Content uploaded by Dalton Tavares Bressane Nielsen
Author content
All content in this area was uploaded by Dalton Tavares Bressane Nielsen on Dec 12, 2017
Content may be subject to copyright.
Keywords
Ichthyology, taxonomy, killifish, Departamento Beni,
Trinidad
Abstract
Papiliolebias habluetzeli, new species, is described based on
specimens collected in a seasonal pool in Rio Mamoré basin,
around the town of Trinidad, northern Bolivia. It differs
from all the other species of the genus apart from Papili-
olebias francescae by the following features in males: dorsal
and anal fins pointed, proximal half portion of dorsal and
anal fin whitish with broad dark red stripes, caudal fin with
transverse rows of dark red spots and metallic golden blotch
on humeral region. It differs from Papiliolebias francescae by
male flank and anal fin color pattern and different number
of branchiostegal rays and pelvic fin rays.
Zusammenfassung
Papiliolebias habluetzeli, eine neue Arten, wird auf der
Grundlage von Proben in einem saisonalen Teich im Rio
Mamoré Becken, um die Stadt Trinidad, im nördlichen Bo-
livien gesammelt beschrieben. Es unterscheidet sich von
allen anderen Arten der Gattung, abgesehen von Papilio -
lebias francescae, durch die folgenden Merkmale bei Män-
nern: dorsal und anale Flossen verlaufen spitz, etwa die
Hälfte der dorsalen und analen Flossen ist weißlich mit bre-
iten dunkelroten Streifen, Schwanzflosse mit Querreihen
von dunkelroten Flecken und metallischen goldenem Fleck
in der Humoralen Region. Es unterscheidet sich von Papi -
liolebias francescae durch unterschiedliche Seiten- und anal
Flossenfarben der Männchen und verschiedene Anzahl von
branchiostegal Strahlen und Beckenflossenstrahlen.
Résumé
Papiliolebias habluetzeli, nouvelle espèce, est décrite sur
base de spécimens collectés dans une mare temporaire dans
le bassin du Rio Mamoré, autour de la ville de Trinidad, au
nord de la Bolivie. Elle se distingue de toutes les autres es-
pècesdu genre, sauf de Papiliolebias francescae par les détails
suivants pour les mâles ; dorsale et anale pointues, à peu près
la moitié de la dorsale et de la caudale blanchâtre avec de
larges lignes rouge foncé, la caudale avec des rangées trans-
versales de taches rouge foncé et une marque dorée mé-
tallique sur la région humérale. Elle se distingue de Papili-
olebias francescae, pour les mâles, par le patron de coloration
du flanc et de l’anale, par un nombre différent de rayons
branchiostégaux et de rayons pelviens
Sommario
Papiliolebias habluetzeli, nuova specie, è descritta sulla base
di esemplari raccolti in una pozza stagionale del bacino del
rio Mamoré, nei pressi della città di Trinidad, nel nord della
Bolivia. Si differenzia da tutte le altre specie del genere, a
parte P. francescae, per le seguenti caratteristiche nei maschi:
pinne dorsale ed anale appuntite, metà prossimali della pin-
na dorsale e di quella anale biancastre con larghe strisce rosse
scure, pinna caudale con file trasversali di macchie rosso
scuro e una macchia diffusa dorata sulla regione omerale. Si
differenzia da P. francescae per la colorazione dei lati del cor-
po e della pinna anale negli individui maschi e per il diverso
numero di raggi branchiostegi e raggi della pinna pelvica.
