Knowledge status, endemism, and conservation of anuran amphibians from Espinhaço Range, Brazil: what we know and what are the main opportunities for future studies?

Estado de conhecimento, endemismo e conservação dos anfíbios anuros da Serra do Espinhaço, Brasil: O que sabemos e quais as principais oportunidades para estudos futuros?

Abstract

Espinhaço Range’s frogs have attracted attention since the middle of the 20th century. Despite great efforts to understand the taxonomy, patterns of distribution and biology of the anurans of this mountain range, many questions remain unanswered. Here, we updated the knowledge on endemic anurans of Espinhaço Range, including information on species ecology, behaviour, natural history, evolution, biogeography, and conservation. There are 42 endemic species, and this number may still be underestimated since numerous species lack formal descriptions. Many of these frogs are associated with the campo rupestre, the mountaintop ecosystem of Espinhaço. The greatest endemism richness in Espinhaço is concentrated in its southern portion, along Serra do Cipó, Minas Gerais, Brazil. Tadpoles and vocalizations are known for most of the endemic species, as well as the phylogenetic relationship within their respective genera. However, data on behaviour, ecology, and natural history are scarce, revealing the need and opportunities for future scientific investigations, such as studies on adaptations of endemic species to the environmental conditions of the campo rupestre.

Keywords
campo rupestre ; diversity ; evolution ; biogeography ; ecology ; behaviour, inventory

Resumo

A Serra do Espinhaço desperta atenção em relação à anurofauna desde meados do século 20. Apesar dos grandes esforços para conhecer os anuros dessa cadeia de montanhas, muitas questões relacionadas aos padrões de riqueza, composição, endemismo e aspectos biológicos ainda permanecem sem resposta. Atualizamos o conhecimento sobre os anuros endêmicos da Serra do Espinhaço, incluindo uma lista de espécies atualizada e dados sobre ecologia, comportamento, história natural, evolução, biogeografia e conservação. Existem 42 espécies endêmicas, e este número pode estar subestimado, uma vez que muitas espécies carecem de descrições formais. A maior riqueza de espécies endêmicas da Serra do Espinhaço está concentrada no sul do Espinhaço Mineiro, ao longo da Serra do Cipó, Minas Gerais. Girinos e vocalizações são conhecidos para a maioria das espécies endêmicas da Serra do Espinhaço, bem como o relacionamento filogenético destas com espécies congêneres. Entretanto, dados de comportamento, ecologia e história natural são escassos para a maioria delas. Muitos dos estudos são incipientes, revelando a necessidade e oportunidades para futuras investigações científicas, como estudos sobre os efeitos de gradientes ambientais e adaptações das espécies endêmicas às condições ambientais do campo rupestre.

Palavras-chave
campo rupestre ; diversidade ; evolução ; biogeografia ; ecologia ; comportamento ; inventário

Introduction

Brazil harbours the highest known anuran richness in the world, with about 15% of the 7690 living species (Segalla et al. 2021, Frost 2024). These animals are known for their low dispersal ability and need for specific habitats (Smith & Green 2005). The low vagility of anurans favours allopatric differentiation of lineages, which can lead to speciation (Wollenberg-Valero et al. 2019). Habitat specificity, in turn, is related to the reproductive particularities of each species. In this context, anurans are the group of tetrapods with the greatest diversity of reproductive modes (Haddad & Prado 2005), with 42 modes recorded in the world and 32 in the Neotropical region (Malagoli et al. 2021). As reproductive modes are related to different oviposition sites, regions with high habitat heterogeneity tend to sustain greater diversity of these modes and, consequently, greater species richness (Eterovick & Barata 2006, Bickford et al. 2010). Topographic complexity may also directly influence the genetic differentiation of tropical anurans since the increase in complexity results in a greater richness of microhabitats (Rodríguez et al. 2015). Each type of microhabitat, in turn, tends to be rare and presents a random spatial distribution, favouring isolation between subpopulations that depend on specific microenvironmental conditions, which may result in genetic differentiation (Rodríguez et al. 2015).

