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aqua, International Journal of Ichthyology

Papiliolebias habluetzeli (: Cynolebiidae) a new miniature annual from the upper Rio Mamoré basin, Bolivia

Stefano Valdesalici1, Dalton Tavares Bressane Nielsen2, Roger Brousseau3 and Jurij Phunkner4

1) Via Cà Bertacchi 5, 42030 Viano (RE), Italy. E-mail: [email protected] 2) Laboratório de Zoologia, departamento de Biologia, Universidade de Taubaté, Pça Marcelino Monteiro 63, CEP: 12030-010, Taubaté, SP, Brazil 3) 8345 Bull Mountain Circle, Elk Grove, California 95758, USA 4) 7 Plenshin Court, Glasgow, Scotland, G53 6QW, UK

Received: 08 June 2016 – Accepted 07 October 2016

Keywords le bassin du Rio Mamoré, autour de la ville de Trinidad, au Ichthyology, , killifish, Departamento Beni, nord de la Bolivie. Elle se distingue de toutes les autres es- Trinidad pècesdu genre, sauf de francescae par les détails suivants pour les mâles ; dorsale et anale pointues, à peu près Abstract la moitié de la dorsale et de la caudale blanchâtre avec de Papiliolebias habluetzeli, new species, is described based on larges lignes rouge foncé, la caudale avec des rangées trans- specimens collected in a seasonal pool in Rio Mamoré basin, versales de taches rouge foncé et une marque dorée mé- around the town of Trinidad, northern Bolivia. It differs tallique sur la région humérale. Elle se distingue de Papili- from all the other species of the apart from Papili- olebias francescae, pour les mâles, par le patron de coloration olebias francescae by the following features in males: dorsal du flanc et de l’anale, par un nombre différent de rayons and anal fins pointed, proximal half portion of dorsal and branchiostégaux et de rayons pelviens anal fin whitish with broad dark red stripes, caudal fin with transverse rows of dark red spots and metallic golden blotch Sommario on humeral region. It differs from Papiliolebias francescae by Papiliolebias habluetzeli, nuova specie, è descritta sulla base male flank and anal fin color pattern and different number di esemplari raccolti in una pozza stagionale del bacino del of branchiostegal rays and pelvic fin rays. rio Mamoré, nei pressi della città di Trinidad, nel nord della Bolivia. Si differenzia da tutte le altre specie del genere, a Zusammenfassung parte P. francescae, per le seguenti caratteristiche nei maschi: Papiliolebias habluetzeli, eine neue Arten, wird auf der pinne dorsale ed anale appuntite, metà prossimali della pin- Grundlage von Proben in einem saisonalen Teich im Rio na dorsale e di quella anale biancastre con larghe strisce rosse Mamoré Becken, um die Stadt Trinidad, im nördlichen Bo- scure, pinna caudale con file trasversali di macchie rosso livien gesammelt beschrieben. Es unterscheidet sich von scuro e una macchia diffusa dorata sulla regione omerale. Si allen anderen Arten der Gattung, abgesehen von Papilio - differenzia da P. francescae per la colorazione dei lati del cor- lebias francescae, durch die folgenden Merkmale bei Män- po e della pinna anale negli individui maschi e per il diverso nern: dorsal und anale Flossen verlaufen spitz, etwa die numero di raggi branchiostegi e raggi della pinna pelvica. Hälfte der dorsalen und analen Flossen ist weißlich mit bre- iten dunkelroten Streifen, Schwanzflosse mit Querreihen INTRODUCTION von dunkelroten Flecken und metallischen goldenem Fleck Bolivia has a high diversity of annual killifish in der Humoralen Region. Es unterscheidet sich von Papi - species belonging to the family Cynolebiidae, with liolebias francescae durch unterschiedliche Seiten- und anal Flossenfarben der Männchen und verschiedene Anzahl von representatives of the genera , , branchiostegal Strahlen und Beckenflossenstrahlen. Neofundulus, Papiliolebias, , Spectrolebias, and Trigonectes with a total of sixteen species found Résumé in the Amazonian area at the central and northern Papiliolebias habluetzeli, nouvelle espèce, est décrite sur Bolivia and in the Bolivian Gran Chaco at the base de spécimens collectés dans une mare temporaire dans southern portion of the country (Costa 1990, 1993,