INTRODUCTION
Bolivia has a high diversity of annual killifish
species belonging to the family Cynolebiidae, with
representatives of the genera Austrolebias, Moema,
Neofundulus, Papiliolebias, Pterolebias, Spectrolebias,
and Trigonectes with a total of sixteen species found
in the Amazonian area at the central and northern
Bolivia and in the Bolivian Gran Chaco at the
southern portion of the country (Costa 1990, 1993,
aqua vol. 22 no. 4 - 22 October 2016
155
aqua, International Journal of Ichthyology
Papiliolebias habluetzeli (Cyprinodontiformes: Cynolebiidae) a new miniature
annual fish from the upper Rio Mamoré basin, Bolivia
Stefano Valdesalici1, Dalton Tavares Bressane Nielsen2, Roger Brousseau3and Jurij Phunkner4
1) Via Cà Bertacchi 5, 42030 Viano (RE), Italy. E-mail: valdesalici.stefano@gmail.com
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
AQUA-22(4).qxp_AQUA 24/10/16 12:29 Pagina 155
1998, 2003, 2005, Costa, Barrera & Sarmiento
1997, Hablützel 2012 a-b, Hablützel et al. 2013,
Nielsen 2013, Nielsen & Brousseau 2013a-b, 2014,
Osinaga 2006, Schalk et al. 2013, Valdesalici &
Brousseau 2014).
The genus Papiliolebias comprises four species: P.
bitteri, from the Chaco region of the Paraguay River
basin, Paraguay and Argentina, P. hatinne from Rio
Bermejo basin, Salta, Argentina and Rio Pilcomayo,
Tarija Department, Bolivia, and P. ashleyae and P.
francescae from Rio San Pablo drainage, Rio Madeira
River basin, Bolivia.
The phenomenon of miniaturization consists in
the extreme reduction in body size within a lineage
(Hanken & Wake 1993). As the result of collections
directed to more specialized habitats and use of ap-
propriated collecting techniques, new reports about
miniature freshwater fishes, maturing at sizes under
20.0 mm SL, or reaching 26.0 mm SL as maximum
adult size, as established by Weitzman & Vari
(1988), have become more frequent in the literature
(Mattox et al. 2013, Costa & Lazzarotto 2014). The
objective of this paper is to describe a new miniature
Papiliolebias species from temporary pools near Río
Mamore around the city of Trinidad, department of
Beni, Bolivia.
MATERIALS AND METHODS
Measurements and counts were taken as described
in Costa (1995). Measurements were made with a
digital calliper, partly under a dissecting microscope,
and rounded to the nearest 0.1 mm. If not stated
otherwise, measurements are presented as percent-
ages of standard length (SL), except for eye diameter,
head width, and head depth which are given as per-
centage of head length (HL). Osteological prepara-
tions were made according to Taylor & Van Dyke
(1985). Nomenclature for cephalic laterosensory se-
ries follows Costa (2001). Terminology for frontal
squamation follows Hoedeman (1958). Type mater-
ial was deposited at the: Museo de Peces (CIRA-
UAB-JB), Trinidad; Museo Civico di Storia Naturale
“Giacomo Doria” (MSNG), Genova; Zoologische
Staatssammlung München (ZSM), München;
Museu de Zoologia Universidade Estadual de Camp-
inas “Adão José Cardoso” (ZUEC), Campinas.
Papiliolebias habluetzeli, n. sp.
(Figs 1-5; Table I)
Papiliolebias sp.: Hablützel, 2012a: 62-65 (reported
as: “Moxos-Kärpfling”, pictures of males and fe-
male, coloration and maximum size reached com-
pared with P. bitteri and P. hatinne).
Holotype: CIRA 3271, male, 25.1 mm SL, Bolivia,
Departamento Beni, about 30 km north of
Trinidad, Rio Mamoré basin, 14°33’16” S, 64°52’4”
W, D. Pillet et al., 22 March 2013
Paratypes: MSNG 59185, 1 male, 19.6 mm SL,
same data as holotype. ZUEC 8301, 6 males 23.0-
31.3 mm SL, 6 females 20.5-22.8 mm SL; Bolivia,
Departamento Beni, East of Trinidad, Río Mamoré
basin, 9, 14°49’27” S, 64°50’17” W, R. D. Brous -
seau & J. Phunkner, 18 February 2013. ZSM
43528, 1 male, 22.8 mm SL, 2 females 21.2-22.9
mm SL, Bolivia, Departemento Beni, small pond at
Campus of Universidad Trinidad, within catchment
of Rio Mamoré, 14°48’43.581” S, 64°53’37.893”
W, R. Guggenbühl et al., 20 July 2014. MSNG
59186, male, 22 mm SL, C&S, Bolivia, Departa-
mento Beni, East of Trinidad, Río Mamoré basin,
14°49’27” S, 64°50’17” W, Joe Bulterman et al., 18
February 2014.