Mountain ranges are the terrestrial environments with the greatest topographical complexity (Körner et al. 2017) and, not coincidentally, they have a high richness of amphibians, being important centres of endemism (e.g. Rödder et al. 2010, Silva et al. 2018, Guedes et al. 2020). Amphibian richness in mountains is inversely correlated with latitude, with tropical mountains being those with greatest diversity (García-Rodríguez et al. 2021). Biotic and abiotic factors play important roles in the evolutionary history of species, affecting biological variability in landscapes (Guedes et al. 2020). Thus, in addition to topographic complexity and dispersal capacity, climate change and interactions between species can influence the distribution and composition of local diversity (Sandel et al. 2011, Wisz et al. 2013, Antonelli et al. 2018).

In this context, the Espinhaço Range stands out for being the second largest mountain range in South America (Guedes et al. 2020), extending in a north-south direction, along 1200 km in eastern Brazil, between the states of Bahia and Minas Gerais (Fernandes et al. 2014). Considering the assemblages of endemic anurans, the mountain range has been classified into three regions (Leite et al. 2008a): (1) Chapada Diamantina (Figures 1, 2A), from northeast Bahia to the Serra das Almas region; (2) Espinhaço Mineiro (Figures 1, 3A), from southwest Bahia to centre of Minas Gerais state, including Serra do Cabral (Figures 1, 4A), a disjoint unit west of the main ridge; and (3) Quadrilátero Ferrífero (Figure 5A), in the extreme south of the mountain range (Leite et al. 2008a). The mountain top areas are dominated by campo rupestre, an ecosystem characterized by a mosaic of grassland and shrub vegetation that grows on arenite, quartzite, or ironstone rock outcrops, and/or poor, sandy, and shallow soils, to which most endemic species of plants and animals are associated (Silveira et al. 2016). Espinhaço delimits part of the border between the Caatinga, Cerrado, and Atlantic Forest domains, being influenced by their biotas, mainly on the slopes (Silveira et al. 2016). The latitudinal extension of Espinhaço, combined with altitudinal, geological, and edaphic variations, result in a pronounced environmental heterogeneity (Silveira et al. 2016, Miola et al. 2021), providing a wide spectrum of habitats for anuran reproduction (Eterovick & Barata 2006, Pezzuti et al. 2021). Furthermore, high altitude aquatic environments seem to play an important role in the composition of the anurofauna, harbouring a wide phylogenetic diversity of endemic species (e.g. species of the genera Bokermannohyla and Phasmahyla (Hylidae), Hylodes (Hylodidae), Physalaemus (Leptodactylidae), Proceratophrys (Odontophrynidae); Eterovick & Barata 2006, Oliveira & Eterovick 2010).

Figure 1
Map of Espinhaço Range and the different regions considering assemblages of endemic frogs: Chapada Diamantina to the north, delimited in blue, Espinhaço Mineiro to the centre, delimited in red, and Quadrilátero Ferrífero to the south, delimited in green. 1 = Couto de Magalhães Depression; 2 = Serra do Cabral.

Figure 2
(A) Landscape in Chapada Diamantina, Bahia, Brazil; (B) Rupirana cardosoi; (C) Pristimantis rupicola; (D) Haddadus aramunha. Photos by: A. Tiago L. Pezzuti; B-D. Leandro Drummond.

Figure 3
(A) Landscape in Espinhaço Mineiro, north of Minas Gerais, Brazil; (B) Couple of Odontophrynus juquinha; (C) Bokermannohyla alvarengai; (D) Tadpole of Bokermannohyla alvarengai. Photos by Tiago L. Pezzuti.

Figure 4
(A) Landscape in Serra do Cabral, Minas Gerais, Brazil; (B) Bokermannohyla saxicola; (C) Scinax cabralensis; (D) Thoropa megatympanum. Photos by Tiago L. Pezzuti.

Figure 5
(A) Anuran reproductive environment in Quadrilátero Ferrífero, Minas Gerais, Brazil; (B) Male, (C) female, and (D) tadpole of Bokermannohyla martinsi. Photos by A. Lucas Perillo; B-D. Tiago L. Pezzuti.

Espinhaço Range has a great diversity of fauna, flora, and funga, with several endemic species and some endemic genera (e.g. Pardiñas et al. 2014, Coutinho et al. 2015, Scatigna et al. 2020). Espinhaço Mineiro is the richest area of endemism for herpetofauna in the Cerrado domain, with more than 20 anurans restricted to it (Azevedo et al. 2016). In the Caatinga, 16 of the 21 species of endemic amphibians have their distributions restricted to Chapada Diamantina (Marques et al. 2021). In addition, much of the anuran richness and endemism in Minas Gerais state is distributed in the Espinhaço Range (Leite et al. 2008a), highlighting this area as a key for the conservation of regional biodiversity. Due to its environmental, economic, and social relevance, Espinhaço Range received the status of Biosphere Reserve in 2005 (UNESCO 2021).

