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Home , Adenomera, Corythomantis, Corythomantis greeningi, Dendropsophus branneri, Dendropsophus minusculus, Dendropsophus minutus

Herpetology Notes, volume 12: 1145-1156 (2019) (published online on 05 November 2019)

Anuran in a Neotropical natural ecotone

Rodrigo Matavelli1,2,*, Aldenise Martins Campos1, Clarenice Loiola Santos1, and Gilda Vasconcellos de Andrade3

Abstract. Little attention has been given to natural ecotone areas around the world. However, natural ecotones play an important role in sustaining high richness and a unique that do not exist in the adjacent . We present the first anuran inventory in a natural ecotone between and restinga in northeastern Maranhão State, . The survey was conducted at 24 sampling points in an area of 14,360 km2. We sampled anurans during the rainy season (January to July 2010) using the visual search (youth and adults) and acoustic search (male reproductive activity of vocalization) methods simultaneously to detect the presence of adult individuals. We recorded 50 anuran species belonging to 15 genera and five families. The anuran fauna showed high , which may be explained by the fact that the study area is a natural biogeographic transition zone.

Keywords. , Conservation efforts, Inventory, Maranhão, Transition areas

Introduction 2014; Johnson et al., 2017), mainly because the species’ two-phase life cycle makes them very sensitive to any Brazil has the largest anuran diversity in the world, with changes in both aquatic and terrestrial environments approximately 1,090 species (Frost, 2019; Segalla et al., (Stuart et al., 2008; Adeba et al., 2010). 2019). This great diversity is probably due to its large Most previous studies on anurans in Brazil evaluated territorial extent, and to a high geographical complexity their distribution patterns and species composition involving various natural that comprise different in Cerrado (Giaretta et al., 2008; Valdujo et al., 2011; phytophysiognomies (IBGE, 1994; Olson et al., 2001) Moraes et al., 2012; Gambale et al., 2014) and restinga and natural ecotone areas. areas (Wachlevski and Rocha, 2010; Vilela et al., 2011; Despite this great diversity, several Brazilian anuran Telles et al., 2012; Gondim-Silva et al., 2016), but little populations have declined in recent decades (Eterovick attention has been paid to the world’s natural ecotone et al., 2005; Becker et al., 2007; Verdade et al., 2010) areas (Smith et al., 2001; Kark and van Rensburg, as a result of human activities that lead to degradation, 2006), including the Brazilian ones. fragmentation, and loss. These processes are the Natural ecotones sustain high species richness and a primary causes of local extinctions and the global decline unique biodiversity. These areas play an important role in in anuran populations (Gibbs et al., 2005; Dirzo et al., maintaining a biodiversity that does not exist in adjacent ecosystems (Ruggiero and Ezcurra, 2003; Kark and van Rensburg, 2006; Kark, 2013; Kark, 2017), justifying a greater conservation effort than they currently receive (Smith et al., 2001; Kark, 2013). Maranhao State acts 1 Universidade Federal do Maranhão (UFMA), Programa de Pós-Graduação em Biodiversidade e Conservação. Avenida as a natural biogeographic transition zone between the dos Portugueses 1966, Campus do Bacanga, CEP: 65.080- Amazon, Caatinga and Cerrado biomes (IBGE, 1984; 805, São Luis, MA, Brasil. AbSaber, 1989; Rebêlo et al., 2010); thus its biodiversity 2 Universidade Estadual Paulista (UNESP), Departamento de needs to be further researched, better understood and, Ecologia, Laboratório de Ecologia Espacial e Conservação ultimately, preserved. (LEEC). Avenida 24A, nº 1515, CEP: 13.506-900, Rio Although there are some recently published lists of Claro, SP, Brasil. the anuran species in Maranhão State, encompassing 3 Universidade Federal do Maranhão (UFMA), Departamento de Biologia, Avenida dos Portugueses 1966, Campus do the Amazon (Freitas et al., 2017), Cerrado biome Bacanga, CEP: 65.080-805, São Luis, MA, Brasil. (Brasileiro et al., 2008; Andrade et al., 2017) and also * Corresponding author. E-mail: [email protected] some islands (Andrade et al., 2012; Andrade et al., 2016), 1146 Rodrigo Matavelli et al. no survey was conducted in natural ecotone areas in this The average annual rainfall is high, around 2,325 mm region. Despite the basic format of species compilations (CPTEC/INPE, 2010). lists, these lists can provide important information The Cerrado biome comprises about 65% of the for research, legislation and other activities related to vegetation cover in Maranhão (Sano et al., 2008) biodiversity management and conservation (Hamer et and occurs on a flat and smooth relief known locally al., 2012), especially in natural ecotone areas, which as “Chapada”, where Cerradão is the predominant sustain high species richness and a unique biodiversity physiognomy (IBGE, 1984). Cerrado is considered (Risser, 1995; Kark and van Rensburg, 2006; Kark et a biodiversity hotspot (Klink and Machado, 2005) al., 2007; Kark, 2017). because it presents a great heterogeneity in its plant The main purpose of this study was to reveal for the formations (Ratter et al., 1997), which include campestre first time the anuran community composition in a natural formations, savannahs and tropical (Ribeiro and ecotone between Cerrado and restinga in northeastern Walter, 2008). Maranhão State, Brazil. The restingas, a phytophysiognomy of the Atlantic biome typical of the sandy coastal plains Material and Methods (IBGE, 1984; Araujo et al., 1998) - also considered a biodiversity hotspot (Myers, 2000) - presents a diverse Study area.—The study was carried out in nine phytophysiognomy ranging from coastal herbaceous to municipalities in northeastern Maranhão, covering an dense forests in sandy soils (Araujo and Lacerda, 1987). area of 14,360 km2 (Figure 1). In northeastern Maranhão, the restingas are composed The region’s climate is mesothermal and humid of species endemic to the biome itself and species that tropical with two well-defined seasons: a rainy season also occupy the , Caatinga and Cerrado (January to June), which receives about 94% of the biomes (Silva et al., 2009). annual rainfall, and the dry or drought season (July to Specifically, our sampling design consisted of 12 sites December), which receives only 6% of the precipitation. in Cerrado areas and 12 sites in restinga areas (Figure

