Biota Neotropica ISSN: 1676-0611
ea@biotaneotropica.org.br Instituto Virtual da Biodiversidade Brasil
Barroso de Andrade, Etielle; Norberto Weber, Luiz; de Souza Almeida Leite, José Roberto Anurans of the Parque Estadual do Mirador, a remnant of Cerrado in the state of
Maranhão, Northeastern Brazil
Biota Neotropica, vol. 17, núm. 4, 2017, pp. 1-12 Instituto Virtual da Biodiversidade
Campinas, Brasil
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Inventory
iot eotropic : e www.scielo.br/bnAnurans of the Parque Estadual do Mirador, a remnant of Cerrado in the state of
Maranhão, Northeastern Brazil
Etielle Barroso de Andrade1, 2, 3*, Luiz Norberto Weber1 & José Roberto de Souza Almeida Leite3, 4 1Universidade Federal do Maranhão, Centro de Ciências Biológicas e da Saúde, Programa de Pós-Graduação em
Biodiversidade e Biotecnologia, Av. dos Portugueses, s/n, Campus do Bacanga, 65085-580, São Luís, MA, Brazil. 2Instituto Federal de Educação, Ciência e Tecnologia do Piauí, Campus Paulistana, BR 407 s/n, Lagoa dos Canudos,
64750-000, Paulistana, PI, Brazil.
3Universidade Federal do Piauí, Núcleo de Pesquisa em Biodiversidade e Biotecnologia, Campus Parnaíba, Av. São Sebastião 2819, 64202-020, Parnaíba, PI, Brazil.
4Universidade de Brasília, Faculdade de Medicina, Área de Morfologia, Campus Universitário Darcy Ribeiro, Asa Norte,70910-900, Brasília, DF, Brazil.
*Corresponding author: Etielle Barroso de Andrade, e-mail: etlandrade@hotmail.com
. . . . . . . . Anurans of the Parque Estadual do Mirador, a remnant of Cerrado in the state of Maranhão, Northeastern Brazil. iot eotropic . : e . http:// . oi. or / . /
Abstract: he err o is one o the ost thre tene bio es in r €il. t is esti te th t •ch o its ori in l ‚e et tion h s been repl ce bƒ so e tƒpe o h• n •se. his is „•ite worrƒin inlƒ in the northern p rt where the n• ber o wil li e inventories is insuf cient and creates the false impression of low diversity in the region. The Parque Estadual do Mirador-PEM, located in the south-central region of the state of Maranhão, presents vegetation typical of the Cerrado biome and corresponds to one o prioritƒ re s or conser‚ tion in the st te. …erein we escribe the species richness n co position o the anurofauna from the PEM and analyze the in uence of different types of vegetation in its formation. Our inventory was con •cte ro ece ber † to ‡ebr• rƒ •sin the cti‚e se rch n • itorƒ cens•s etho s on bree in sites in different water bodies of the park. We recorded 31 anuran species belonging to ve families (species number in parentheses): Leptodactylidae (14), Hylidae (12), Bufonidae (3), Microhylidae (1) and Phyllomedusidae (1). The rarefaction curve and species richness esti tors in ic te th t the s plin e ort w s eno• h to recor ost o the species in the re ion. he richness of anurans in the PEM was higher than reported by other authors for several areas of Cerrado. Most species have a wide distribution in Brazil or are strongly associated with the Caatinga or Amazon biomes. Only about 19% are endemic to the Cerrado biome. This study is the rst to inventory the anurans species of the south-central region of state of Maranhão and pro‚i es i port nt t on phibi n co •nities ro the northern p rt o the r €ili n err o.
Keywords: inventory, Amphibia, Anura, conservation unit, species richness.
Anfíbios anuros do Parque Estadual do Mirador, um remanescente de Cerrado no estado
do Maranhão, nordeste do Brasil
Resumo: O Cerrado é um dos biomas mais ameaçados do Brasil. Estima-se que grande parte da cobertura vegetal original deste bioma tenha sido substituída por alguma forma de utilização humana. Este fato é bastante preocupante, principalmente na porção norte, onde o número de inventários faunísticos é insu ciente e gera a falsa impressão de baixa diversidade na região. O Parque Estadual do Mirador-PEM, localizado na região centro-meridional do Maranhão, apresenta vegetação típica do Cerrado e corresponde a uma das 46 áreas prioritárias para conservação no estado. Aqui, nós descrevemos a riqueza e a composição da anurofauna no PEM, analisando a in uência dos diferentes tipos vegetacionais na sua formação. Inventariamos a anurofauna de dezembro de 2013 a fevereiro de 2015, utilizando métodos de procura ativa e censo auditivo em sítios reprodutivos de diferentes corpos d’água do parque. Registramos 31 espécies de anuros, pertencentes a cinco famílias (números de espécies entre parênteses): Leptodactylidae (14), Hylidae (12), Bufonidae (3), Microhylidae (1) e Phyllomedusidae (1). A curva de rarefação e os estimadores de riqueza indicaram que o esforço amostral foi su ciente para registrar a maior parte das espécies da região. A riqueza de anuros no PEM foi maior que a registrada por outros autores em diversas áreas de Cerrado. A maioria das espécies possuem ampla distribuição no Brasil ou são fortemente associadas aos biomas Caatinga ou Amazônia. Somente cerca de 19% são endêmicas do bioma Cerrado. O presente trabalho representa o primeiro estudo a inventariar as espécies de anfíbios anuros na região Centro-Sul do Maranhão e fornece dados importante sobre as comunidades de anfíbios da porção norte do Cerrado brasileiro.