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A brief history of research on anurans of Espinhaço Range

Studies on the anurofauna of Espinhaço Range began in the 1950s, with the efforts of naturalists Werner Bokermann and Ivan Sazima to describe several of its endemic species and observational aspects of their biology (e.g. Bokermann 1956, 1964, 1967, Bokermann & Sazima 1973a, b, 1978, Sazima & Bokermann 1978, 1982). A series of five scientific articles entitled Amphibians of Cipó Range (Anfíbios da Serra do Cipó, originally in Portuguese) were the result of their efforts, in which six anuran species from three different families were described, as well as observations on the natural history of Bokermannohyla alvarengai (Bokermann, 1956) (Bokermann & Sazima 1973a, b, 1978, Sazima & Bokermann 1977, 1982). These early descriptive studies were essential to minimize the Linnean shortfall in the region (see Hortal et al. 2015).

Heyer (1999) was the first author to suggest that the natural fragmentation of Espinhaço Range, its geographical position between the Caatinga, the Cerrado, and the Atlantic Forest, in addition to the landscape peculiarities of the campo rupestre, could be associated with the endemic anurans of the region. According to the author, several species restricted to Espinhaço would possibly be derived from Atlantic Forest ancestors since genera such as Hylodes, Phasmahyla, and Thoropa are almost entirely endemic to this domain, with exception of the disjunct species that occur in the mountain range. The author pointed out that one of the explanations for this phenomenon is that few Cerrado anuran species have adaptations for reproduction and development in lotic environments, contrary to what is observed in the Atlantic Forest. Espinhaço Range presents an abundance of this type of water bodies, which offered opportunities for the occupation of the region by the forest ancestors of many of the endemic species (see Pezzuti et al. 2021). According to Heyer (1999) few grassland species from lentic environments, such as Leptodactylus camaquaraSazima & Bokermann, 1978 and Leptodactylus cuniculariusSazima & Bokermann, 1978 (Leptodactylidae), would be derived from Cerrado ancestors (Heyer 1999). Finally, Heyer (1999) indicated that all endemic anurans from Espinhaço Range were species pertaining to more widely distributed genera, except for Rupirana cardosoiHeyer, 1999 (Figure 2B), a monotypic and endemic genus to the area, described in that same work. Heyer presented alternative hypotheses to explain the endemism of Rupirana, suggesting that (1) this genus would be a biogeographic relict; (2) it would be more widely distributed; or (3) it would represent a taxonomic definition error. More than a decade later, the first of Heyer’s hypotheses (1999) was corroborated by Fouquet et al. (2013) and by Santos et al. (2020a). These findings show the importance of the geographic position of Espinhaço Range and its evolutionary history in the diversification of the anurofauna endemic to it.

In subsequent years, in addition to taxonomy work, some ecology and natural history studies were carried out by researcher Paula Eterovick and collaborators. In these studies, the researchers evaluated how abiotic (e.g. temporal and spatial parameters) and biotic (e.g. predation and competition) factors influence the composition of anuran assemblages in different regions of Espinhaço, such as the Quadrilátero Ferrífero (Kopp & Eterovick 2006, Afonso & Eterovick 2007a, b) and Espinhaço Mineiro (Eterovick & Fernandes 2001, Eterovick 2003, Oliveira & Eterovick 2009, 2010). The research group also carried out several studies on the natural history of species endemic to Espinhaço, with approaches ranging from reproductive biology, demography, and larval development (Leite et al. 2008b, Oliveira et al. 2012) to behavioural experiments involving tadpole defence strategies and diet studies (Gontijo et al. 2018, Kloh et al. 2018). Knowledge of the natural history of these species has provided information for conservation and the assessment of human impacts on their populations (Eterovick et al. 2015, Mascarenhas et al. 2016, Lima et al. 2019).

