httpsdoiorg1011646zootaxa4661112httpzoobankorgurnlsidzoobankorgpub7F9CBF28-6AB1-4BD9-8E9E-001F0C372BAA

ZOOTAXA ISSN 1175-5326 (print edition)

ISSN 1175-5334 (online edition)

Accepted by E Twomey 25 Jul 2019 published 27 Aug 2019 197

Zootaxa 4661 (1) 197ndash200httpswwwmapresscomjzt

Copyright copy 2019 Magnolia PressCorrespondence

The tadpole of Ameerega boehmei in southeastern Bolivia

CONNOR M FRENCH12 CARMEN BURKETTE1 STEFFEN REICHLE3 amp JASON L BROWN14

1Department of Zoology Southern Illinois University 1125 Lincoln Drive Carbondale IL USA 629012Current Address Biology Department The Graduate Center City University of New York 365 Fifth Avenue New York NY USA 100163Museo de Charupas Santiago de Chiquitos Bolivia4Corresponding author E-mail jasonleebrowngmailcom

To date half (16 of 32) of the species of Ameerega have had their tadpoles described A altamazonica A bassleri A bilinguis A braccata A cainarachi A flavopicta A hahneli A macero A parvula A petersi A picta A rubriventris A shihuemoy A silverstonei A smaragdina and A trivittata (Lescure 1976 Silverstone 1976 Duellman 1978 Myers amp Daly 1979 Rodriguez amp Myers 1993 Haddad amp Martins 1994 Loumltters et al 1997 Duellman 2005 Costa et al 2006 Twomey amp Brown 2008 Brown amp Twomey 2009 Poelman et al 2010 Schulze et al 2015) Ameerega boehmei is a putative member of a clade containing Ameerega braccata A flavopicta A berohoka A munduruku all of which in-habit various parts of the lsquodry diagonalrsquo between the Amazon and Atlantic rainforests (Prado amp Gibbs 1993) Adult frogs in this group are morphologically similar generally dark-bodied with yellow dorsolateral stripes orange flash marks and some also possessing bright-yellow dorsal spots Despite considerable research on their breeding behavior acoustics and systematics (Loumltters et al 2009 Forti et al 2013) the tadpole of Ameerega boehmei the southern-most and western-most distributed species in this tentative group has not been described Ameerega boehmei is restricted to the Serraniacuteas de Santiago and Chochis isolated Precambrian sandstone massifs in the Chiquitaniacutea region of Bolivia (Loumltters et al 2009) The cerrado semi-arid open savanna ecosystem where these frogs are found is surrounded by seasonally dry tropical forests that have undergone fire regimes of variable intensity in the past (Power et al 2016) Ameerega boehmei are found close to slow-flowing streams and are observed calling from rock crevices or small tufts of riparian grasses and shrubs punctuating the edges of streams We observed six adults emitting territorial calls across the surveyed time period (21 July 2017 1130 am to 215 pm) and recorded the temperature at two crevice calling sites as 241ordm C and 234ordm C recorded at midday No tadpoles were seen in the observed stream However between 80-120 tadpoles were observed in an adjacent small pool (Fig 2) No predatory insects or fish were observed in the pool It had a thick mixture of sand and silt lining the bottom and was partially shaded by a rocky outcrop and bushes Its maximum depth was 170 mm and its width at the widest points were 191 mm and 112 mm Water temperature ranged from 253ordm C to 262ordm C recorded at 1110 am The surrounding relative humidity was 514 Tadpoles exhibited behavior similar to other Ameerega species with benthic tadpoles settling at the bottom of the pool mostly in shaded areas unless disturbed (Schultze et al 2015) Nearby pools contained no tadpoles and were inhabited by predatory insects Specimens are housed in Coleccioacuten Boliviana de Fauna (CBF) in La Paz Bolivia and were collected by SR in Ser-raniacutea de Santiago roughly 6 km east of Santiago de Chiquitos (1819rsquo S 5934rsquo W ca 800 m above sea level) Chiquitaniacutea region Provincia San Joseacute de Chiquitos Departamento Santa Cruz Bolivia April 2002 Tadpoles were fixed in 10 buff-ered commercial formaldehyde solution Tadpoles were staged following the Gosnerrsquos table (Gosner 1960) The descrip-tion is based on an individual in Gosnerrsquos Stage 28 (CBF 7505) Eight measurements were taken with a dial caliper (to the nearest 01 mm) following Altig and McDiarmid (1999) total length body length tail length maximum tail height tail muscle height tail muscle width internarial distance and interocular distance Morphometric data are given as mean plusmn standard deviation The tadpole of A boehmei belongs to the exotrophic ecomorphological guild benthic type as defined by Altig amp Johnson (1989) This description is based on a tadpole (CBF 7505) at developmental Stage 28 (Gosner 1960 Fig 1) with a total length 268 mm body length 106 mm maximum width 62 mm depth 51 mm internarial distance 18 mm eye to nares distance 09 mm eye diameter 12 mm interorbital distance 22 mm oral disc width 23 mm tail length 162 mm The body is globular compressed in lateral view and ovoid in dorsal view The snout is rounded in dorsal view