Figure 1. Study region encompassing 24 sampled points in a Neotropical natural ecotone between Cerrado and restinga in northeastern Maranhão State, Brazil. Triangles: Cerrado areas; Circles: restinga areas. Anuran community in a Neotropical natural ecotone 1147

1) distributed in lentic and/or temporary environments increased. In addition, seven (14%) were classified as (two small floodplain and eight ponds) and in lotic/ “data unknown”, and five (10%) as “no data” (Table permanent environments called “buritizais” (14 gallery 1). forests with crystalline waters and a predominance of Regarding conservation status (43 species or 86%) are the palm tree Mauritia flexuosa L. [Arecaceae]) along actually listed as “Least Concern” (LC), two (4%) as a natural ecotone between Cerrado and restinga in “Data Deficient” (DD) on a global level (IUCN, 2019), northeastern Maranhão State, Brazil. and five (10%) as “no data” (Table 1). Anuran fauna sampling.—The qualitative sampling Discussion of the anurans (presence of species) was conducted monthly during the rainy season (January to August The anuran species richness recorded in the present 2010) at 24 sampling points in northeastern Maranhão study was higher in comparison to other works State, Brazil (Figure 1). conducted in Cerrado areas (Valdujo et al., 2011; Morais We sampled the anuran communities using the et al., 2012; Silva et al., 2015), restinga areas (Bastazini visual search (youth and adults) and acoustic search et al., 2007; Vilela et al., 2011; Gondim-Silva et al., (male reproductive activity of vocalization) methods 2016), and other natural ecotones comprised of different simultaneously to maximize the number of species biomes (Bitar et al., 2012; Magalhães et al., 2013; Silva observed by sampling (Heyer et al., 1994; Pearman et et al., 2013; Batista and Bastos, 2014; Borges-Leite et al., 1995). al., 2014). Anurans were sampled in areas up to 1 m from the This higher anuran richness found in our study margins surrounding the lentic environments (two small is perhaps explained simply by the sampled area’s floodplains and eight ponds), and in 300-m transects location within a natural ecotone (IBGE 1984; along the two margins of the lotic environments (14 Ab’Saber 1989; Rebêlo et al., 2010). For example, we buritizais). All environments and adjacent vegetation recorded some species that are commonly found in were inspected between 18:00h and 24:00h for the the Amazon (Boana boans and Boana geographica), presence of species (Heyer et al., 1994). Data sampling Caatinga ( greeningi and jimi), was standardized to 1h/day at each of the 24 sampled and Cerrado ( pustulatus, points to equalize the sampling effort among them. centralis and ) biomes, as well as some Unidentified adult anurans were collected, euthanized species with wide distribution (, with xylocaine 5%, fixed in 10% formalin and then and fuscomarginatus), preserved in 70% alcohol. All material collected which supports the hypothesis that a natural ecotone was deposited in the Coleção de Herpetologia da exists in this region. Universidade Federal do Maranhão (CHUFMA). Regions considered natural ecotones are unique areas that share physical and biological characteristics of Results adjacent regions (Williams, 1996; Ramanamanjato et We recorded 50 species belonging to fifteen genera al., 2002; Ruggiero and Ezcurra, 2003; Kark, 2013). and five families in northeastern Maranhão State (Table These characteristics are defined mainly on temporal 1). Five species (10%) could not be identified to species and spatial scales, but also by the strength of interactions level and their population trend and conservation status between the different connecting biomes (Risser, 1995; was characterized as “no data”. Kark, 2013). These connections between different family had the highest species richness (25 biomes favor a high species richness, with a faunistic species or 50%), followed by (15 or composition constituted by elements of both biomes, as 30%), Bufonidae (5 or 10%), Microhylidae (3 or 6%), observed in other herpetofauna studies (Matavelli et al., (2 or 4%) respectively (Table 1). 2013; Freitas et al., 2014a,b; Matavelli et al., 2014a,b; branneri was the most frequent Freitas et al., 2017) carried out in Maranhão State. species in all environments, occurring in (23 or 96%) of These findings corroborate the idea that natural the 24 sampled points (Table 1). ecotones derive their species composition from two The IUCN (2019) data on current population trends for different adjacent ecological systems, which generally the 50 species recorded in northeastern Maranhão show present a unique ecotonal environment highly diverse that most populations (35 species or 70%) are actually at both the intraspecific and community levels (Risser, stable, two (4%) have decreased, and only one (2%) has 1995; Kark and van Rensburg, 2006; Kark et al., 2007; 1148 Rodrigo Matavelli et al.

Table 1. Anurans registered in a Neotropical natural ecotone between Cerrado and restinga in northeastern Maranhão State, Brazil. Frequency (F): Anuran species frequency in up to 24 sample points. Sampling methods: Visual (V) and Acoustic (A) searches. TableIUCN 1. ConservationAnurans registered status: in a Neotropical Least Concern natural ecotone (LC) andbetween Deficient Cerrado dataand restinga (DD). in northeastern Maranhão State, Brazil. Frequency (F): Anurans species frequency in up to 24 sample points. Sampling methods: Visual (V) and Acoustic (A) searches. IUCN Conservation status: Least Concern (LC) and Deficient data (DD).