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Introduction
he err o is the secon l r est bio e in r €il co‚erin bo•t „• rter of national territory, and extends from the state of Paraná to northern of the state of Maranhão ( ibeiro lter incl in tr nsition areas in the state of Piauí. Despite its great extension, it is believed that ore th n h l o the re s ori in ll occ pie b this bio e h e been lost in recent e rs e to ncontrolle h n occ p tion n rib siness e p nsion Klink & Machado 2005 .
Except for Pampas biome, the Cerrado biome borders with all other Brazilian biomes, forming ecotonal areas of mutual in uence. This mutual in uence added to the historical, climatic and geomorphological processes il tes re responsible or the or tion o co ple os ic of phytophysionomies, ranging from open elds ( elds or savannas) to orest or tions ibeiro lter . hese ctors contrib te to the or tion o i erent t pes o icroh bit ts llowin coe istence o species with different ecological niches, placing the Cerrado biome as holding 5% of the ni ls n pl nts in the worl n cco ntin or bo t one thir o r ili n bio i ersit r sil . rther ore hi h r tes o en e is n hi h le el o thre t e this bio e one o bio i ersit hotspots or conser tion priorities. espite the lob l reco nition o biolo ic l i port nce n conser tion priorities o the err o conser tion nits protect only 9.4% of its area (IBAMA 2009 n t le st species o
ni ls re c rrentl t e tinction ris MMA 2014 .
The state of Maranhão has about 65% of its territorial extension co ere b the err o bio e €• ‚ which correspon s to l ost ƒ n h s one o the best„preser e err o re s o the northern portion o the bio e bein consi ere n i port nt priorit re or bio i ersit conser tion ini „ ilho et l. b . he st te h s lso l r e ecotone re s tr nsitions between … on„ err o or tions n err o„ tin cre tin ecolo ic l corri ors with hi h potenti l or species en e is rreto il et l. b t th t re rarely considered in environmental policy de nitions. Furthermore, the Brazilian Ministry of the Environment (Ministério do Meio Ambiente), through Ordinance No. 09 from 27 January 2007, established actions for
the i ple ent tion o priorit re s or bio i ersit conser tion o the Brazilian biomes, and identi ed 46 priority areas for conservation in the state of Maranhão, 28 of them of extremely high priority (MMA 2007 .
…ltho h o re t i port nce or bio i ersit conser tion st ies in the northern p rt o the r ili n err o re r in phibi n communities are still insuf cient, mainly in the state of Maranhão rreto et l. r sileiro et l. …n r e which cre tes lse i pression o low species i ersit in the re ion ini „ ilho et l. . The south-central portion of Maranhão, which encompasses the northern sector o the err o bio e h s l r e priorit re s or n l in entor MMA 2007 especi ll b presentin nowle e ps on rio s t ono ic ro ps which rther rein orces the nee to obt in b sic in or tion bo t anuran fauna in the region. Moreover, this region is located in an important Brazilian ecotone, which suffer strong in uence of the other biomes, as s ch … oni n tin .
n this scen rio n l in entories re i port nt tools to collect in or tion on the biolo n species richness pro i in b sic re† ire ents or e elop ent o ecolo ic l o els necess r or the option o e ecti e conser tion e s res €otelli olwell . rther ore the const nt i p ct on phibi n pop l tions c se b the intense nthropic cti ities in the err o bio e rein orces the nee or t ono ic in entories Ribeiro-Júnior & Bertoluci 2009 . here ore this st i s to inventory the anuran fauna of the Parque Estadual do Mirador-PEM, n i port nt re n nt o err o en iron ent in the northern portion o the err o bio e ‡orthe stern r il.
Material and Methods
1. Study area
The Parque Estadual do Mirador (PEM) is located in the central-meriodional region of the state of Maranhão (06º10’- 06º42’ S and 44º43’- 45º54’ W, ‚ sl € ‚ t r il between the he w ters o the t pec r n …lperc rt s ri ers i re n enco p sses the nicip lities o
Figure 1. Map featuring the Parque Estadual do Mirador (PEM), state of Maranhão, Northeastern Brazil (in green). On the left, northernmost Brazilian areas of the
Cerrado biome, in gray; in the upper-right corner, sampling areas (A-B) within the park; underneath: A - Geraldina’s advanced checkpoint (P1-P6), B - Zé Miguel’s advanced checkpoint (P7).
Anurans of the Parque Estadual do Mirador-MA Biota Neotrop. ‚ : e ƒ ƒ
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Mirador, Formosa da Serra Negra and Fernando Falcão. Created in 1980 by State Decree nº. 641 of June 20, the PEM has the Cerrado sensu lato s pre o in nt e et tion Conceição & Castro 2009 on re „ ellow l tosols ssoci te with † rt s n s n lithic soils ston n roc . ith n initial area of 700,000 ha, the PEM was expanded by Law nº. 8.958 of May 8, 2009, having now a total area of 766,781.00 ha (Maranhão 2009 . he cli te is w t pe tropic l s b h i r with nn l r in ll n er e te per t res r n in ro . to lc nt r .
e s ple se en points istrib te between two re s. he re (advanced monitoring station Geraldina) has six sampling points: P1 - permanent pond amidst the riparian forest; P2 - temporary pond with large amounts of aquatic vegetation inside; P3 - temporary pond in an open eld; P4 - permanent stream in dirty eld area with presence of spaced trees; P5 - permanent stream amidst the gallery forest; P6 - permanent stream in open area. The area B (advanced monitoring station Zé Miguel) has only one sampling point: P7 - swamp area, located near the banks of the Rio t pec r see et ils in ble . he s ple sites presente i erent t pes o e et tion r in ro r ssl n s to re s o l r e trees n p l trees i re .
