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The geographic distribution of Costa Rican velvet worms (Onychophora: Peripatidae) José Pablo Barquero-González1, Adrián Alonso Cabrera Alvarado2, Stephanie Valle-Cubero1, Julián Monge-Nájera3 & Bernal Morera-Brenes1 1. Laboratorio de Sistemática, Genética y Evolución (LabSGE), Escuela de Ciencias Biológicas, Universidad Nacional, Heredia, Costa Rica; [email protected], [email protected], [email protected] 2. Universidad Latina, San José, Costa Rica; [email protected] 3. Laboratorio de Ecología Urbana, Universidad Estatal a Distancia (UNED), 2050 San José, Costa Rica; [email protected] Received 25-VI-2015. Corrected 23-V-2016. Accepted 28-VI-2016. Abstract: Velvet worms, “peripatus” or onychophorans, are “living fossils” that were geographically wide- spread in Cambrian seas but now occur exclusively on terrestrial habitats. The only extant species studied in some detail are those from Costa Rica, but their real geographic distribution was in urgent need of revision. To solve this problem we visited the localities mentioned in all the original taxonomic descriptions and redescrip- tions. These visits covered a 25 year period (1988-2014) and included interviews with local residents. We also examined all Costa Rican collections, and checked the information in old maps and books. Here we critically review geographic data, correct errors, assign neotype localities, report on the survival of populations after heavy volcanic eruptions or urbanization, and present the correct geographical distribution for the seven currently described Costa Rican species. Rev. Biol. Trop. 64 (4): 1401-1414. Epub 2016 December 01. Key words: taxonomy, localities, correction of records. Velvet worms, also known as “peripa- and the production of a hunting adhesive net tus”, or onychophorans, are “living fossils” that is self-assembled in a fraction of a second that have been documented as fossils since (Bouvier, 1905; Morera-Brenes & Monge- their Cambrian origin in China and Canada Nájera, 2010; Concha, Mellado, Morera- (Monge-Nájera & Hou, 1999). The phylum Brenes, Costa, Mahadevan, & Monge-Nájera, Onychophora unites the primitive features of 2015). Despite their extraordinary biology and “worms,” such as Nematoda and Nematomor- their uncertain location in the phylogeny of pha, with those of the arthropods (Grimaldi & life (e.g. Podsiadlowski, Braband, & Mayer, Engel, 2005). Modern velvet worms are classi- 2008; Rota-Stabelli et al., 2010) little is known fied in two families, Peripatidae and Peripatop- about them, probably because they have low sidae. The early diversification of these groups population densities, with the exception of pre-dates the break-up of Pangaea, maintaining some areas in New Zealand. In the rainforests regionalization even in landmasses that have of tropical and temperate zones, they live under remained contiguous throughout the history of rotten trees, stones, moss, leaf litter, rotting the Onychophora (Murienne, Daniels, Buckley, wood, crevices in the soil and ant and termite Mayer, & Giribet, 2014). tunnels (Grimaldi & Engel, 2005). Their rarity Their extraordinary biology includes the is the main cause most biologists never see only true placenta known from an invertebrate, them alive. For most of the approximately 200 Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 64 (4): 1401-1414, December 2016 1401 known species, there is no information whatso- reported locality (San José province: cantón ever about their ecology, physiology, behavior, of San José, cantón of Moravia, cantón of embryology or other aspects. Vázquez de Coronado, cantón of Goicoechea; Research work has focused mainly on spe- Puntarenas province: cantón of Parrita; Guana- cies that inhabit the small Central American caste province: cantón of Nicoya; Limón Prov- country of Costa Rica (Morera-Brenes, 2012). ince: cantón of Siquirres, cantón of Limón), Nevertheless, the knowledge of Costa Rican we searched manually under stones, inside and species is preliminary, fragmentary and troubled under fallen trees, partially decomposed trunks, by outdated taxonomy and serious doubts about as well as under moss covering the ground and the true geographic distribution of each species. trees. Every visit day, at least two of us searched The first described onychophorans from Costa for half a day or more, and as a result collected Rica were collected in the Nineteenth Century a little less than 200 specimens in total. around San José, capital of the country, by the In every locality we also asked verbally Alsacian naturalist Paul Biolley. At that time, to the local residents about their knowledge, “around San José” could be just a few blocks including name, folkloric beliefs and any other away from the current center of the city (Hilje, information that they might have. Addition- 2013, p. 477). The currently known species ally, we examined all specimens in all Costa are Epiperipatus isthmicola (Bouvier 1902a); Rican collections: INBio (Instituto Nacional de Epiperipatus biolleyi (Bouvier 1902b); Peripa- Biodiversidad), UNA (Universidad Nacional; tus ruber Fuhrmann (1913); Macroperipatus both in Heredia Province) and UCR (Uni- valerioi Morera-Brenes & León (1986); Epipe- versidad de Costa Rica; San José Province). ripatus hilkae Morera-Brenes & Monge-Nájera We checked the information in old maps and (1990); Peripatus solorzanoi Morera-Brenes books in the libraries of UNA and UCR, as & Monge-Nájera (2010) and Principapillatus well as online information through Google. hitoyensis Oliveira, et al. (2012a). Recent work com, and consulted an expert in the history of (Oliveira, Read, & Mayer, 2012b) concluded Costa Rican science (Jaime García, UCR), a that the real