BIOME IUCN SPECIES F METHODS Conservation Population VOUCHERS Cerrado Restinga status trends Bufonidae (Stevaux, 2002) 4 X X V/A LC Stable 1140 - CHUFMA Rhinella margaritifera (Laurenti, 1768) 3 X X V/A LC Stable 1143 - CHUFMA Rhinella mirandaribeiroi Gallardo 1965 5 X X V/A LC Data unknown 1148 - CHUFMA Rhinella ocellata (Günther, 1858) 5 X X V/A LC Decreasing 1047 - CHUFMA Rhinella schneideri (Werner, 1894) 8 X X V/A LC Increasing 1145 - CHUFMA Hylidae Boana albopunctata (Spix, 1824) 1 X V/A LC Stable 1020 - CHUFMA

Boana boans (Linnaeus, 1758) 3 X V/A LC Stable 11126 - MZUFBA

Boana crepitans (Wied-Neuwied, 1824) 1 X A LC Stable

Boana geographica (Spix, 1824) 2 X V/A LC Stable 11236 - MZUFBA

Boana multifasciata (Günther, 1859"1858") 21 X X V/A LC Stable 1123 - CHUFMA Boana punctata (Schneider, 1799) 16 X X V/A LC Stable 1015 - CHUFMA Boana raniceps Cope, 1862 15 X X V/A LC Stable 1017 - CHUFMA Boulenger, 1896 3 X A LC Stable

Dendropsophus branneri (Cochran, 1948) 23 X X V/A LC Stable 1193 - CHUFMA Dendropsophus melanargyreus (Cope, 1887) 1 X V/A LC Stable 1139 - CHUFMA

Dendropsophus minusculus (Rivero, 1971) 5 X X V/A LC Stable 1135 - CHUFMA Dendropsophus minutus (Peters, 1872) 17 X X V/A LC Stable 1029 - CHUFMA Dendropsophus nanus (Boulenger, 1889) 6 X X V/A LC Stable 1037 - CHUFMA Dendropsophus rubicundulus (Reinhardt and Lütken, 1862) 1 X V/A LC Decreasing 1027 - CHUFMA

Dendropsophus soaresi (Caramaschi and Jim, 1983) 2 X V/A LC Stable 1138 - CHUFMA

Osteocephalus taurinus Steindachner, 1862 6 X V/A LC Stable 1013 - CHUFMA

Scinax constrictus Lima, Bastos and Giaretta, 2004 4 X X V/A LC Data unknown 1194 - CHUFMA (A. Lutz, 1925) 18 X X V/A LC Stable 1196 - CHUFMA Scinax aff. hayii 1 X V/A No data No data 1125 - CHUFMA

Scinax nebulosus (Spix, 1824) 21 X X V/A LC Stable 1061 - CHUFMA Scinax x-signatus (Spix, 1824) 11 X X V/A LC Stable 1059 - CHUFMA Scinax aff. x-signatus 1 1 X V/A No data No data 1057 - CHUFMA

Scinax aff. x-signatus 2 3 X V/A No data No data 1058 - CHUFMA

Scinax sp1. 2 X V/A No data No data 1028 - CHUFMA

Trachycephalus typhonius (Linnaeus, 1758) 1 X X V/A LC Stable 1036 - CHUFMA Leptodactylidae hylaedactyla (Cope, 1868) 1 X V/A LC Stable 1016 - CHUFMA

Leptodactylus fuscus (Schneider, 1799) 13 X X V/A LC Stable 1022 - CHUFMA Leptodactylus macrosternum Miranda-Ribeiro, 1926 12 X X V/A LC Stable 1030 - CHUFMA Lutz, 1930 9 X X V/A LC Stable 1121 - CHUFMA Leptodactylus podicipinus (Cope, 1862) 7 X X V/A LC Stable 1032 - CHUFMA (Peters, 1870) 8 X X V/A LC Stable 1043 - CHUFMA Bokermann, 1969 1 X V/A LC Stable 10383 - MZUFBA

Leptodactylus troglodytes Lutz, 1926 3 X X V/A LC Stable 1150 - CHUFMA Leptodactylus vastus Lutz, 1930 21 X X V/A LC Data unknown 1005 - CHUFMA (Spix, 1824) 1 X A LC Stable 1166 - CHUFMA