2. Data collection
Were conducted, bimonthly, eight eld expeditions in each sampling area ro ece ber to ebr r co prisin both r in n r se sons. e se two s plin etho s: cti e is l se rch n itor cens s in i erent icroh bit ts se b ro s e er et l. . hese etho s are inexpensive and considered the most ef cient to record the largest species n ber in the shortest ti e l €o et l. . hree rese rchers carried out eld activities for three consecutive days, starting around 6 p.m n en in t p. res ltin in s plin e ort o ho rs/person. rther ore opport nistic recor s o oc li• tions or in i i ls o n o tsi e s plin points were incl e in the list o species.
Identi cation of specimens were carried out through vocalization and/or co p rison with speci ens ho se t the erpetolo ic l ollection o the Universidade Federal do Maranhão and Delta do Parnaíba Zoological Collection housed at the Universidade Federal do Piauí, Campus Parnaíba, Piauí, Brazil. Voucher specimens (Appendix 1) were collected under permit granted by “Secretaria de Estado do Meio Ambiente e Recursos Naturais do Maranhão” (SEMA-MA #008/2013) and were deposited at the Delta do Parnaíba Zoological Collection (CZDP I1). No collected species is listed on the ‚r •ili n list o hre tene ƒpecies MMA 2014 . he species
istrib tion n t „ono ic rr n e ent ollow rost … .
3. Data analysis
We evaluated the ef ciency of anuran sampling methods in the PEM ro sin in i i l b se cc l tion c r es †otelli ‡ olwell . e c lc l te the e„pecte species richness sin the nonp r etric esti tors ˆ c‰ni e n ‚ootstr p Magurran 2004 . he n l sis w s per or e in Šsti teƒ so tw re .‹. . with r n o i• tions olwell Œ .
To compare the anuran species composition of PEM with studies per or e in re s o err o n in other bio es •on tl ntic orest Caatinga and Pantanal), we performed a hierarchical cluster analysis using the unweighted pair-group method with averaging (UPGMA) (Magurran . his n l sis opti i•es intr ro p ho o eneit cl sterin the ost si il r s ples i erent loc lities b se on the species co position si il rities ƒil et l. . he st ies were chosen r n o l or according to the proximity to the PEM, and only six studies per biome were selecte . espite the isp rities between t pes o en iron ents n s plin etho s ener te i erence in the n r n species co position Pombal Jr. 1995 n the rbitr r chose o st ies to insert bi s in our comparisons, the analysis was performed to demonstrate in uence of other biomes on the anuran species composition of the PEM. We used the ˆ cc r si il rit in e„ Magurran 2004 to constr ct the si il rit tri„ b se in presence n bsence tri„ with ‹ n r n species. o re ce i erences c se b t „ono ic proble s we e„cl e ro tri„ the species without speci c identi cation (“gr.”, “aff.” and “sp.”), considering only species with identi cation to be con rmed (“cf.”). The cluster analysis was performed on the software Past 3.06 ( er et l. .
t ro n r n co position w s t ‰en ro the ollowin st ies c rrie o t in i erent re ions o ‚r •il: Cerrado • ƒerr o † o ‚r o ƒ†‚ Maranhão (‚ rreto et l. …), Tocantins river basin, southwestern Maranhão ‚r sileiro et l. ‹), Parque Nacional das Emas-PNE, Goiás (Žopp et l. ), Estação Ecológica Serra Geral do Tocantins-EESGT, Tocantins and ‚ hi l €o et l. ), Estação Ecológica Uruçuí-Una-EEUU, Piauí l echio et l. ), Piracanjuba and Peixe river basins, southeastern Goiás (ƒ ntos et l. • Caatinga – Boa Vista and São João do Cariri, Paraíba ( ieir et l. …), Planalto da Ibiapaba, Ceará (•oeb nn ‡ ), Chapada do Araripe, Ceará (‘ibeiro et l. ), Estação Ecológica Raso da Catarina-EERC, Bahia († r et l. lh †r n e Delta do Rio Parnaíba, Piauí ( n r e et l. ), Parque Nacional do Catimbau-PNC, Pernambuco (Pedrosa et al. 2014 • Amazon • ‘eser c‰e •on s •i et l. ‘eser Š„peri ent l t b ‘Š cre ƒo • et l. ‹), Altamira, Pará (Žnispel ‡ ‚ rros ‘io Preto da Eva, Amazonas ( lh ‡ i„o ‘eser Š„tr ti ist o ‘io Gregório-RERG, Amazonas (Pantoja & Fraga 2012), Querência, Mato Grosso
Table 1. Environmental description of the sampled habitats of the Parque Estadual do Mirador (PEM), south-central region of the state of Maranhão, Northeastern Brazil. Sampled habitats Coordinates Description
P1 45°52’44.00” W6°37’49.60” S • r e pon s rro n e b e ie et tion within the pon . to l r e trees n the presence o ’ tic wee s n s ll isl n s or e b e er ent P2 45°50’32.0” W6°36’10.6” S ƒn ’ tic e et tion within the w ter.ll pon s rro n e b sp ce e et tion ew trees n n herb ceo s pl nts with l r e o nt o herb ceo s P3 45°50’29.58” W6°36’27.65” S Pond formed in a ooded eld, located in a spaced arboreal vegetation area, with little shrub vegetation inside. P4 45°49’1.50” W6°36’13.30” S Stream located in a “campo sujo” (grassland with sparse shrubs) area. The marginal vegetation is shrub type with opened re s n e er ent e et tion.