Leite et al. (2008a) compiled the endemic amphibians of Espinhaço and identified 28 species restricted to it. Some studies with a similar scope, but restricted to specific areas of Espinhaço Range, were later published, including books (Pimenta et al. 2014, Silveira et al. 2019, Eterovick et al. 2020) and digital resources (Leite et al. 2019a). Pimenta et al. (2014) included 58 species with information on taxonomy, morphology, habits, reproduction, vocalization, tadpoles, and conservation from Alvorada de Minas, Conceição do Mato Dentro, and Dom Joaquim municipalities, in addition to identification keys. Silveira et al. (2019) presented an annotated list with photos and occurrence maps of 92 species, with data compiled through field sampling, bibliographic reviews, and scientific collections from Quadrilátero Ferrífero region. Eterovick et al. (2020) brought a list of 58 species from Serra do Cipó, as well as information on reproduction, types of spawning, and tadpoles, and an illustrated key for the identification. As digital resources, Leite et al. (2019a) provided tools for species identification, such as adult and tadpole identification keys (Pezzuti et al. 2019a, b), vocalization guides (Leite et al. 2019b), and maps with the distribution of species in the Quadrilátero Ferrífero (Leite et al. 2019a, c). Additional, Pezzuti et al. (2021) recorded 96 anuran species for Quadrilátero Ferrífero and presented a morphological and illustrated catalogue, and identification keys for the exotrophic larvae of this region, with important taxonomic contributions.

Over the years, the number of amphibian species described for the Espinhaço Range has increased, following the national and global trend of descriptions of new taxa (Guerra et al. 2020, Moura & Jetz 2021). Almost every year a new species is discovered and described for the region (e.g. Pinheiro et al. 2021, Mângia et al. 2022, Santos et al. 2023), but the last regional inventory dates back more than a decade (Leite et al. 2008a). Here we update the state of knowledge of the endemic amphibians of the Espinhaço Range, providing information that can assist in conservation actions and strategies, in the elaboration of management plans, and other studies.

Material and Methods

We compiled data for all sections of this review through the scientific literature published since Leite et al. (2008a), Amphibian Collections from Centro de Coleções Taxonômicas of Universidade Federal de Minas Gerais (UFMG-AMP), Museu de Zoologia of Universidade Federal da Bahia (MZUFBA), and of Universidade de Campinas (ZUEC-AMP), Herpetological Collection from Laboratório de Zoologia of Universidade Federal de Ouro Preto (LZV-UFOP), Herpetological Collection from Museu de Ciências Naturais da PUC Minas, Museu de Zoologia of Universidade de São Paulo (MZUSP), and Museu de Zoologia of Universidade Federal de Viçosa (MZUFV), and from authors field observations.

^1.

Taxonomic knowledge and distribution patterns

To update the list of endemic species of Espinhaço Range, we added to the checklist of Leite et al. (2008a) the new species described after this paper. We searched for literature with new endemic species, new records of supposedly endemic species outside the area, and taxonomic changes in endemic species with distribution in Espinhaço Range. In addition to the morphology of adults, bioacoustics and larval data of anura also provide important characters for the taxonomy (Grosjean 2005, Köhler et al. 2017), so we also performed a review of these data. To geospatialize the distribution patterns of endemic species of Espinhaço Range, we evaluated the richness of endemism along the mountain range through the LetsR v.5.0 package (Vilela & Villalobos 2015), with a grid resolution of 0.3 degrees for both latitude and longitude. We performed all analyses within the R platform v.4.3.2 (R Core Team 2023) and generated subsequent mapping representations using QGIS software (2023).

^2.

Ecology, behaviour, and natural history

To classify the endemic species into the reproductive modes, we followed Haddad & Prado (2005). The reproductive modes in this classification system are related to a combination of ecological, behavioural, and morphophysiological aspects of the different species, such as: (1) places for oviposition (aquatic, terrestrial or arboreal); (2) types of larval development (indirect – with exotrophic larvae, or direct – endotrophic larvae); (3) types of water bodies (lentic – swamps, puddles, and ponds; lotic – streams); (4) specifics of microhabitat in which spawns are deposited (e.g. underground cavities, underwater chambers, plant cavities, wet rocks); (5) nest characteristics (e.g. foam or bubble nests); (6) presence of parental care, among others. Additionally, we characterized tadpoles of each species following the ecomorphological guilds proposed by Altig & Johnston (1989), summarized by McDiarmid & Altig (1999).

^3.