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Papiliolebias habluetzeli (Cyprinodontiformes: Cynolebiidae) a new miniature annual fish from the upper Rio Mamoré basin, Bolivia

1998, 2003, 2005, Costa, Barrera & Sarmiento as: “Moxos-Kärpfling”, pictures of males and fe- 1997, Hablützel 2012 a-b, Hablützel et al. 2013, male, coloration and maximum size reached com- Nielsen 2013, Nielsen & Brousseau 2013a-b, 2014, pared with P. bitteri and P. hatinne). Osinaga 2006, Schalk et al. 2013, Valdesalici & Brousseau 2014). Holotype: CIRA 3271, male, 25.1 mm SL, Bolivia, The genus Papiliolebias comprises four species: P. Departamento Beni, about 30 km north of bitteri, from the Chaco region of the Paraguay River Trinidad, Rio Mamoré basin, 14°33’16” S, 64°52’4” basin, Paraguay and Argentina, P. hatinne from Rio W, D. Pillet et al., 22 March 2013 Bermejo basin, Salta, Argentina and Rio Pilcomayo, Paratypes: MSNG 59185, 1 male, 19.6 mm SL, Tarija Department, Bolivia, and P. ashleyae and P. same data as holotype. ZUEC 8301, 6 males 23.0- francescae from Rio San Pablo drainage, Rio Madeira 31.3 mm SL, 6 females 20.5-22.8 mm SL; Bolivia, River basin, Bolivia. Departamento Beni, East of Trinidad, Río Mamoré The phenomenon of miniaturization consists in basin, 9, 14°49’27” S, 64°50’17” W, R. D. Brous - the extreme reduction in body size within a lineage seau & J. Phunkner, 18 February 2013. ZSM (Hanken & Wake 1993). As the result of collections 43528, 1 male, 22.8 mm SL, 2 females 21.2-22.9 directed to more specialized habitats and use of ap- mm SL, Bolivia, Departemento Beni, small pond at propriated collecting techniques, new reports about Campus of Universidad Trinidad, within catchment miniature freshwater , maturing at sizes under of Rio Mamoré, 14°48’43.581” S, 64°53’37.893” 20.0 mm SL, or reaching 26.0 mm SL as maximum W, R. Guggenbühl et al., 20 July 2014. MSNG adult size, as established by Weitzman & Vari 59186, male, 22 mm SL, C&S, Bolivia, Departa- (1988), have become more frequent in the literature mento Beni, East of Trinidad, Río Mamoré basin, (Mattox et al. 2013, Costa & Lazzarotto 2014). The 14°49’27” S, 64°50’17” W, Joe Bulterman et al., 18 objective of this paper is to describe a new miniature February 2014. Papiliolebias species from temporary pools near Río Diagnosis: Males Papiliolebias habluetzeli are simi- Mamore around the city of Trinidad, department of lar to males of P.francescae and differ from the other Beni, Bolivia. members of the genus by the following unique fea- tures: dorsal and anal fins pointed (vs. rounded); MATERIALS AND METHODS proximal half dorsal and anal fin whitish with broad Measurements and counts were taken as described dark red stripes (vs. proximal portion white with in Costa (1995). Measurements were made with a black spots); caudal fin with transverse rows of dark digital calliper, partly under a dissecting microscope, red spots (vs. never a similar colour pattern); and and rounded to the nearest 0.1 mm. If not stated metallic golden blotch on humeral region (vs. metal- otherwise, measurements are presented as percent- lic bluish green). P. habluetzeli differs from P. ages of standard length (SL), except for eye diameter, francescae by colour, number and shape of bars on head width, and head depth which are given as per- flanks (orange red vs. dark red; 11-13 vs. 9-10, rarely centage of head length (HL). Osteological prepara- 11, and thin formed by single scale line, vs. broad, tions were made according to Taylor & Van Dyke sometime fused into more than a single line, mostly (1985). Nomenclature for cephalic laterosensory se- on anterior portion of body), number and shape of ries follows Costa (2001). Terminology for frontal red proximal stripes on anal fin (5-8, usually 7, vs. 5, squamation follows Hoedeman (1958). Type mater- rarely 6; thin vs. broad and long); extension of white ial was deposited at the: Museo de Peces (CIRA- pigmentation at proximal area on anal fin (about ¼ UAB-JB), Trinidad; Museo Civico di Storia Naturale of the fin vs. half fin); absence of thin white rim on “Giacomo Doria” (MSNG), Genova; Zoologische anal fin (vs. presence), 5 (vs. 6) branchiostegal rays Staatssammlung München (ZSM), München; and 6 (vs. 7) pelvic-fin rays. Museu de Zoologia Universidade Estadual de Camp- Description: Morphometric data are presented in inas “Adão José Cardoso” (ZUEC), Campinas. Table I. Largest male examined 31.3 mm SL; largest female examined 22.8 mm SL. Dorsal profile slight- ly convex from snout to end of dorsal-fin base, Papiliolebias habluetzeli, n. sp. slightly concave on caudal peduncle. Ventral profile (Figs 1-5; Table I) gently convex from lower jaw to anal-fin origin, nearly straight to slightly concave along caudal pe- Papiliolebias sp.: Hablützel, 2012a: 62-65 (reported duncle. Body moderately slender, compressed.