Diagnosis: Males Papiliolebias habluetzeli are simi-
lar to males of P. francescae and differ from the other
members of the genus by the following unique fea-
tures: dorsal and anal fins pointed (vs. rounded);
proximal half dorsal and anal fin whitish with broad
dark red stripes (vs. proximal portion white with
black spots); caudal fin with transverse rows of dark
red spots (vs. never a similar colour pattern); and
metallic golden blotch on humeral region (vs. metal-
lic bluish green). P. habluetzeli differs from P.
francescae by colour, number and shape of bars on
flanks (orange red vs. dark red; 11-13 vs. 9-10, rarely
11, and thin formed by single scale line, vs. broad,
sometime fused into more than a single line, mostly
on anterior portion of body), number and shape of
red proximal stripes on anal fin (5-8, usually 7, vs. 5,
rarely 6; thin vs. broad and long); extension of white
pigmentation at proximal area on anal fin (about ¼
of the fin vs. half fin); absence of thin white rim on
anal fin (vs. presence), 5 (vs. 6) branchiostegal rays
and 6 (vs. 7) pelvic-fin rays.
Description: Morphometric data are presented in
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,
slightly concave on caudal peduncle. Ventral profile
gently convex from lower jaw to anal-fin origin,
nearly straight to slightly concave along caudal pe-
duncle. Body moderately slender, compressed.
aqua vol. 22 no. 4 - 22 October 2016 156
Papiliolebias habluetzeli (Cyprinodontiformes: Cynolebiidae) a new miniature annual fish from the upper Rio Mamoré basin, Bolivia
AQUA-22(4).qxp_AQUA 24/10/16 12:29 Pagina 156
Greatest body depth at level of pelvic-fin base. Jaws
short, snout blunt. Dorsal and anal-fins pointed in
males, tip reaching to vertical through base of caudal
fin in males, dorsal fin slightly pointed, anal-fin
rounded in females. Caudal-fin rounded. Pectoral-
fin rounded, its posterior margin reaching vertical
between and urogenital papilla and first ray of anal-
fin in males. Pelvic-fins pointed, with filamentous
tip reaching between base of 5th and 6th anal-fin ray
in males; between urogenital papilla and first ray of
anal fin in females. Pelvic-fin bases separated. Dor-
sal-fin origin on vertical through base of 6th to 8th
anal-fin rays. Dorsal-fin rays 11-12; anal-fin rays 19-
20; caudal-fin rays 20-21; pectoral-fin rays 11-12;
pelvic-fin rays 6. Scales large, cycloid. Body and
head entirely scaled, except anterior ventral surface
of head. Body squamation extending onto anterior
10% of caudal fin; no scales on dorsal and anal-fin
bases. Frontal squamation F-patterned; E-scales not
overlapping medially; frontal scales circularly
arranged around A-scale. Longitudinal series of
scales 24-25; transverse series of scales 8-11; scale
rows around caudal peduncle 14. Cephalic neuro-
masts: supraorbital 1+3+ 4, posterior rostral 1, infra-
orbital 9 + 2, preorbital 3, otic 1, postotic 1, preop-
ercular 1+1. One neuromast on center of each scale
of lateral line of trunk, sometimes absent in few
scales. Five branchiostegal rays. Total vertebrae 25.