FRENCH ET AL198 middot Zootaxa 4661 (1) copy 2019 Magnolia Press

(Fig 1) The oral disc is small and located anteroventrally (Fig 1) Papillae are laterally emarginated simple and coni-cal absent on middle third of anterior labium Anterior jaw sheath has a medial indentation with serration posterior jaw sheath V-shaped and has serration throughout Lateral processes long extending well past lower jaw sheath Labial tooth row formula (LTRF) is 2(2)3 P-1 and P-2 equal width P-3 shorter (80 of P1 and P2) Nares are oval small without projections and inflections and are located dorsolaterally Eyes are small and oriented dorsolaterally The spiracle is single sinistral and located just before mid-body Lateral lines present on either side of the dorsal midline extending from the nares to the base of the tail Fins are concave and the posterior end is pointed Fins reach maximum height at the last third of the tail the dorsal fin does not extend onto the body The maximum tail height is reached at about mid-length and is as high as body height In preservative the body is dark grey the belly is slightly translucent with digestive tract slightly visible caudal musculature creamy white with small irregular grey flecks and slightly translucent fins In life the body is dark brown with black spots the belly is transparent but slightly pigmented posteriorly digestive tract well vis-ible through skin caudal musculature poorly pigmented and transparent tail fin with melanophores in small and irregular clusters along the tail Ontogenetic variation of 12 characteristics was measured on 6 tadpoles in stages 25ndash30 (Gosner 1960) and minimal inter-tadpole variation was observed (Table 1) Despite the unique habitat distribution and natural history the morphology of the tadpole of Ameerega boehmei ap-pears to be incredibly similar to most other Ameerega species For a detailed discussion of tadpole variation in context of other members of this group see Poelman et al (2010) Schultze et al (2015) and Menin et al (2017)

FIGURE 1 Tadpole of Ameerega boehmei Top to Bottom dorsal lateral and ventral view of tadpole (CBF 7505) Inset illustration of the oral disc from a preserved specimen (CBF 7505 Gosner stage 28) Scale bar = 5 mm

THE TADPOLE OF AMEErEGA BoEhMEI Zootaxa 4661 (1) copy 2019 Magnolia Press middot 199

FIGURE 2 (a) An overview of the habitat for Ameerega boehmei in Serraniacutea de Santiago about 6 km east of Santiago de Chiquitos in Provincia San Joseacute de Chiquitos (b) Habitat where adult males were observed in the small patches of vegetation adjacent to the stream (c) Pool used for tadpole deposition by Ameerega boehmei (d) Adult Ameerega boehmei (e) Arrow points to tadpole of Ameerega boehmei in situ