Physalaemus centralis Bokermann, 1962 7 X X V/A LC Data unknown 1011 - CHUFMA Physalaemus cuvieri Fitzinger, 1826 18 X X V/A LC Stable 1167 - CHUFMA Pseudopaludicola mystacalis (Cope, 1887) 17 X X V/A LC Stable 1198 - CHUFMA Pseudopaludicola aff. canga Giaretta and Kokubum, 2003 3 X V/A DD Data unknown 1195 - CHUFMA

Pseudopaludicola sp.1 1 X V/A No data No data 1190 - CHUFMA

Microhylidae Dermatonotus muelleri (Boettger, 1885) 1 X A LC Stable

Anuran community in a Neotropical natural ecotone 1149

TableTable 1. 1.Anurans Continued. registered in a Neotropical natural ecotone between Cerrado and restinga in northeastern Maranhão State, Brazil. Frequency (F): Anurans species frequency in up to 24 sample points. Sampling methods: Visual (V) and Acoustic (A) searches. IUCN Conservation status: Least Concern (LC) and Deficient data (DD).

BIOME IUCN SPECIES F METHODS Conservation Population VOUCHERS Cerrado Restinga status trends BufonidaeElachistocleis bumbameuboi Caramaschi, 2010 2 X V/A DD Data unknown 1024 - CHUFMA

RhinellaElachistocleis jimi (Stevaux, carvalhoi 2002) Caramaschi, 2010 43 X X V/A LLCC Data Stable unknown 11401025 - CHUFMA

PhyllomedusidaeRhinella margaritifera (Laurenti, 1768) 3 X X V/A L C Stable 1143 - CHUFMA RhinellaPhyllomedusa mirandaribeiroi bicolor (Boddaert, Gallardo 1772) 1965 15 X X V/AA LLCC Data Stable unknown 1148 - CHUFMA

RhinellaPithecopus ocellata hypochondrialis (Günther, 1858)(Daudin, 1800) 195 X X V/A LC Decreasing Stable 10471133 - CHUFMA Rhinella schneideri (Werner, 1894) 8 X X V/A L C Increasing 1145 - CHUFMA

Hylidae Boana albopunctata (Spix, 1824) 1 X V/A LC Stable 1020 - CHUFMA

Boana boans (Linnaeus, 1758) 3 X V/A LC Stable 11126 - MZUFBA Kark, 2017) and also a species richness and et al., 2013). Another important fact is that most hylids Boana crepitans (Wied-Neuwied, 1824) 1 X A LC Stable higher than in a single biome (Ramanamanjato et have arboreal habits and successfully manage to occupy Boana geographica (Spix, 1824) 2 X V/A LC Stable 11236 - MZUFBA

al.,Boana 2002; multifasciata Ruggiero (Günther, and 1859"1858") Ezcurra, 2003; Kark,21 2013). X environments X V/A with extensiveLC structural Stable heterogeneity, 1123 - CHUFMA However,Boana punctata it is (Schneider, worth 1799)mentioning that some studies16 X on such X as V/A forests. ThisLC corroborates Stable Cardoso 1015 - CHUFMA et al. biodiversityBoana raniceps patterns Cope, 1862 in different natural ecotonal15 areas X (1989), X that V/A the traits ofLC expanded Stable digital pads 1017 - giveCHUFMA this Corythomantis greeningi Boulenger, 1896 3 X A LC Stable have shown conflicting results, making it difficult to group an advantage over terrestrial species. All of the generalizeDendropsophus without branneri (Cochran, carefully 1948) examining each23 case, X abovementioned X V/A characteristicsLC allow Stable hylids 1193 to - CHUFMA occupy Dendropsophus melanargyreus (Cope, 1887) 1 X V/A LC Stable 1139 - CHUFMA community, region and country (Kark, 2013; Kark, different and various strata of vegetation, which Dendropsophus minusculus (Rivero, 1971) 5 X X V/A LC Stable 1135 - CHUFMA 2017). might explain the of this family, in terms of Dendropsophus minutus (Peters, 1872) 17 X X V/A LC Stable 1029 - CHUFMA Finally,Dendropsophus our nanusresults (Boulenger, and other 1889) previous studies6 support X number X of V/A species, in LseveralC Neotropical Stable 1037communities - CHUFMA theDendropsophus hypothesis rubicundulus that Maranhão (Reinhardt and StateLütken, 1862) is a large1 X and (Afonso andV/A Eterovick,LC 2007; Zina Decreasing et al., 2012; 1027 - CHUFMA Segalla