P5 6°36’37.30” S
45°47’59.20” W
Stream within the gallery forest, with the presence of large palm trees. It features at edge and soaked in much of its len th n cc l tion o le litter on the ro n .
P6 45°46’43.90” W6°36’34.20” S Stream within an opened eld area with the presence of some palm trees. The marginal vegetation is formed by herbaceous pl nts. P7 45°28’25.10” W6°47’28.20” S Flooded eld formed periodically during the rainy season, presenting a large extension and covered by emergent vegetation n ew trees irl sp ce .
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‚it r et l. • Atlantic Forest – Área de Preservação Permanente Mata do Buraquinho-APPMB, Paraíba (ƒ nt n et l. ‹), Reserva Ecológica Rio das Pedras-RERP, Rio de Janeiro ( r lho e ƒil et l. ‹ ƒerr do Ouro Branco-SOB, Minas Gerais (São Pedro & Feio 2011), Parque Estadual Carlos Botelho-PECB, São Paulo ( orl ni et l. ), Jequié, ‚ hi ƒil et l. ‘eser e ƒerr ‚onit ‘ƒ‚ ‚ hi i s et l.
• Pantanal – Corumbá, Mato Groso do Sul ( il erreir Serras do Entorno do Pantanal Sul-SEPS, Mato Groso do Sul ( or o
pos ), Estação Ecológica Nhumirim-EEN, Mato Grosso do Sul or o pos ), Parque Nacional da Serra da Bodoquena-PNSB, Mato Groso do Sul ( et n b ro et l. ), Fazenda Baía da Pedra-FBP, Mato Grosso (Pansonato et al. 2011 .
Results and Discussion
e recor e species o n r n phibi ns istrib te in ener and ve families (species number in paretheses): Leptodactylidae (14), Hylidae (12), Bufonidae (3), Microhylidae (1) and Phyllomedusidae (1)
ble i re . ro this tot l species h their occ rrence recor e ro is l enco nters n two species Elachistocleis sp. n Boana boans were onl recor e thro h oc li tion. wo species Leptodactylus petersii n L. mystaceus were is ll obser e outside the sampled points. Among the species recorded in the PEM, 80.6% (n = 25) were considered as least concern (LC) according to IUCN e €ist te ories n riteri • ‚ . he € c te or incl es generalist and abundant species not quali ed in another category (Critically ƒn n ere ƒn n ere „ lner ble or ‚e r hre tene • ‚ . Pseudopaludicola canga n P. jaredi present de cient data (DD) due the l c… o ppropri te in or tions on their b n nces istrib tions n ecolo ic l re† ire ents • ‚ . onser tion st t s w s not pro i e or Dendropsophus sp. Scinax . ruber Adenomera sp. n Elachistocleis sp. since they were not identi ed at the speci c level ( ble . onsi erin the in i i ls n ber we recor e tot l o ‡ ini i ls which Scinax fuscomarginatus (n = 83; 9.30%), Boana multifasciata (n = 76; 8.52%) and Dendropsophus rubicundulus (n = 68; 7.62%) were
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the most abundant species, accounting for 25.45% of the total number of s ple in i i ls i re .
Out of 31 recorded species, 19.3% are endemic to Cerrado, 29% are istrib te in t le st one o the other bio es inl in the tin and Amazon biomes, and 41.9% of them have wide distribution in Brazil „ l ‹o et l. rost . Œll species h e pre io s recor s or the state of Maranhão. Recently, three endemic species of the Cerrado hitherto nrecor e or the st te h their eo r phic l istrib tions e‰ten e ntil the limits of the PEM: A. saci Araújo et al. 2015 L. sertanejo €i et l. n P. jaredi Œn r e et l. ˆ . e recor e these species calling under dense vegetation in a ooded eld covered by emergent e et tion loc te ne r the b n…s o the io •t pec r within t pic l Cerrado area (sampling point P7). Pseudopaludicola jaredi w s recentl escribe bein c rrentl reco ni e three isol te pop l tions in the st tes of Ceará, Rio Grande do Norte and Maranhão (Œn r e et l. ˆ b
occ rrin s ntopic ll with P. canga in the PEM (Œn r e et l. ˆ . •n this c se the e elop ent o st ies to ccess the ct l istrib tion
n conser tion st t s o this species is i port nt.
The anuran fauna of the PEM consists for the most part by species t pic l o open or tions err o tin h co co ple‰ n o ten o n in the err o bio e „ l ‹o et l. rost ). Our results s pport other st ies con cte in err o re s Šr sileiro et l. ‡ Oda et al. 2009 oberto et l. • l „echio et l. Ž ntoro & Brandão 2014 Dória et al. 2015), which af rm that the amphibian co nities re o in nte b toler nt n ener list species. •owe er we recor e lso t pic l species o oreste re s s Osteocephalus taurinus
n B. boans co on species in rip ri n orests o the err o n the Œ on bio es €i et l. • n er et l. Matavelli et al. reit s et l. . Boana boans w s restricte to the Œ on Š sin b t Matavelli et al. (2013) recorded the rst occurrence of this species
Table 2. Anurans recorded in the Parque Estadual do Mirador (PEM), municipalities of Mirador, Formosa da Serra Negra and Fernando Falcão, state of Maranhão,
Northeastern Brazil. Sampling points: P1 - P7 (see point characterization in Material and Methods); *Record of specimens outside the respective sampling point. Habitat: A - open formations, F - forest formations. Geographic distribution: CAM - species occurring in the Cerrado and Amazon biomes; CC - species recorded in the Cerrado n tin bio es ƒ en e ic to the err o bio e wi e istrib tion. Ž plin etho : Œ Œco stic „ „is l. ‚ n ber o in i i ls recor e . ‚ ber of species per family in parentheses. CS - Conservation status of the species classi ed according to IUCN: LC - least concern, DD - data de cient.