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Table I. Morphometric and meristic data for the holotype fin in males, dorsal fin slightly pointed, anal-fin (H) and paratypes of Papiliolebias habluetzeli. rounded in females. Caudal-fin rounded. Pectoral- fin rounded, its posterior margin reaching vertical H Paratypes between and urogenital papilla and first ray of anal- Male Male n=10 Females n=8 fin in males. Pelvic-fins pointed, with filamentous Standard length (mm) 25.1 19.6-31.3 20.5-22.9 tip reaching between base of 5th and 6th anal-fin ray Percent of standard length in males; between urogenital papilla and first ray of Body depth 29.8 29.0-36.0 28.1-31.1 anal fin in females. Pelvic-fin bases separated. Dor- Caudal peduncle depth 13.1 13.1-18.4 13.0-16.4 sal-fin origin on vertical through base of 6th to 8th Pre-dorsal length 69.3 63.4-71.4 69.7-72.6 anal-fin rays. Dorsal-fin rays 11-12; anal-fin rays 19- Pre-anal length 58.5 56.1-64.9 63.3-65.0 20; caudal-fin rays 20-21; pectoral-fin rays 11-12; Pre-pelvic length 45.0 42.1-56.5 49.2-52.8 pelvic-fin rays 6. Scales large, cycloid. Body and Length of dorsal-fin base 14.3 14.3-18.3 11.3-15.7 head entirely scaled, except anterior ventral surface Length of anal-fin base 24.3 24.3-28.9 22.0-27.9 of head. Body squamation extending onto anterior Caudal-fin length 21.1 21.1-40.8 23.6-33.9 10% of caudal fin; no scales on dorsal and anal-fin Pectoral-fin length 23.9 17.6-24.1 17.9-21.4 bases. Frontal squamation F-patterned; E-scales not Pelvic-fin length 13.1 12.8-23.4 11.3-14.1 overlapping medially; frontal scales circularly Head length 29.4 28.0-32.1 25.8-34.1 arranged around A-scale. Longitudinal series of Percent of head length scales 24-25; transverse series of scales 8-11; scale Head depth 87.2 77.5-92.7 79.7-92.7 rows around caudal peduncle 14. Cephalic neuro- Head width 54.5 35.1-56.4 39.3-47.6 masts: supraorbital 1+3+ 4, posterior rostral 1, infra- Eye diameter 45.4 28.4-45.4 31.7-37.2 orbital 9 + 2, preorbital 3, otic 1, postotic 1, preop- ercular 1+1. One neuromast on center of each scale Greatest body depth at level of pelvic-fin base. Jaws of lateral line of trunk, sometimes absent in few short, snout blunt. Dorsal and anal-fins pointed in scales. Five branchiostegal rays. Total vertebrae 25. males, tip reaching to vertical through base of caudal Colour in life: Males (Figs 1-4): Sides of