peculiarDendropsophus natural soaresi biogeographic (Caramaschi and Jim,transition 1983) zone2 with the etX al., 2019). V/A LC Stable 1138 - CHUFMA

Osteocephalus taurinus Steindachner, 1862 6 X V/A LC Stable 1013 - CHUFMA Amazon Forest on the western portion, Caatinga areas Dendropsophus branneri (Cochran, 1948) is on Scinax eastern constrictus portion, Lima, Bastos Cerrado and Giaretta, areas 2004 on the central4 X and considered X V/A a generalistLC species Data widely unknown distributed 1194 - CHUFMA along northeastern portions (IBGE, 1984; Ab’Saber, 1989; the northeastern and eastern Brazilian coast (Frost, 2019; Rebêlo et al., 2010), and coastal ecosystems (restingas IUCN 2019). This species’ enormous plasticity and and mangroves) on northern and northeastern portions prolonged reproductive period, which often involves (Matavelli et al., 2014a; Matavelli et al., 2015), which the use of temporary and/or permanent pools (Lutz, further emphasizes the importance of conserving this 1973), allows it to inhabit a wide variety of habitats, region. including savannahs, shrubs, open areas, dunes and Hylidae is the richest family in the Neotropical region, highly anthropogenic areas (Feio and Ferreira, 2005; comprising 25% of the anurans in South America, being Santana et al., 2010; Frost 2019; IUCN 2019). This generally predominant throughout the Neotropical generalism explains the species’ greater abundance in region (Duellman, 1988; Duellman, 1999; Frost, 2019). diverse environments and regions (Baracho et al., 2014; This predominance of the Hylidae family, followed Palmeira and Gonçalves, 2015; Pereira et al., 2016; by the Leptodactylidae, is a well-known pattern in Barbosa and Rodrigues, 2017). various Brazilian biomes as Amazon (Lima et al., IUCN (2019) data on the current population trends 2006; Neckel-Oliveira, 2013), Atlantic Forest (Bertoluci and conservation status of the anuran fauna reveals that and Rodriguez, 2002; Martins et al., 2014), Caatinga most populations in northeastern Maranhão State are (Magalhães et al., 2015; Roberto and Loebmann, 2016) stable and listed as “Least Concern” (Table 1). These and Cerrado (Valdujo et al., 2011; Silva et al., 2015) and results are due to the fact that most species present also on continental islands (Silva et al., 2008; Quintela et wide distributions, tolerate different types of habitat, al., 2009; Zina et al., 2012), corroborating our results. and have large populations that are unlikely to decline The high diversity of hylids found in our study may fast enough to qualify them as threatened (Frost 2019; be a result of the great number of related species in this IUCN 2019). family (Frost, 2019; Segalla et al., 2019), which are Natural ecotones have gained greater attention in recent morphologically and ecologically very diverse (Wells, decades for their importance in helping us understand 2007) and also exhibit a wide diversity of reproductive evolutionary and ecological processes. Several studies modes (Haddad and Prado, 2005; Wells, 2007; Haddad have been carried out within an ecological context 1150 Rodrigo Matavelli et al.