geographic distribution of Costa professional field collector (Francisco Morales, Rican species needed urgent revision. In this INBio) and a field zoologist who knows both article we provide that revision and correct the animals and the historic locations (Bernal several taxonomic and biogeographic errors Rodríguez, UCR). that were undetected in the scientific literature for more than a century. RESULTS MATERIALS AND METHODS The following revision of all onychopho- rans described from Costa Rica (Fig. 1) is To review the collecting localities of all organized chronologically and includes syn- described Costa Rican velvet worms we vis- onyms, type information, language of original ited in eight field trips (September 1988, July description, and English translation of the most 1991, September 1996, October 2004, June important characteristics (until now, research 2009, November 2010, October 2012, Novem- has been hindered by the use of several lan- ber 2014) the areas mentioned in the original guages in the older literature about this group). taxonomic descriptions as well as in rede- We have summarized our revision of all Costa scriptions. These visits cover a 25 year period Rican species in Fig. 2 and Fig. 4. Both support (1988-2014). our statement that Bouvier’s (1902a, 1902b) Following the standard procedure for ony- original descriptions differ from his later work chophorans (e.g. Bouvier, 1905), in every (Bouvier, 1907a): 1402 Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 64 (4): 1401-1414, December 2016 Fig. 1. Graphic catalogue of all described species of Costa Rican Onychophora. A. P. solorzanoi, photograph by Alejandro Solórzano; B. E. isthmicola, by Adrián Cabrera, C. P. ruber, by Bernal Morera-Brenes, D. E. hilkae, by Hilke Ruhberg; E. P. hitoyensis, by Georg Mayer, F. E.biolleyi, by Bernal Morera-Brenes; and G. M. cf. valerioi, by José Barquero-González. Epiperipatus isthmicola (Bouvier, 1902) Described type locality: COSTA RICA, “near [the city of] San José, around 1 100 m Synonyms: Peripatus nicaraguensis var. above sea level”. July 1900, P. Biolley col. isthmicola, by original designation (Bouvier, (Bouvier 1902a). 1902a: 240); Peripatus (Epiperipatus) isthmi- cola (Clark, 1913: 18); Epiperipatus isthmicola Neotype locality: COSTA RICA, San José (Stewart B, P., 1900: 345). Province, cantón of San José, distrito Hospital, Barrio Cristo Rey, formerly Premontane Moist Holotype: The holotype was not clear- Forest in Holdridge’s (1978) system, 9° 55’ ly designated in the original description 29.90”N - 84° 5’5.03” W, 1 143 m.a.s.l., 27 (see Remarks). May 2012, col. A.A. Cabrera Alvarado. Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 64 (4): 1401-1414, December 2016 1403 Outer Blade Inner Blade Urinary papillae Language of species description: French. E. nicaraguensis (holotype), Matagalpa, female Relevant taxonomic characteristics in the holotype description: “female color black- 1/1/0 1/1/0/11 berry [original French: mûre] [decolored in alcohol], of a smaller size, it comes from Costa Rica, where it was captured some two years E. isthmicola (holotype), San José, female ago. The dorsal flank of this specimen has a “remind from all points the jaws of the “similar to the type species” latter species” [E. nicaraguensis] [E. nicaraguensis] perfectly uniform dye, and the rudiments of a [1/1/0 ?] [1/1/0/11] darker axial line are barely distinguishable in E. isthmicola ?, Cachí, Cartago, female some places; the ventral flank is a little paler, lightly washed by a yellowish rose; the anten- nas are blackish with the antennal tip almost ? 1/1/0 1/2/0/10-12 black. The back is very regularly convex, and the body attenuates a lot more towards the back than towards the front; the length is 20 mm, It is unclear whether this E. isthmicola ?, Santa Clara, Siquirres
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    Steinmetz et al. EvoDevo 2010, 1:14 http://www.evodevojournal.com/content/1/1/14 RESEARCH Open Access Six3 demarcates the anterior-most developing brain region in bilaterian animals Patrick RH Steinmetz1,6†, Rolf Urbach2†, Nico Posnien3,7, Joakim Eriksson4,8, Roman P Kostyuchenko5, Carlo Brena4, Keren Guy1, Michael Akam4*, Gregor Bucher3*, Detlev Arendt1* Abstract Background: The heads of annelids (earthworms, polychaetes, and others) and arthropods (insects, myriapods, spiders, and others) and the arthropod-related onychophorans (velvet worms) show similar brain architecture and for this reason have long been considered homologous. However, this view is challenged by the ‘new phylogeny’ placing arthropods and annelids into distinct superphyla, Ecdysozoa and Lophotrochozoa, together with many other phyla lacking elaborate heads or brains. To compare the organisation of annelid and arthropod heads and brains at the molecular level, we investigated head regionalisation genes in various groups. Regionalisation genes subdivide developing animals into molecular regions and can be used to align head regions between remote animal phyla. Results: We find that in the marine annelid Platynereis dumerilii, expression of the homeobox gene six3 defines the apical region of the larval body, peripherally overlapping the equatorial otx+ expression. The six3+ and otx+ regions thus define the developing head in anterior-to-posterior sequence. In another annelid, the earthworm Pristina, as well as in the onychophoran Euperipatoides, the centipede Strigamia and the insects Tribolium and Drosophila,asix3/optix+ region likewise demarcates the tip of the developing animal, followed by a more posterior otx/otd+ region. Identification of six3+ head neuroectoderm in Drosophila reveals that this region gives rise to median neurosecretory brain parts, as is also the case in annelids.