Taxon Samp. point Habit. Geogr. dist. Samp. method N CS BUFONIDAE (3)
Rhinella jimi Žte ‰ P1, P5, P6 Œ Œ/„ €
Rhinella mirandaribeiroi ll r o ˆ P2*, P6 Œ Œ/„ €
Rhinella ocellata nther P2 /
HYLIDAE (12)
Dendropsophus branneri ochr n P1, P2 /
Dendropsophus minutus (Peters, 1872) P1-P3 /
Dendropsophus rubicundulus einh r t t en P2, P3, P5 /
Dendropsophus soaresi r schi i P3, P5 /
Dendropsophus sp. P1, P7* /
Boana boans inn e s P2*, P7 CAM
Boana multifasciata nther P1, P2, P4-P7 / CAM /
Boana punctata chnei er P1, P2, P4-P7* / / €
Osteocephalus taurinus tein chner P1, P5 CAM /
Scinax fuscomarginatus t• P1-P3 /
Scinax nebulosus pi‚ P1, P2, P4-P6 / CAM / €
Scinax ƒƒ. ruber P3, P5, P7 /
LEPTODACTYLIDAE (14)
Adenomera hylaedactyla ope P2, P3, P6 / CAM / €
Adenomera saci r„ lho i rett € P7 /
Adenomera sp. P1*, P6, P7 /
Leptodactylus fuscus chnei er P2-P5 /
Leptodactylus mystaceus pi‚ P1*
Leptodactylus petersii tein chner P5 CAM
Leptodactylus sertanejo i rett ost €€ P7 /
Leptodactylus troglodytes t• P3 /
Leptodactylus vastus t• € P3, P5
Physalaemus centralis …o er nn P3, P6 /
Physalaemus cuvieri it•in†er P3, P5 /
Pseudopaludicola canga i rett ‡o b €€ P1, P2, P5, P7 CAM / ˆˆ
Pseudopaludicola jaredi Andrade, Magalhães, Nunes-de-Almeida,
Veiga-Menoncello, Santana, Garda, Loebmann, Recco-Pimentel, i rett ‰ole o €
P7 / ˆˆ
Pseudopaludicola mystacalis ope P1, P3, P5 /
MICROHYLIDAE (1)
Elachistocleis sp. P5, P7
PHYLLOMEDUSIDAE (1)
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in Cerrado areas in the state of Maranhão. Recently, reit s et l. € recorded the presence of this species in the REBIO Gurupi, a Biological Reserve of the Amazon biome in the northwestern Maranhão. We present here the thir recor oƒ B. boans in the state of Maranhão, lling the distribution gap between the REBIO Gurupi region and the municipality of Mata Roma (Matavelli et al. 2013 reit s et l. € . ‰his in ic tes th t this species h s wi e istrib tion in ƒorest re s in the •on n err o bio es. ‹n ition we present the secon recor oƒ Rhinella ocellata for the state of Maranhão, lling a distribution gap between its rst occurrence in the northeast region of the state (Matavelli et al. 2014 and its closest record in the Estação Ecológica Uruçuí-Una, state of Piauí
ˆ l echio et l. € .
‰he cc l tion c r„e presente stron† ten encŒ tow r s st bili• tion i† re in ic tin† th t the etho s se herein were eƒƒecti„e to s ple
large part of the PEM species. Furthermore, according to the estimators se it is e‚pecte the ition oƒ onlŒ two species on obser„e richness (observed richness = 31 ± 0.79; Jacknife 1 = 33.95 ± 1.67; Bootstrap = 33.34). The species richness of PEM was higher than that reported by other authors in iƒƒerent re s oƒ the …r •ili n err o: … rreto et l. €€ • spp. il„ eite et l. €€ • spp. Oda et al. (2009• spp. ‡opp et l. € €• spp. r Žo l ei ntos € • spp. ˆ l echio et l. € • spp. n Dória et al. (2015• spp. n • ite si il r to the n ber oƒ species obser„e bŒ l Žo et l. €€ • spp. in the municipality of São Desidério, Western Chapadão region of the state of … hi ee ‰ ble ƒor co p rison between the iƒƒerent loc lities oƒ the err o . … rreto et l. €€ h s reporte the presence oƒ onlŒ ƒro† species in st Œ on the n r n ƒ n oƒ the err o o …r „o i„er Basin Balsas, state of Maranhão, neighboring region to the PEM.
Figure 3. Anurans recorded in the Parque Estadual do Mirador (PEM), state of Maranhão, Northeastern Brazil. In parentheses, the institutional registration number and
the speci en sno t „ent len†th ƒor e ch „o chere speci en. Rhinella jimi n„o chere speci en • … R. mirandaribeiroi (CZDP I1 520; SVL 55.63 mm); R. occelata (CZDP I1 521; 40.70 mm); D - Dendropsophus braneri (CZDP I1 604; SVL 16.46 mm); E - D. minutus (CZDP I1 533; SVL 22.61 mm); F - D. rubicundulus (CZDP I1 535; SVL 21.65 mm); G - D. soaresi (CZDP I1 625; SVL 32.07 mm); H - Dendropsophus sp. (CZDP I1 607; SVL 19.97 mm); I - Boana multifasciata (CZDP I1 525; SVL 44.72 mm); J - B. punctata (CZDP I1 529; SVL 29.79 mm); K - Osteocephalus taurinus (CZDP I1 615; SVL 71.29 mm); L - Scinax fuscomarginatus (CZDP I1 532; SVL 22.76 mm); M - S. nebulosus (CZDP I1 611; SVL 26.82 mm); N - Scinax ƒƒ. ruber (CZDP I1 539; SVL 39.59 mm); O - Adenomera hylaedactyla (CZDP I1-613; SVL 16.98 mm); P - A. saci (CZDP I1 456; SVL 23.05 mm).