Figure 2. Anurans registered in a Neotropical natural ecotone between Cerrado and restinga in northeastern Maranhão State, Brazil. A) Rhinella margaritifera; B) Rhinella mirandaribeiroi C) Rhinella ocellata; D) Rhinella schneideri; E) Boana albopunctata; F) Boana boans; G) Boana geographica; H) Boana multifasciata; I) Boana punctata; J) Boana raniceps; K) Dendropsophus branneri; L) Dendropsophus melanargyreus. Anuran community in a Neotropical natural ecotone 1151

Figure 3. Anurans registered in a Neotropical natural ecotone between Cerrado and restinga in northeastern Maranhão State, Brazil. A) Dendropsophus minutus; B) Dendropsophus nanus; C) Dendropsophus rubicundulus; D) Dendropsophus soaresi; E) Osteocephalus taurinus; F) ; G) Scinax fuscomarginatus; H) ; I) Scinax x-signatus; J) Trachycephalus typhonius; K) ; L) Leptodactylus fuscus. 1152 Rodrigo Matavelli et al.

Figure 4. Anurans registered in a Neotropical natural ecotone between Cerrado and restinga in northeastern Maranhão State, Brazil. A) Leptodactylus macrosternum; B) Leptodactylus podicipinus; C) Leptodactylus pustulatus; D) Leptodactylus syphax; E) Leptodactylus troglodytes; F) Leptodactylus vastus; G) ; H) Physalaemus cuvieri; I) Pseudopaludicola mystacalis; J) Pseudopaludicola aff. canga; K) bicolor; L) hypochondrialis. Anuran community in a Neotropical natural ecotone 1153