TABLE 1 Table of tadpole measurements Measurements in mmCBF 7506 CBF 7507 CBF 7505 CBF 7508 CBF 7510 CBF 7509

Gosner Stage 25 25 28 28 28 30Total Length 230 235 268 202 196 210Body Length 101 93 106 98 88 87Maximum Width 56 52 62 44 44 45Depth 44 51 51 44 43 49Internarial Distance 20 21 18 19 17 18Eye to Nares Distance 08 09 09 09 08 09Eye Diameter 10 09 12 08 07 07Interorbital Distance 23 23 22 19 20 20Oral Disc Width 25 25 23 22 20 21Tail Length 129 142 162 104 108 123

ReferencesAltig R amp McDiarmid RW (1999) Diversity familial and generic characterizations In McDiarmid RW amp Altig R (Eds)

Tadpoles The Biology of Anuran Larvae University of Chicago Press Chicago pp 295ndash337 Brown JL amp Twomey E (2009) Complicated histories three new species of poison frogs of the genus Ameerega (Anura

Dendrobatidae) from north-central Peru Zootaxa 2049 1ndash38 httpsdoiorg1011646zootaxa204911Costa RC Facure KG amp Giaretta AA (2006) Courtship vocalization and tadpole description of Epipedobates flavopictus

(Anura Dendrobatidae) in southern Goiaacutes Brazil Biota Neotropica 6 (1) httpsdoiorg101590S1676-06032006000100006Duellman (1978) The biology of an equatorial herpetofuna in Amazonian Ecuador University of Kansas Museum of Natural

history Miscellaneous Publications 1ndash352 4 plates

FRENCH ET AL198 middot Zootaxa 4661 (1) copy 2019 Magnolia Press

(Fig 1) The oral disc is small and located anteroventrally (Fig 1) Papillae are laterally emarginated simple and coni-cal absent on middle third of anterior labium Anterior jaw sheath has a medial indentation with serration posterior jaw sheath V-shaped and has serration throughout Lateral processes long extending well past lower jaw sheath Labial tooth row formula (LTRF) is 2(2)3 P-1 and P-2 equal width P-3 shorter (80 of P1 and P2) Nares are oval small without projections and inflections and are located dorsolaterally Eyes are small and oriented dorsolaterally The spiracle is single sinistral and located just before mid-body Lateral lines present on either side of the dorsal midline extending from the nares to the base of the tail Fins are concave and the posterior end is pointed Fins reach maximum height at the last third of the tail the dorsal fin does not extend onto the body The maximum tail height is reached at about mid-length and is as high as body height In preservative the body is dark grey the belly is slightly translucent with digestive tract slightly visible caudal musculature creamy white with small irregular grey flecks and slightly translucent fins In life the body is dark brown with black spots the belly is transparent but slightly pigmented posteriorly digestive tract well vis-ible through skin caudal musculature poorly pigmented and transparent tail fin with melanophores in small and irregular clusters along the tail Ontogenetic variation of 12 characteristics was measured on 6 tadpoles in stages 25ndash30 (Gosner 1960) and minimal inter-tadpole variation was observed (Table 1) Despite the unique habitat distribution and natural history the morphology of the tadpole of Ameerega boehmei ap-pears to be incredibly similar to most other Ameerega species For a detailed discussion of tadpole variation in context of other members of this group see Poelman et al (2010) Schultze et al (2015) and Menin et al (2017)

FIGURE 1 Tadpole of Ameerega boehmei Top to Bottom dorsal lateral and ventral view of tadpole (CBF 7505) Inset illustration of the oral disc from a preserved specimen (CBF 7505 Gosner stage 28) Scale bar = 5 mm

THE TADPOLE OF AMEErEGA BoEhMEI Zootaxa 4661 (1) copy 2019 Magnolia Press middot 199