Anurans of the Parque Estadual do Mirador-MA Biota Neotrop. : e € € € €
http:// ‚. oi.or†/ €. €/ € …Š € € € http://www.scielo.br/bn
Figure 4. Anurans recorded in the Parque Estadual do Mirador (PEM), state of Maranhão, Northeastern Brazil. See caption of the gure 3 ƒor ition l inƒor tion. Adenomera sp. (CZDP I1 537; SVL 18.42 mm); B - Leptodactulus fuscus (CZDP I1 541; SVL 37.79 mm); C - L. mystaceus (CZDP I1 543; SVL 44.42 mm); ˆ L. petersii (CZDP I1 627; 42.88 mm); E - L. sertanejo (CZDP I1 544; 48.77 mm); F - L. troglodytes (CZDP I1 545; SVL 47.48 mm); G - L. vastus (CZDP I1 547; € . • • Physalaemus centralis (CZDP I1 562; SVL 34.79 mm); I - P. cuvieri (CZDP I1 564; SVL 27.09 mm); J - Pseudopaludicola canga (CZDP I1 548; . • ‡ P. jaredi (CZDP I1 624; SVL 16.63 mm); L - P. mystacalis (CZDP I1 554; SVL 14.89 mm); M - Pithecopus azureus (CZDP I1 560; SVL 31.04 mm).
Figure 5. Relative abundance of anuran species in the Parque Estadual do Mirador (PEM), state of Maranhão, Northeastern Brazil. The total number of recorded
in i„i ls is in ic te bo„e e ch col n. n r n species: Ž Rhinella jimi• R. mirandaribeiroi• o R. occelata• ˆb Dendropsophus braneri• ˆ D. minutus• ˆr D. rubicundulus• ˆs D. soaresi• ˆsp Dendropsophus sp.• …b Boana boans• … B. multifasciata• …p B. punctata; Ot - Osteocephalus taurinus• ƒ Scinax
fuscomarginatus• n S. nebulosus• r Scinax ƒƒ. ruber• h Adenomera hylaedactyla• s A. saci• sp Adenomera sp.• ƒ Leptodactulus fuscus• L. mystaceus• p L. petersii• s L. sertanejo• t L. troglodytes• „ L. vastus; Pc - Physalaemus centralis; Pcu - P. cuvieri; Pca - Pseudopaludicola canga; Pj - P. jaredi• Pm - P. mystacalis• sp Elachistocleis sp.; Pa - Pithecopus azureus.
n r e .…. et l.
Biota Neotrop. : e € € € €
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„en in other en„iron ent l protecte re s the species richness w s lower th n th t obser„e in this st Œ s ch s the st ies c rrie o t in the Parque Estadual Terra Ronca, state of the Goiás ( il„ eite et l. €€ in the Parque Nacional da Emas, state of Goiás (‡opp et l. € € n in the Estação Ecológica Uruçuí-Una, state of Piauí (ˆ l echio et l. € in which were recor e n phibi n species respecti„elŒ. Our results support the idea that the low anuran diversity of the northern Cerrado biome re ects the small number of studies in these areas ˆini• ilho et l. €€ €€ • l Žo et l. € . ‹n ition it is evident the importance of PEM in terms of anuran diversity if compared to other re s oƒ the …r •ili n err o.
On the other hand, increasing the sampled areas the number of species ten s to incre se s obser„e bŒ …r sileiro et l. €€ n Melo et al. € which recor e n species respecti„elŒ in st ies c rrie o t in various sampling sites in the states of Maranhão and Goiás. ntos et l. € re†istere € species oƒ phibi ns in nicip lities oƒ the Piracanjuba and Peixe rivers basins in the southeast of Goiás. In the same w Œ lon† ter st ies con cte to etect s ll sp tio te por l „ ri tions in the species co position between en„iron ents oƒ s e re†ion en ble the re†istr tion oƒ †re ter species n ber n llows eter inin† the
ct l species richness in the s ple en„iron ents l Žo et l. €
b le et l. € . ‹n ition the se oƒ se„er l collection etho s is critic l to ens re the re†istr tion oƒ species with iƒƒerent repro cti„e beh „iors n /or iƒƒerent h bits terrestri l „s. rbore l „s. • tic h bits .
…Œ st Œin† the n r n ƒ n oƒ n ere‚plore re s it is possible to nd new species occurrences or even new species. Furthermore, it is s l to recor species with t ‚ono ic proble s s ch s the species oƒ the †en s Scinax. In the PEM, we recognized at least two species pop l tions closelŒ rel te to S. ruber b t to pre„ent ƒ t re t ‚ono ic proble s we opte here ore conser„ ti„e position reco†ni•in† the onlŒ s Scinax ƒƒ. ruber s opte bŒ other thors e.†. l Žo et l. € ˆ l echio et l. € oberto et l. € n r e et l. € . i il rlŒ co stic iƒƒerences between species oƒ the †en s Elachistocleis are almost undetectable to human ear, which prevented the identi cation of the species from this genus in the PEM because they were recorded only bŒ their „oc li• tions n bec se there is the possibilitŒ th t occ r t le st three species in re†ion: E. piauiensis E. carvalhoi n E. bumbameuboi
r schi € € . rther ore we belie„e th t Dendropsophus sp. n Adenomera sp. re still n escribe species bein† this l tter orpholo†ic llŒ si il r to pop l tion s ples obt ine in se„er l re s oƒ the err o n tin† bio es e.†. oeb nn • € € ˆ l echio et l. € oberto et l. € .