Colour in life: Males (Figs 1-4): Sides of
aqua vol. 22 no. 4 - 22 October 2016
157
Stefano Valdesalici, Dalton Tavares Bressane Nielsen, Roger Brousseau and Jurij Phunkner
H Paratypes
Male Male n=10 Females n=8
Standard length (mm) 25.1 19.6-31.3 20.5-22.9
Percent of standard length
Body depth 29.8 29.0-36.0 28.1-31.1
Caudal peduncle depth 13.1 13.1-18.4 13.0-16.4
Pre-dorsal length 69.3 63.4-71.4 69.7-72.6
Pre-anal length 58.5 56.1-64.9 63.3-65.0
Pre-pelvic length 45.0 42.1-56.5 49.2-52.8
Length of dorsal-fin base 14.3 14.3-18.3 11.3-15.7
Length of anal-fin base 24.3 24.3-28.9 22.0-27.9
Caudal-fin length 21.1 21.1-40.8 23.6-33.9
Pectoral-fin length 23.9 17.6-24.1 17.9-21.4
Pelvic-fin length 13.1 12.8-23.4 11.3-14.1
Head length 29.4 28.0-32.1 25.8-34.1
Percent of head length
Head depth 87.2 77.5-92.7 79.7-92.7
Head width 54.5 35.1-56.4 39.3-47.6
Eye diameter 45.4 28.4-45.4 31.7-37.2
Table I. Morphometric and meristic data for the holotype
(H) and paratypes of Papiliolebias habluetzeli.
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.
AQUA-22(4).qxp_AQUA 24/10/16 12:29 Pagina 157
aqua vol. 22 no. 4 - 22 October 2016 158
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.
AQUA-22(4).qxp_AQUA 24/10/16 12:29 Pagina 158
aqua vol. 22 no. 4 - 22 October 2016
159
Stefano Valdesalici, Dalton Tavares Bressane Nielsen, Roger Brousseau and Jurij Phunkner
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.
AQUA-22(4).qxp_AQUA 24/10/16 12:29 Pagina 159
body whitish greenish with 11-13 oblique, chevron-
shaped, light blue and red alternating stripes; dark
metallic golden vertical blotch on humeral region.
Dorsum red brown with small black dots extending
on caudal peduncle. Sides of head yellowish, opercle
golden yellow. Jaws red brown. Iris orange, with a
black vertical bar through center of eye. Bran-
chiostegal membranes golden yellow. Dorsal fin
white to yellowish white on the basal half, with 5-6
red bars on basal portion, distal portion bluish. Anal
fin white to yellowish white on the proximal por-
tion, with 5-8 red bars; distal portion bluish. Caudal
fin whitish on proximal portion with two or three
transverse rows of reddish spots, hyaline to greyish
on distal portion. Pectoral-fins hyaline. Pelvic fins
whitish, hyaline with bluish tint on distal portion.
Females (Fig. 5): Sides of head and trunk light
brown with a gray tint. Dorsum light brown with
small black dots extending to caudal peduncle. Low-
er surface of head light gray to whitish. Opercular
region silvery. Humeral region golden. Black subor-
bital bar. Jaws light brown. Iris yellow orange, with
black bar through center of eye. Unpaired and
paired fins hyaline.
Distribution: Known from several localities north,
east and south of the city of Trinidad. All localities
lying within the Rio Mamoré basin, Departamento
Beni, northern Bolivia (Fig. 6).
Habitat: The type locality (Fig. 7) was a small pool
with water depth about 0.3 m. Most parts of the
habitat were heavily overgrown by grass and aquatic
vegetation. The water was slightly turbid. The ac-
companying fauna consisted of non-annual fish
species: Cichlasoma (presumably C. boliviense), Syn-
branchus sp., and Brachyhypopomus sp. and another
annual species, Pterolebias longipinnis.
aqua vol. 22 no. 4 - 22 October 2016 160
Papiliolebias habluetzeli (Cyprinodontiformes: Cynolebiidae) a new miniature annual fish from the upper Rio Mamoré basin, Bolivia
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).