FIGURE 2 (a) An overview of the habitat for Ameerega boehmei in Serraniacutea de Santiago about 6 km east of Santiago de Chiquitos in Provincia San Joseacute de Chiquitos (b) Habitat where adult males were observed in the small patches of vegetation adjacent to the stream (c) Pool used for tadpole deposition by Ameerega boehmei (d) Adult Ameerega boehmei (e) Arrow points to tadpole of Ameerega boehmei in situ

TABLE 1 Table of tadpole measurements Measurements in mmCBF 7506 CBF 7507 CBF 7505 CBF 7508 CBF 7510 CBF 7509

Gosner Stage 25 25 28 28 28 30Total Length 230 235 268 202 196 210Body Length 101 93 106 98 88 87Maximum Width 56 52 62 44 44 45Depth 44 51 51 44 43 49Internarial Distance 20 21 18 19 17 18Eye to Nares Distance 08 09 09 09 08 09Eye Diameter 10 09 12 08 07 07Interorbital Distance 23 23 22 19 20 20Oral Disc Width 25 25 23 22 20 21Tail Length 129 142 162 104 108 123

ReferencesAltig R amp McDiarmid RW (1999) Diversity familial and generic characterizations In McDiarmid RW amp Altig R (Eds)

Tadpoles The Biology of Anuran Larvae University of Chicago Press Chicago pp 295ndash337 Brown JL amp Twomey E (2009) Complicated histories three new species of poison frogs of the genus Ameerega (Anura

Dendrobatidae) from north-central Peru Zootaxa 2049 1ndash38 httpsdoiorg1011646zootaxa204911Costa RC Facure KG amp Giaretta AA (2006) Courtship vocalization and tadpole description of Epipedobates flavopictus

(Anura Dendrobatidae) in southern Goiaacutes Brazil Biota Neotropica 6 (1) httpsdoiorg101590S1676-06032006000100006Duellman (1978) The biology of an equatorial herpetofuna in Amazonian Ecuador University of Kansas Museum of Natural

history Miscellaneous Publications 1ndash352 4 plates

THE TADPOLE OF AMEErEGA BoEhMEI Zootaxa 4661 (1) copy 2019 Magnolia Press middot 199

FIGURE 2 (a) An overview of the habitat for Ameerega boehmei in Serraniacutea de Santiago about 6 km east of Santiago de Chiquitos in Provincia San Joseacute de Chiquitos (b) Habitat where adult males were observed in the small patches of vegetation adjacent to the stream (c) Pool used for tadpole deposition by Ameerega boehmei (d) Adult Ameerega boehmei (e) Arrow points to tadpole of Ameerega boehmei in situ

TABLE 1 Table of tadpole measurements Measurements in mmCBF 7506 CBF 7507 CBF 7505 CBF 7508 CBF 7510 CBF 7509

Gosner Stage 25 25 28 28 28 30Total Length 230 235 268 202 196 210Body Length 101 93 106 98 88 87Maximum Width 56 52 62 44 44 45Depth 44 51 51 44 43 49Internarial Distance 20 21 18 19 17 18Eye to Nares Distance 08 09 09 09 08 09Eye Diameter 10 09 12 08 07 07Interorbital Distance 23 23 22 19 20 20Oral Disc Width 25 25 23 22 20 21Tail Length 129 142 162 104 108 123

ReferencesAltig R amp McDiarmid RW (1999) Diversity familial and generic characterizations In McDiarmid RW amp Altig R (Eds)

Tadpoles The Biology of Anuran Larvae University of Chicago Press Chicago pp 295ndash337 Brown JL amp Twomey E (2009) Complicated histories three new species of poison frogs of the genus Ameerega (Anura

Dendrobatidae) from north-central Peru Zootaxa 2049 1ndash38 httpsdoiorg1011646zootaxa204911Costa RC Facure KG amp Giaretta AA (2006) Courtship vocalization and tadpole description of Epipedobates flavopictus