Fig. 1. Papiliolebias habluetzeli, male, holotype, CIRA 3271, male, 25.1 mm SL: Bolivia, about 30 km north of the city of Trinidad, Rio Mamoré basin. Photo by G. Dethu.

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Papiliolebias habluetzeli (Cyprinodontiformes: Cynolebiidae) a new miniature annual fish from the upper Rio Mamoré basin, Bolivia

Fig. 2. Papiliolebias habluetzeli, male, about 30 mm SL, not preserved, Bolivia, about 6 km to the east of the city of Trinidad, Rio Mamoré basin. Photo by R. Brousseau.

Fig. 3. Papiliolebias habluetzeli, male, about 30 mm SL, not preserved, Bolivia, about 15 km east of city of Trinidad along Ruta 9, Rio Mamoré basin. Photo by J. Phunkner.

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Fig. 4. Papiliolebias habluetzeli, male, about 30 mm SL, not preserved, Bolivia, about 35 km east of the city of Trinidad, Rio Mamoré basin. Photo by J. Phunkner.

Fig. 5. Papiliolebias habluetzeli, female, about 25 mm SL, not preserved, Bolivia, Trinidad, Rio Mamoré basin. Photo by G. Dethu.

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body whitish greenish with 11-13 oblique, chevron- small black dots extending to caudal peduncle. Low- shaped, light blue and red alternating stripes; dark er surface of head light gray to whitish. Opercular metallic golden vertical blotch on humeral region. region silvery. Humeral region golden. Black subor- Dorsum red brown with small black dots extending bital bar. Jaws light brown. Iris yellow orange, with on caudal peduncle. Sides of head yellowish, opercle black bar through center of eye. Unpaired and golden yellow. Jaws red brown. Iris orange, with a paired fins hyaline. black vertical bar through center of eye. Bran- Distribution: Known from several localities north, chiostegal membranes golden yellow. Dorsal fin east and south of the city of Trinidad. All localities white to yellowish white on the basal half, with 5-6 lying within the Rio Mamoré basin, Departamento red bars on basal portion, distal portion bluish. Anal Beni, northern Bolivia (Fig. 6). fin white to yellowish white on the proximal por- Habitat: The type locality (Fig. 7) was a small pool tion, with 5-8 red bars; distal portion bluish. Caudal with water depth about 0.3 m. Most parts of the fin whitish on proximal portion with two or three habitat were heavily overgrown by grass and aquatic transverse rows of reddish spots, hyaline to greyish vegetation. The water was slightly turbid. The ac- on distal portion. Pectoral-fins hyaline. Pelvic fins companying fauna consisted of non-annual fish whitish, hyaline with bluish tint on distal portion. species: Cichlasoma (presumably C. boliviense), Syn- Females (Fig. 5): Sides of head and trunk light branchus sp., and Brachyhypopomus sp. and another brown with a gray tint. Dorsum light brown with annual species, Pterolebias longipinnis.

Fig. 6. Geographical distribution of Papiliolebias habluetzeli (lozenges, open lozenge type locality), Papiliolebias francescae (stars), P. ashleyae (circles), P. bitteri (squares), and P. hatinne (inverted triangle).

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Fig. 7. Type locality of Papiliolebias habluetzeli. Photo by D. Pillet.