AQUA-22(4).qxp_AQUA 24/10/16 12:29 Pagina 160
aqua vol. 22 no. 4 - 22 October 2016
161
Stefano Valdesalici, Dalton Tavares Bressane Nielsen, Roger Brousseau and Jurij Phunkner
Fig. 7. Type locality of Papiliolebias habluetzeli. Photo by D. Pillet.
AQUA-22(4).qxp_AQUA 24/10/16 12:29 Pagina 161
Etymology: In honor of Pascal István Hablützel,
who was the first to document this species and for
his research on Bolivian ichthyofauna.
DISCUSSION
Miniaturization is an evolutionary process observed
in all vertebrate lineages, consisting of extreme re-
duction in body size (Hanken & Wake 1993).
Weitzman & Vari (1988) undertook the first survey
documenting the numerous miniature freshwater
fishes of South America. They defined miniature
fishes as those no greater than 26 mm SL or matur-
ing at sizes smaller than 20 mm SL and identified 85
such species. Costa & Le Bail (1999) added 26 more
species, while recently Toledo-Piza et al. (2014)
adopting the cut-off point of 26 mm SL presented a
list of 213 species of miniature Neotropical freshwa-
ter fishes. Since Papiliolebias habluetzeli reaches an
adult size of 31.3 mm SL, it does not fit in the upper
limit for miniatures suugested by Weitzman & Vari
(1988) and followed by Toledo-Piza et al. (2014).
However, both Papiliolebias habluetzeli and P.
francescae might be considered as miniature species
because both reach maturity at sizes smaller than 20
mm SL. Weitzman & Vari (1988) observed that
miniaturization is commonly accompanied by a re-
duction in morphological characters. The reduced
number of branchiostegal and pelvic fin rays in Pa-
piliolebias habluetzeli may represent reductive mor-
phological characters associated with minaturization.
The genus Papiliolebias was defined by four
synapomorphies (Costa 1998): unpaired fins dark
blue and with a white line along distal margin of
anal fin in males, nine pelvic-fin rays, and a metallic
bluish green humeral blotch. Based on the features
presented by recently described species the number
of pelvic-fin rays and unpaired fins colouration are
autapomorphic for P. bitteri. We currently prefer to
assign the new species to Papiliolebias instead of cre-
ating a new genus, since we consider this choice
more conservative. Additionally to the above the
genus Papiliolebias is characterized by: urohyal, dor-
sal process branched (also present in some species of
Pituna); third epibranchial, uncinate process, form-
ing an angle of 45-60° with distal process (but not
in plesiolebiasines); ventral process of posttemporal
present; opercular region with regular reticulate pat-
tern formed by iridescent colour on middle of scales
contrasting with dark orangish brown pigment
along entire scale margins (also in Pituna); and
humeral region with iridescent blotch (also in Pitu-
na) (Costa 2011).
Papiliolebias hablutzeli differs from all species of the
genus by 5 (vs. 6 in P. francescae, P. ashleyae, P.
hatinne, P. bitteri) branchiostegal rays and 6 pelvic
fin rays (vs. 7 in P. francescae,, 7-8 in P. ashleyae and
P. hatinne and 9 in P. bitteri). Additionally, P.
hablutzeli can be diagnosed from its congeners by
the number of caudal-fin rays (20-21 vs. 22-25 in P.
francescae, 19-20 in P. ashleyae, 25-28 in P. bitteri,
20-23 in P. hatinne), fewer number of vertebrae (25
vs. 26 in P. francescae, 25-28 in P. ashleyae, 27-30 in
P. bitteri, 26-28 in P. hatinne), more scales in trans-
verse series (8-11 vs. 11-12 in P. francescae, 11 in P.
hatinne, 9 in P. ashleyae), and more anal-fin rays (19-
20 vs.18-19 in P. francescae, 15-16 in P. ashleyae, 17-
18 in P. bitteri).
