus Naatlo (Araneae: Theridiosomatidae): distribution and taxonomic history. Revista Brasileira de Biociências 8 (2): 131–138.

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

World Spider Catalog 2025. World spider catalog. Ver. 26. Natural History Museum Bern. Available from http://wsc.nmbe.ch [accessed on 23 Mar. 2025].

Zhang J.S., Yu H. & Lin Y.C. 2023. Simonia gen. nov., a new spider genus (Araneae, Theridiosomatidae) from Southeast Asia. ZooKeys 1185: 277–294. https://doi.org/10.3897/zookeys.1185.104120

Zhao Q.Y. & Li S.Q. 2012. Eleven new species of theridiosomatid spiders from southern China (Araneae, Theridiosomatidae). ZooKeys 255: 1–48. https://doi.org/10.3897/zookeys.255.3272

Published
2025-08-22
How to Cite
Labarque, F. M., Piacentini, L. N., Pons, J., Hormiga, G., Arnedo, M. A., & Ramírez, M. J. (2025). Ray spider rush: Fast-tracking integrative taxonomy in Panama’s cloud forests. European Journal of Taxonomy, 1010(1), 1-145. https://doi.org/10.5852/ejt.2025.1010.3021
Section
Monograph