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Papiliolebias habluetzeli (Cyprinodontiformes: Cynolebiidae) a new miniature annual fish from the upper Rio Mamoré basin, Bolivia

Etymology: In honor of Pascal István Hablützel, Papiliolebias hablutzeli differs from all species of the who was the first to document this species and for genus by 5 (vs. 6 in P. francescae, P. ashleyae, P. his research on Bolivian ichthyofauna. hatinne, P. bitteri) branchiostegal rays and 6 pelvic fin rays (vs. 7 in P. francescae,, 7-8 in P. ashleyae and DISCUSSION P. hatinne and 9 in P. bitteri). Additionally, P. Miniaturization is an evolutionary process observed hablutzeli can be diagnosed from its congeners by in all vertebrate lineages, consisting of extreme re- the number of caudal-fin rays (20-21 vs. 22-25 in P. duction in body size (Hanken & Wake 1993). francescae, 19-20 in P. ashleyae, 25-28 in P. bitteri, Weitzman & Vari (1988) undertook the first survey 20-23 in P. hatinne), fewer number of vertebrae (25 documenting the numerous miniature freshwater vs. 26 in P. francescae, 25-28 in P. ashleyae, 27-30 in fishes of South America. They defined miniature P. bitteri, 26-28 in P. hatinne), more scales in trans- fishes as those no greater than 26 mm SL or matur- verse series (8-11 vs. 11-12 in P. francescae, 11 in P. ing at sizes smaller than 20 mm SL and identified 85 hatinne, 9 in P. ashleyae), and more anal-fin rays (19- such species. Costa & Le Bail (1999) added 26 more 20 vs.18-19 in P. francescae, 15-16 in P. ashleyae, 17- species, while recently Toledo-Piza et al. (2014) 18 in P. bitteri). adopting the cut-off point of 26 mm SL presented a The presence of the genus Papiliolebias in the up- list of 213 species of miniature Neotropical freshwa- per Río Mamore basin and in Río Paraguay basin, ter fishes. Since Papiliolebias habluetzeli reaches an plus the presence of other genus of annual fish also adult size of 31.3 mm SL, it does not fit in the upper present in these two areas, such as Moema, limit for miniatures suugested by Weitzman & Vari Pterolebias, Trigonectes, Neofundulus, Austrolebias and (1988) and followed by Toledo-Piza et al. (2014). Spectrolebias indicates that faunal exchange has oc- However, both Papiliolebias habluetzeli and P. curred among these drainages. This portion of west- francescae might be considered as miniature species ern South America undertook intense tectonic activ- because both reach maturity at sizes smaller than 20 ity during the course of the last few millions years, mm SL. Weitzman & Vari (1988) observed that with the subsidence of the Pantanal wetland, and miniaturization is commonly accompanied by a re- consequent rearrangement of the hydrographic duction in morphological characters. The reduced basins in the area (Ribeiro et al. 2013). The two number of branchiostegal and pelvic fin rays in Pa- basins are separated now by a few miles in southeast- piliolebias habluetzeli may represent reductive mor- ern Bolivia near the border with Brazil by a small phological characters associated with minaturization. difference in elevation. The interchanges between The genus Papiliolebias was defined by four Paraguay River with the southern tributaries of the synapomorphies (Costa 1998): unpaired fins dark Amazon River is corroborated by sister group rela- blue and with a white line along distal margin of tionship between the genus Papiliolebias from the anal fin in males, nine pelvic-fin rays, and a metallic Paraguayan Chaco and the clade comprising bluish green humeral blotch. Based on the features Maratecoara and (Murphy et al. 1999). This presented by recently described species the number proposed former interchange is congruent with the of pelvic-fin rays and unpaired fins colouration are palaeogeographic reconstruction of the cis-Andean autapomorphic for P. bitteri. We currently prefer to region of Bolivia that shows a separation between assign the new species to Papiliolebias instead of cre- the Paraguay and Amazon basin, between the late ating a new genus, since we consider this choice Oligocene and early Miocene Periods (e.g. Sempere more conservative. Additionally to the above the et al. 1990; Lundberg et al., 1998). This region sub- genus Papiliolebias is characterized by: urohyal, dor- sequently underwent intense wetter climatic condi- sal process branched (also present in some species of tions than at present (Ab’ Saber 1988). Pituna); third epibranchial, uncinate process, form- ing an angle of 45-60° with distal process (but not ACKNOWLEDGEMENTS in plesiolebiasines); ventral process of posttemporal We thank Joe Bulterman for his assistance during present; opercular region with regular reticulate pat- fieldwork, Pascal Hablützel for sharing information tern formed by iridescent colour on middle of scales on the species, Didier Piller donating specimens and contrasting with dark orangish brown pigment pictures, Guillaume Dethu for the pictures, and fi- along entire scale margins (also in Pituna); and nally Flávio C. T. Lima and the anonymous review- humeral region with iridescent blotch (also in Pitu- ers for providing constructive comments on the na) (Costa 2011). manuscript. We are grateful to Federico Moreno