(Anura Dendrobatidae) in southern Goiaacutes Brazil Biota Neotropica 6 (1) httpsdoiorg101590S1676-06032006000100006Duellman (1978) The biology of an equatorial herpetofuna in Amazonian Ecuador University of Kansas Museum of Natural

history Miscellaneous Publications 1ndash352 4 plates

FRENCH ET AL200 middot Zootaxa 4661 (1) copy 2019 Magnolia Press

Duellman W (2005) Species Accounts Amphibians In Duellman W (Eds) Cusco Amazoacutenico in The lives of amphibians and reptiles in an Amazonian forest Comstock Publishing Association Ithaca and London pp 183ndash305

Forti LR Mott T amp Struumlssmann C (2013) Breeding biology of Ameerega braccata (Steindachner 1864)(Anura Dendroba-tidae) in the Cerrado of Brazil Journal of Natural history 47 2363ndash2371

httpsdoiorg101080002229332013773099Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification herpetologica 16

183ndash190Haddad CFB amp Martins M (1994) Four species of Brazilian poison frogs related to Epipedobates pictus (Dendrobatidae)

Taxonomy and natural history observations herpetologica 50 282ndash295Lescure J (1976) Etude de deux tecirctards de Phyllobates (Dendrobatidae) P femoralis (Boulenger) et P pictus (Bibron) Bulletin

de la socieacuteteacute Zoologique de France 101 299ndash304Loumltters S Debold P Henle K Glaw F amp Kneller M (1997) Ein neur pfeilgiftfrosch aus der Epipedobates pictus-gruppe

vom osthang der Cordillera Azul in Peruacute herpetofauna 19 25ndash34Menin M Pinto RMC Pegorini RJ amp Silva MR da (2017) Redescription of the tadpole of Ameerega hahneli (Boulenger

1884) (Anura Dendrobatidae) with notes on ontogenetic variations and development habitats South American Journal of herpetology 12 236ndash243

httpsdoiorg102994SAJH-D-17-000521Myers CW amp Daly JW (1979) A name for the poison frog of Cordillera Azul Eastern Peru with notes on its biology and skin

toxins (Dendrobatidae) American Museum Novitates 1ndash24Poelman EH Verkade JC van Wijngaarden RP amp Feacutelix-Novoa C (2010) Descriptions of the tadpoles of two poison frogs

Ameerega parvula and Ameerega bilinguis (Anura Dendrobatidae) from Ecuador Journal of herpetology 409ndash417 httpsdoiorg10167009-0171Prado DE amp Gibbs PE (1993) Patterns of species distributions in the dry seasonal forests of South America Annals of the

Missouri Botanical Garden 902ndash927 httpsdoiorg1023072399937Loumltters S Schmitz A Reichle S Roumldder D amp Quennet V (2009) Another case of cryptic diversity in poison frogs (Den-

drobatidae Ameerega)mdashdescription of a new species from Bolivia Zootaxa 2028 20ndash30 httpsdoiorg1011646zootaxa202812Rodriguez L amp Myers CW (1993) A new poison frog from Manu National Park southeastern Peru (Dendrobatidae Epipedo-

bates) American Museum Novitates 3068 1ndash15Schulze A Jansen M amp Koumlhler G (2015) Tadpole diversity of Boliviarsquos lowland anuran communities molecular identifica-

tion morphological characterisation and ecological assignment Zootaxa 4016 (1) 1ndash111 httpsdoiorg1011646zootaxa401611Silverstone PA (1976) A revision of the poison-arrow frogs of the genus Phyllobates Bibron in Sagra (Family Dendrobatidae)

Natural history Museum of Los Angeles County Science Bulletin 1ndash53 + 2 color platesTwomey E amp Brown JL (2008) A partial revision of the Ameerega hahneli complex (Anura Dendrobatidae) and a new cryp-

tic species from the East-Andean versant of Central Peru Zootaxa 1757 49ndash65 httpsdoiorg1011646zootaxa175713