The presence of the genus Papiliolebias in the up-
per Río Mamore basin and in Río Paraguay basin,
plus the presence of other genus of annual fish also
present in these two areas, such as Moema,
Pterolebias, Trigonectes, Neofundulus, Austrolebias and
Spectrolebias indicates that faunal exchange has oc-
curred among these drainages. This portion of west-
ern South America undertook intense tectonic activ-
ity during the course of the last few millions years,
with the subsidence of the Pantanal wetland, and
consequent rearrangement of the hydrographic
basins in the area (Ribeiro et al. 2013). The two
basins are separated now by a few miles in southeast-
ern Bolivia near the border with Brazil by a small
difference in elevation. The interchanges between
Paraguay River with the southern tributaries of the
Amazon River is corroborated by sister group rela-
tionship between the genus Papiliolebias from the
Paraguayan Chaco and the clade comprising
Maratecoara and Pituna (Murphy et al. 1999). This
proposed former interchange is congruent with the
palaeogeographic reconstruction of the cis-Andean
region of Bolivia that shows a separation between
the Paraguay and Amazon basin, between the late
Oligocene and early Miocene Periods (e.g. Sempere
et al. 1990; Lundberg et al., 1998). This region sub-
sequently underwent intense wetter climatic condi-
tions than at present (Ab’ Saber 1988).
ACKNOWLEDGEMENTS
We thank Joe Bulterman for his assistance during
fieldwork, Pascal Hablützel for sharing information
on the species, Didier Piller donating specimens and
pictures, Guillaume Dethu for the pictures, and fi-
nally Flávio C. T. Lima and the anonymous review-
ers for providing constructive comments on the
manuscript. We are grateful to Federico Moreno
aqua vol. 22 no. 4 - 22 October 2016 162
Papiliolebias habluetzeli (Cyprinodontiformes: Cynolebiidae) a new miniature annual fish from the upper Rio Mamoré basin, Bolivia
AQUA-22(4).qxp_AQUA 24/10/16 12:29 Pagina 162
Aulo and Takayuki Yunoki (CIRA-UAB-JB), Giu-
liano Doria (MSNG), Dirk Neumann (ZSM), and
Flávio C. T. Lima (ZUEC) for access to the collec-
tions under their care.
REFERENCES
AB’SABER, A. N. 1988. O Pantanal Mato-grossense e a teoria
dos refúgios. Revista Brasileira de Geografia 50 (2): 9-57.
COSTA, W. J. E. M. 1990. Systematics and distribution of the
Neotropical annual fish genus Trigonectes (Cyprino don -
tiformes, Rivulidae), with description of two new spe cies.
Ichthyological Exploration of Freshwaters 1(2): 135-150.
COSTA, W. J. E. M 1993. Sistemática e distribução do
gênero Moema (Cyprinodontiformes, Rivulidae), com a
descrição de uma nova espécie. Revista Brasileira de Biologia
52 (4): 619-625.
COSTA, W. J. E. M. 1995. Pearl killifishes, the Cynolebiatinae:
systematics and biogeography of the neotropical annual fish
subfamily (Cyprinodontiformes: Rivulidae). Neptune City,
TFH, 128 pp.
COSTA, W. J. E. M. 1998. Revision of the neotropical annu-
al fish genus Plesiolebias (Cyprinodontiformes: Rivulidae).
Ichthyological Exploration of Freshwaters 8: 313–334.
COSTA, W. J. E. M. 2001. The neotropical annual fish genus
Cynolebias (Cyprinodontiformes: Rivulidae): phylogenetic
relationships, taxonomic revision and biogeography.
Ichthyological Exploration of Freshwaters 12: 333–383.
COSTA, W. J. E. M. 2003. Three new annual fishes of the
genus Aphyolebias Costa, 1998 (Cyprinodontiformes:
Rivulidae) from Bolivian and Peruvian Amazon. Comuni-
cações do Museu de Ciências e Tecnologia da PUCRS, Série
Zoologia 16: 155-166.
COSTA, W. J. E. M. 2005. The Neotropical annual killifish
genus Pterolebias Garman (Teleostei: Cyprinodontiformes:
Rivulidae): phylogenetic relationships, descriptive mor-
phology, and taxonomic revision. Zootaxa 1067: 1-36.