(populations, communities and ecosystems), mainly RM (process #2014/27320-8). We thank also Instituto Chico because these areas sustain and preserve a rich and Mendes de Conservação da Biodiversidade (ICMBio/SISBio) unique biodiversity for future generations (Kark, for the collection license (Authorization #20896-1). GVA was supported by CNPq - Conselho Nacional de Desenvolvimento 2013; Kark, 2017), but also because they can serve as Científico e Tecnológico (Casadinho/620163/2009-8), and thanks centres (Schilthuizen, 2000). the research fellowship (process CNPq/PQ/312286/2015-5). In recent years, some studies have focused on determining which of the world’s natural environments References are most valuable and should therefore be prioritized for conservation (Smith et al., 2001; Kark et al., 2007; Ab’Saber, A.N. (1989): Zoneamento Ecológico e Econômico da Kark, 2013). This effort is driven mainly by the effect of Amazônia: Questões de Escala e Método. Estudos Avançados climate change on the planet (Chen et al., 2011; Shoo et (USP) 3: 4–20. Abreu, R.O., Juncá, F.A., Souza, I.C.A., Napoli, M.F. (2015): The al., 2013; Catenazzi, 2015). Among the most important tadpole of Dendropsophus branneri (Cochran, 1948) (Amphibia, criteria and/or parameters for selecting conservation Anura, Hylidae). Zootaxa 3946: 296–300. priority areas are species compilation lists, as their Adeba, P.J., Kouassi, P., Rödel, M.O. (2010): Anuran amphibians in information on the anuran richness and abundance a rapidly changing environment - revisiting lamto, côte d’ivoire, is very important for understanding population 40 years after the first herpetofaunal investigations. African fluctuations, assessing species’ conservation status, Journal of Herpetology 59: 1–16. and identifying new species and the degree of regional Afonso, L.G., Eterovick, P.C. (2007): Spatial and temporal distribution of breeding anurans in streams in southeastern (Drummond et al., 2005; Lucas and Fortes, Brazil. Journal of Natural History 41: 949–963. 2008; Bressan et al., 2009). Andrade, E.B., Leite-Júnior, J.M.A., Silva-Leite, R.R., Vieira, Thus, when selecting priority areas for future D.L., Santos, R.C., Silva, V.G., Barbosa, É.A., Souza, V.V., conservation action, natural ecotone areas provide a Leite, J.R.S.A. (2012): Diversidade de anuros na Ilha do Caju, unique opportunity to protect attributes of their adjacent Delta do Rio Parnaíba, Estado do Maranhão, nordeste do Brasil. ecosystems as well as preserving and maintaining their Revista Biociências 18: 14–21. high species richness and high complementarity of Andrade, E.B., Leite, J.R.S.A., Andrade, G.V. (2016): Diversity and “rare species” (Ramanamanjato et al., 2002; Ruggiero distribution of anuran in two islands of Parnaíba River Delta, Northeastern Brazil. Journal of Biodiversity and Environmental and Ezcurra, 2003; Kark, 2013). Furthermore, given Sciences 8: 74–86. that ecotones possess a