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Aulo and Takayuki Yunoki (CIRA-UAB-JB), Giu- HABLÜTZEL, P. I.2012a. Iténez- und Moxos-Kärpfling, zwei liano Doria (MSNG), Dirk Neumann (ZSM), and neue Killifische aus Bolivien. Die Aquarien- und Terrarien- Flávio C. T. Lima (ZUEC) for access to the collec- zeitschrift 3: 62-65. tions under their care. HABLÜTZEL, P. I. 2012b. A preliminary survey of the fish fauna in the vicinity of Santa Ana del Yacuma in Bolivia REFERENCES (río Mamoré drainage). Biota Neotropica 12 (4): 1-10. HABLÜTZEL, P. I., YUNOKI, T. & VELASCO, L. T. 2013. Up- AB’SABER, A. N. 1988. O Pantanal Mato-grossense e a teoria dos refúgios. Revista Brasileira de Geografia 50 (2): 9-57. date on the checklist of fish species of the Bolivian Amazon Check List 9 (2): 208-210. COSTA, W. J. E. M. 1990. Systematics and distribution of the Neotropical annual fish genus Trigonectes (Cyprino don - HANKEN, J. & WAKE, D. B. 1993. 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Papiliolebias habluetzeli (Cyprinodontiformes: Cynolebiidae) a new miniature annual fish from the upper Rio Mamoré basin, Bolivia

and phylogeographic data of rheophilic freshwater fishes dures for staining and clearing small fishes and other ver- provide evidences on the geographic extension of a central- tebrates for bone and cartilage study. Cybium 9: 107-109. brazilian Amazonian palaeoplateau in the area of the pre- TOLEDO-PIZA, M., MATTOX, G. M. T. & BRITZ, R. 2014. sent day Pantanal Wetland. Neotropical Ichthyology 11: Priocharax nanus, a new miniature characid from the rio 319-326. Negro, Amazon basin (Ostariophysi: ), with SCHALK, M. C., MONTAÑA, C. G. & LIBSON, M. E. 2014 an updated list of miniature Neotropical freshwater fishes. Reproductive strategies of two Neotropical killifish, Aus- Neotropical Ichthyology 12: 229-246. trolebias vandenbergi and Neofundulus ornatipinnis VALDESALICI, S. & BROSSEAU, R. D. 2014. A new Papili- (Cyprinodontiformes: Rivulidae) in the Bolivian Gran olebias species (Teleostei: Cyprinodontiformes: Rivulidae) Chaco. Revista de Biologia Tropical 62: 109-17. from Bolivian Amazon. aqua, International Journal of SEMPERE, T., HERAIL, J., OLLER, J. & BONHOMME, M. G. Ichthyology 20: 117-122. 1990. Late Oligocene-early Miocene major tectonic crisis WEITZMAN, S. H. & VARI, R. P. 1988. Miniaturization in and related basin in Bolivia. Geology 18: 946-949. South American freshwater fishes; an overview and discus- TAYLOR, W. R & VAN DYKE, G. C. 1985. Revised proce- sion. Proceedings of the Biological Society of Washington 101: 444-465.

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