Figure 6. Accumulation curves for anurans sampled in the Parque Estadual do Mirador (PEM), state of Maranhão, Northeastern Brazil, based on the number of individuals
representin† the obser„e obs n esti te species richness …ootstr p n c niƒe . r„es constr cte ƒro € €€€ r n o i• tions.
Table 3. Localities with amphibian inventories in the Cerrado biome, including the Parque Estadual do Mirador (PEM). Spp. - Number of species; SE - sampling
effort (days/month); NS - number of sampling sites; SM - sampling method (1 - interception and pitfall traps, 2 - sampling in breeding site; 3 - active search; 4 - casual encounter); DP - distance in kilometers from PEM.
Localities Spp. SE
(days/month) NS SM
DP
(Km) Reference
Balsas-MA €/ … rreto et l. €€
Parque Estadual de Terra-Ronca-GO / € il„ eite et l. €€
‹n† •eir r … €/ € € Dória et al. (2015)
Parque Nacional das Emas-GO / €€ ‡opp et l. € €
Estação Ecológica Uruçuí-Una-PI / € ˆ l echio et l. €
Estação Ecológica de Assis-SP / € r Žo l ei ntos €
Municipality of Niquelândia-GO / € Oda et al. (2009)
Parque Estadual do Mirador-MA 31 24/8 7 2, 3, 4 - Present study
São Desidério-BA / € l Žo et l. €€
Southeast of Maranhão / € …r sileiro et l. €€
Estação Ecológica Nova Roma-GO €/ €€ pos †e €
Estação Ecológica Serra Geral do
Tocantins-TO/BA €/ € l Žo et l. €
Anurans of the Parque Estadual do Mirador-MA Biota Neotrop. : e € € € €
http:// ‚. oi.or†/ €. €/ € …Š € € € http://www.scielo.br/bn
Figure 7. Similarity (Jaccard index and clustering method “UPGMA”; cophenetic correlation coef cient = 0.8841) among the anuran species composition of the
Parque Estadual do Mirador (PEM), state of Maranhão, Northeastern Brazil, and 24 Brazilian locaties distributed in the following biomes: Amazon DCKE eser„ ˆ c e• REC eser„ ‚peri ent l t b • ALTA lt ir • RPEV - Rio Preto da Eva; RERG - Reserva Extrativista do Rio Gregório; QCIA - Querência); Caatinga
CARI - Boa Vista e São João do Cariri; IBPA - Planalto da Ibiapaba; ARAR h p o r ripe• EERC - Estação Ecológica Raso da Catarina; IGRA ‹lh r n e Piauí; PNC - Parque Nacional do Catimbau); Cerrado SOMA - Bacia do Rio Tocantins, Sudoeste do Maranhã; SGB err o o …r „o• PNE - Parque Nacional das s• EESGT - Estação Ecológica Serra Geral do Tocantins; EEUU - Estação Ecológica Uruçuí-Una; SDGO - Bacia dos Rios Piracanjuba e Peixe, Sudeste de Goiás;
PEM - Parque Estadual do Mirador); Atlantic Forest PPMB - Área de Preservação Permanente Mata do Buraquinho; RERP - Reserva Rio das Pedras; SOB err o
Ouro Branco; PECB - Parque Estadual Carlos Botelho; JQUI - Jequié; RSB eser„ e err …onit • n Pantanal CRBA - Corumbá; SEPS err s e ntorno o Pantanal Sul; EEN - Estação Ecológica Nhumirim; PNSB - Parque Nacional da Serra da Bodoquena; FBP - Fazenda Baía de Pedra.
l ster n lŒsis e„i ence iƒƒerences in species co position between the different biomes, revealing similarities lower than 30% in most of the co p risions i† re ). Despite the anuran community of PEM be co pose lso bŒ species occ rrin† in other tŒpes oƒ en„iron ents we obser„e the †ro pin† oƒ st ies c rrie o t in the err o bio e. The anuran species composition of the PEM presented a greater similarity with the study conducted in the Estação Ecológica Uruçuí-Una-EEUU ˆ l ecchio et l. € ), located about 250 km in the southwest Piauí,
n to the st Œ con cte in err o o …r „o loc te bo t in municipality of Balsas, southern state of Maranhão. Out of 26 species of anurans recorded in the EEUU, about 60% (16 species) (D. minutus D. rubicundulus D. soaresi B. multifasciata O. taurinus Pithecopus azureus S. fuscomarginatus L. fuscus L. petersii L. troglodytes L. vastus Physalaemus centralis P. cuvieri R. jimi R. mirandaribeiroi n R. ocellata were also common to the PEM. Six species (D. nanus Trachycephalus typhonius Rhaebo guttatus R. veredas Dermatonotus muelleri n E. carvalhoi) were exclusive to the EEUU. Out of 23 species recorded in the Serra do Gado Bravo, about 48% (11 species) were also present in the PEM n in the ‘‘ D. minutus D. rubicundulus B. multifasciata L. fuscus L. petersii L. vastus P. cuvieri R. jimi R. ocellata R. mirandaribeiroi n P. azureus . e„en other species were e‚cl si„e to err o o …r „o