COSTA, W. J. E. M. 2011. Comparative morphology, phylo-
genetic relationships, and historical biogeography of plesi-
olebiasine seasonal killifishes (Teleostei: Cyprinodontif-
ormes: Rivulidae). Zoological Journal of the Linnean Society
162: 131-148.
COSTA, W. J. E. M. 2014 Phylogeny and evolutionary ra-
diation in seasonal rachovine killifishes: biogeographical
and taxonomical implications. Vertebrate Zoology 64 (2):
177-192.
COSTA, W. J. E. M. & LEBAIL, P.-Y. 1999. Fluviphylax pa-
likur: a new poeciliid from the Rio Oiapoque basin, north-
ern Brazil (Cyprinodontiformes: Cyprinodontoidei), with
comments on miniaturization in Fluviphylax and other
Neotropical freshwater fishes. Copeia 1999: 1027-1034.
COSTA, W. J. E. M. & LAZZAROTTO, H. 2014. Laimosemion
ubim, a new miniature killifish From the Brazilian Amazon
(Teleostei: Rivulidae) Ichthyological Exploration of Freshwa-
ters 24: 371-378.
COSTA, W. J. E. M., BARRERA, S. & SARMIENTO, J. 1997.
Simpsonichthys filamentosus, une nouvelle espèce des Lla-
nuras Benianas, bassin du río Mamoré, Bolivia. Revue
Française d’Aquariologie 24: 83-86.
HABLÜTZEL, P. I. 2012a. Iténez- und Moxos-Kärpfling, zwei
neue Killifische aus Bolivien. Die Aquarien- und Terrarien-
zeitschrift 3: 62-65.
HABLÜTZEL, P. I. 2012b. A preliminary survey of the fish
fauna in the vicinity of Santa Ana del Yacuma in Bolivia
(río Mamoré drainage). Biota Neotropica 12 (4): 1-10.
HABLÜTZEL, P. I., YUNOKI, T. & VELASCO, L. T. 2013. Up-
date on the checklist of fish species of the Bolivian Amazon
Check List 9 (2): 208-210.
HANKEN, J. & WAKE, D. B. 1993. Miniaturization of body
size: organismal consequences and evolutionary signifi-
cance. Annual Review of Ecology and Systematics 24: 501-
519.
HOEDEMAN, J. J. 1958. The frontal scalation pattern in
some groups of toothcarps (Pisces, Cyprinodontiformes).
Bulletin of Aquatic Biology 1: 23-28.
LUNDBERG, J. G., MARSHALL, L. G., GUERRERO, J., HOER-
TON, B., MALABARBA, M. C. S. L. & WESSELINGH, F.
1998. The stage for Neotropical fish diversification: a his-
tory of tropical South American rivers. In: Malabarba, L.
R., Reis, R. E., Vari, R. P., Lucena, Z. M. S. & Lucena, C.
A. S. (Eds.), Phylogeny and Classification of Neotropical fish-
es, Edipucrs, Porto Alegre, pp.13-48.
MATTOX, G. M. T., BRITZ, R., TOLEDO-PIZA, M. & MAR-
INHO, M. M. F. 2013. Cyanogaster noctivaga, a remarkable
new genus and species of miniature fish from the Rio Ne-
gro, Amazon basin (Ostariophysi: Characidae). Ichthyolog-
ical Exploration of Freshwaters 23: 297-318.
MURPHY,W. J., THOMERSON, J. E. & COLLIER, G. E. 1999.
Phylogeny of the neotropical Killifish family Rivulidae
(Cyprinodontiformes: Aplocheiloidei) inferred from mito-
chondrial DNA sequences. Molecular and Phylogenetic
Evolution 13: 289-301.