high biodiversity within a Andrade, E.B., Weber, L.N., Leite, J.R.S.A. (2017): Anurans of the relatively small area, their conservation may prove to Parque Estadual do Mirador, a remnant of Cerrado in the state of be a cost-effective strategy, providing a high return on Maranhão, Northeastern Brazil. Biota Neotropica 17: 1–12. investment (Kark et al., 2007; Kark, 2017). In light Araujo, D.S.D., Lacerda, L.D. (1987): A natureza das restingas. of all these characteristics, natural ecotones should Ciência Hoje 6: 42–48. undoubtedly receive more attention, be included in Araujo, D.S.D., Scarano, F.R., Sá, C.F.C., Kurtz, B.C., Zaluar, H.L.T., Montezuma, R.C.M., Oliveira, R.C. (1998): future conservation analyses and decision-making, and Comunidades vegetais do Parque Nacional da Restinga de be the focus of conservation programs. Furthermore, Jurubatiba. In: Ecologia das lagoas costeiras do Parque Nacional any conservation plans for regional ecotones should da Restinga de Jurubatiba e do município de Macaé, (RJ), p. always consider their surrounding environments (Kark 39–62. Esteves, F.A., Ed., Rio de Janeiro, Universidade Federal et al., 2007; Kark, 2013). do Rio de Janeiro, Brazil. Finally, our results highlight the substantial value and Araújo, K.C., Santos, M.V., Pires, L.T.G., Andrade, E.B., Weber, importance of conserving natural ecotone areas, as these L.N. (2015): First record of Adenomera saci Carvalho & diverse and peculiar natural biogeographic transition Giaretta, 2013 (Anura: Leptodactylidae) for the State of Maranhão, Northeastern Brazil. Herpetology notes 8: 183–185. zones are essential for sustaining and maintaining the life Baracho, E.B.O., Silva, J.S., Nascimento, B.H.M., Fonseca, E.M., cycles of various taxa, including anuran communities. Magalhães, F.M. (2014): Dendropsophus branneri (Cochran, 1948) (Anura: Hylidae) as prey to invertebrates in Northeastern Acknowledgements. We are grateful to Marcelo Napoli (UFBA), Brazil. Herpetology notes 7: 17–19. Célio Haddad (UNESP/Rio Claro) and Délio Baêta (UNESP/Rio Barbosa, G.G., Rodrigues, G.G. (2017): Anuros em áreas com Claro) for taxonomic support. We also thank all those who helped diferentes graus de ações antrópicas no refúgio de vida silvestre in the fieldwork, mainly Jorge Luiz Pinto Moraes (FUNASA/ matas do sistema Gurjaú, Nordeste do Brasil. Revista Brasileira MA). This research was supported by the CAPES - Coordenação de Geografia Física 10: 767–783. de Aperfeiçoamento de Pessoal de Nível Superior for a master’s Bastazini, C.V., Munduruca, J.F.V., Rocha, P.L.B., Napoli, M.F. fellowship to RM and AMC and FAPESP - Fundação de Amparo (2007): Which environmental variables better explain changes à Pesquisa do Estado de São Paulo for a doctoral fellowship to in anuran community composition? A case study in the resting of 1154 Rodrigo Matavelli et al.

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Accepted by Javier Cortés Suárez