R. margaritifera B. albopunctata B. raniceps D. nanus D. walfordi Barycholos ternetzi n E. piauienseis .
ltho †h this hŒpothesis h s not been teste we belie„e th t the similarity pattern among the PEM, SGB and EEUU could be explained by bio†eo†r phic historic l n cli tic ƒ ctors th t res lte in the ƒor tion oƒ si il r „e†et tion tŒpes olli et l. €€ . ‰he three protecte re s re located in high and steep areas of inter uvial, forming extensive gallery ƒorests in r ine re s Conceição & Castro 2009 ˆ l ecchio et l. € th t llows ispl ce ent oƒ species between p tches oƒ „e†et tion o ri† es €€ ƒ „orin† species co position si il ritŒ on† these areas. Additionaly, the PEM presents several types of vegetation formations (typical cerrado, cerradão, veredas, dirty elds, ooded elds, open elds and riparian forests) and is inserted in the Uruçuí-Mirador biodiversity corridor, which c n e‚pl in the †re t species richness n species co position. The Uruçuí-Mirador corridor, still in the implementation phase, has an esti te initi l re oƒ bo t . illion hect res istrib te on† the states of Piauí, Maranhão and Tocantins (Conceição & Castro 2009 ˆ l ecchio et l. € .
e lso obser„e the occ rrence oƒ tŒpic l species ƒro other bio es within the PEM, such as B. boans n P. canga tŒpic l species oƒ the •on bio e n L. troglodytes n L. vastus tŒpic l species oƒ
n r e .…. et l.
€ Biota Neotrop. : e € € € €
http://www.scielo.br/bn http:// ‚. oi.or†/ €. €/ € …Š € € €
the Caatinga biome). This pattern of species composition in the PEM is co onlŒ obser„e in st ies oƒ n r ns ƒro the err o bio e
‘et n b ro et l. €€ …r sileiro et l. €€ l Žo et l. €€ € ˆ l echio et l. € n co l be res lt oƒ its loc tion in the re†ion of Chapadas do Alto Itapecuru. This region receives the in uence from ele ents oƒ the •on n tin† bio es e.†. „e†et tion cli te hŒ ro†r phŒ soil which ƒor s os ic oƒ connecte „e†et tion th t en bles possible e‚ch n†e oƒ species between nei†hborin† re s ne €€ . In this case, PEM is located in a transition zone (humid vs. semiarid) and the sp ti l rr n†e ent oƒ h bit t p tches pro„i es corri ors ƒor possible
ispers l on† the ne rbŒ wetl n s Maltchik et al. 2008 .
Our research is one of the few studies to inventory the amphibians’ species of south-central region of the state of Maranhão. It also provides important data about the amphibian communities of the PEM, which can contribute to implementation of management plan for the PEM and the ƒor e„elop ent oƒ conser„ tion e s res oƒ the phibi ns’ species in the northern p rt oƒ the …r •ili n err o. ˆespite the obser„e species richness we belie„e th t the n ber oƒ species is e„en †re ter since the PEM has several not yet sampled environments and the methods adopted here o not incl e ƒossori l species re†istr tion or repro cti„e h bits oƒ the e‚plosi„e tŒpe. ‰h s there is nee to con ct ƒ t re s r„eŒs to i pro„e the nowle †e ent bo t the i„ersitŒ n istrib tion oƒ n r ns in this i port nt re in the Šorthe stern …r •il. ‹n ition ƒ rther ecolo†ic l st ies re nee e to n erst n the species richness pattern and the dynamics of PEM’s amphibian populations, as these data re essenti l ƒor the i ple ent tion oƒ e s res ƒor species conser„ tion. ‹n ƒ ct sŒste tic st ies on conser„ tion pl nnin† re e‚tre elŒ r†ent in the re†ion bec se oƒ the thre t i pose bŒ †ric lt r l e‚p nsion in the Cerrado biome that is replacing the natural oristic composition by large †r in onoc lt re pl nt tions c sin† n ero s en„iron ent l i p cts n le in† to the loss oƒ re†ion l bio i„ersitŒ in the northern istrib tion of the Cerrado biome. Furthermore, the Parque Estadual do Mirador is n i port nt biore†ion l corri or oƒ preser„ tion which is cr ci l ƒor the
inten ncŒ oƒ species i„ersitŒ.
Supplementary material
‰he ƒollowin† online teri l is „ il ble ƒor this rticle: ppen i‚ – o cher speci ens
Acknowledgment
e th n ‰hi †o ibeiro e r„ lho n elipe il„ e n r e for con rmation of the species identity. To Tássia Graziele Pires Lima, Micheli Véras dos Santos, Kássio de Castro Araújo, Johnny Sousa Ferreira and Sâmia Caroline Melo Araújo for helping in eldwork. To Vinícius de Avelar São Pedro and Nivaldo Magalhães Piorski for suggestions and „ l ble contrib tions to i pro„in† the n script. e th n ecret ri de Estado de Meio Ambiente e Recursos Naturais-SEMA for providing collecting permit (008/2013), APERMIRA for permission to access to the Parque Estadual do Mirador and to Universidade Federal do Piauí-UFPI (Campus de Parnaíba) for logistical support. EBA thanks Fundação de Amparo à Pesquisa do Estado do Maranhão (FAPEMA) for nancial support through the Support Program for Research Projects UNIVERSAL (edital n° 001/2013 - FAPEMA) and Ph.D. grant (BD-01163/13).
Author contributions
tielle … rroso e n r e: contrib te in t c• isition n lŒsis n interpret tion oƒ t n writin† oƒ the p per.
Luiz Norberto Weber and José Roberto de Souza Almeida Leite: contrib te in the conception n esi†n oƒ the p per n critic l re„iew
in† intellect l content.
Con icts of interest
The authors declare that they have no con ict of interest related to the p blic tion oƒ this n script.
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Received: 12/09/2016 Revised: 13/11/2017 Accepted: 20/11/2017