NIELSEN, D. T. B. 2013. Spectrolebias brousseaui (Cyprin-
odontiformes: Rivulidae: Cynolebiatinae), a new annual
fish from the upper río Mamoré basin, Bolivia. Neotropical
Ichthyology 11: 81-84.
NIELSEN, D. T. B. & BROUSEEAU, R. D. 2013a. Description
of a new species of annual fish of the genus Neofundulus
(Cyprinodontiformes: Rivulidae) from the upper río
Mamoré basin, Bolivia. aqua, International Journal of
Ichthyology 19 (3): 109-114.
NIELSEN, D. T. B. & BROUSEEAU, R. D. 2013b. Spectrolebias
pilleti, a new annual killifish (Cyprinodontiformes: Rivul-
idae: Cynolebiatinae) from the upper rio Mamoré basin,
Bolivia. aqua, International Journal of Ichthyology 19 (3):
115-122.
NIELSEN, D. T. B. & BROUSEEAU, R. D. 2014. Description
of a new annual fish, Papiliolebias ashleyae (Cyprinodon-
tiformes: Rivulidae) from the upper Rio Mamoré basin,
Bolivia. aqua, International Journal of Ichthyology 20 (1):
53-59.
OSINAGA, K. R. 2006. Nuevo registro para Bolivia de Aus-
trolebias monstrosus Huber, 1995 (Rivulidae). Kempffiana
2: 60-62.
RIBEIRO, A. C., JACOB, R. M., SILVA, R. S. R. R., LIMA, F. C.
T., FERREIRA, D. C., FERREIRA, K. M., MARIGUELA, T. C.,
PEREIRA, L. H. G. & OLIVEIRA, C. 2013. Distributions
aqua vol. 22 no. 4 - 22 October 2016
163
Stefano Valdesalici, Dalton Tavares Bressane Nielsen, Roger Brousseau and Jurij Phunkner
AQUA-22(4).qxp_AQUA 24/10/16 12:29 Pagina 163
and phylogeographic data of rheophilic freshwater fishes
provide evidences on the geographic extension of a central-
brazilian Amazonian palaeoplateau in the area of the pre-
sent day Pantanal Wetland. Neotropical Ichthyology 11:
319-326.
SCHALK, M. C., MONTAÑA, C. G. & LIBSON, M. E. 2014
Reproductive strategies of two Neotropical killifish, Aus-
trolebias vandenbergi and Neofundulus ornatipinnis
(Cyprinodontiformes: Rivulidae) in the Bolivian Gran
Chaco. Revista de Biologia Tropical 62: 109-17.
SEMPERE, T., HERAIL, J., OLLER, J. & BONHOMME, M. G.
1990. Late Oligocene-early Miocene major tectonic crisis
and related basin in Bolivia. Geology 18: 946-949.
TAYLOR , W. R & VAN DYKE, G. C. 1985. Revised proce-
dures for staining and clearing small fishes and other ver-
tebrates for bone and cartilage study. Cybium 9: 107-109.
TOLEDO-PIZA, M., MATTOX, G. M. T. & BRITZ, R. 2014.
Priocharax nanus, a new miniature characid from the rio
Negro, Amazon basin (Ostariophysi: Characiformes), with
an updated list of miniature Neotropical freshwater fishes.
Neotropical Ichthyology 12: 229-246.
VALDESALICI, S. & BROSSEAU, R. D. 2014. A new Papili-
olebias species (Teleostei: Cyprinodontiformes: Rivulidae)
from Bolivian Amazon. aqua, International Journal of
Ichthyology 20: 117-122.
WEITZMAN, S. H. & VARI, R. P. 1988. Miniaturization in
South American freshwater fishes; an overview and discus-
sion. Proceedings of the Biological Society of Washington 101:
444-465.
aqua vol. 22 no. 4 - 22 October 2016 164
Papiliolebias habluetzeli (Cyprinodontiformes: Cynolebiidae) a new miniature annual fish from the upper Rio Mamoré basin, Bolivia
AQUA-22(4).qxp_AQUA 24/10/16 12:29 Pagina 164