Evolution and biogeography

For each species or set of endemic species, we searched for phylogenies that included them and converted phylogenetic trees into taxon-area cladograms (Morrone & Carpenter 1994), replacing the species with the areas where they occur (Figure 6). From this, we optimized the ancestral areas through the principle of parsimony using delayed optimization (ACCTRAN; Swofford & Maddison 1987). Although there are more accurate methods for reconstructing ancestral state areas (e.g. Holland et al. 2020), our objective was only to generate testable hypotheses for further biogeographic investigations.

Figure 6
Example of possible origins of endemic species of the Espinhaço Range. (A) Autochthone origin in the Espinhaço Range with subsequent colonization of other areas; (B) Origin in other areas with subsequent colonization of the Espinhaço Range; (C) Independent colonization of the Espinhaço Range; (D) Uncertain ancestral origin. Anura picture available from phylopic.org.

^4.

Conservation

To evaluate the conservation status of endemic species in the Espinhaço Range, we assessed the conservation status in global (IUCN 2023) and national (Brasil 2022) red lists, the presence of the species in protected areas (PA), and current or potential threats through scientific literature. We only consider areas of integral protection, meaning those defined by the Brazilian System of Protected Areas (Sistema Nacional de Unidades de Conservação - SNUC; Brasil 2000), including those administered by the Union and by the states. To evaluate the presence of endemic species in PA, we plotted in a single map with all delimited integral PA from the states of Bahia and Minas Gerais available in Ministério do Meio Ambiente database (i3geo, n.d.) and endemic species records.

Results and Discussion

^1.

Taxonomic knowledge and distribution patterns

Forty-two species are endemic to the Espinhaço Range (Table 1), distributed in 22 genera and seven families, with Hylidae being the one with the highest number of endemics (20 spp.). The second richest family is Leptodactylidae (11 spp.), followed by Odontophrynidae (5 spp.), and Hylodidae (3 spp.). The families Craugastoridae, Cycloramphidae, and Strabomantidae were represented by only one species each.

Table 1
Endemic anurans to Espinhaço Range. Distribution: CD = Chapada Diamantina, EM = Espinhaço Mineiro, QFe = Quadrilátero Ferrífero; Reproductive environment: R = rocky outcrop, LA= water depth in wet rock, LP = permanent ponds, puddles and swamps, RP = permanent streams, RT = temporary streams, AT = temporary shallow swamps, LT = temporary ponds, puddles and swamps, BR = bromeliads); reproductive mode (sensu Haddad & Prado 2005): ? = unknown, 1 = eggs and exotrophic tadpoles in lentic water bodies, 2 = eggs and exotrophic tadpoles in lotic water bodies, 3 = eggs and early larval stages in constructed underwater chambers; exotrophic tadpoles in streams, 4 = eggs and early larval stages in natural or constructed basins; after flooding, exotrophic tadpoles in ponds or streams, 5 = eggs and early larval stages in constructed underground nests; after flooding, exotrophic tadpoles in ponds or streams, 19 = eggs in wet rocks; semi-terrestrial exotrophic tadpoles living in water, on rocks at the water-land interface, 21 = eggs hatch into endotrophic tadpoles that complete their development in the nest, 25 = eggs hatching into exotrophic tadpoles that fall from leaves suspended in lotic water bodies, 26 = eggs hatching into exotrophic tadpoles that develop in water-filled cavities in bromeliads, 28 = foam nest in damp soil; after the flood, exotrophic tadpoles in puddles, 30 = foam nest with eggs and early larval stages in constructed underground nests; after the flood, exotrophic tadpoles in puddles; and tadpole ecomorphological guilds (Altig & Johnston 1989, McDiarmid & Altig 1999): I = Endotrophic, II = Exotrophic, A1= Lentic and lotic habitat, benthic, A2= Lentic and lotic habitat, nektonic, A3 = Lentic and lotic habitat, neustonic, B4a = Lentic only, arboreal, type1, B8 = Lentic only, suspension rasper, B10 = Lotic only, adherent, B11 = Lotic only, suctorial, B15 = Lotic only, semiterrestrial, * = Do not fit perfectly in this guild because occurs in streams, and not in lentic water bodies as used for the B category (Lentic only), ? = no additional information/unknown.

Taxon	Distribution	Reproductive environment		Reproductive mode (Haddad & Prado 2005)	Tadpole Ecomorphological guilds
		Open area	Gallery forests and hillside forests
Craugastoridae
Haddadus aramunha	CD	AR		23	I?
Cycloramphidae
Thoropa megatympanum	QFe, EM	LA		19	IIB15
Hylidae
Aplastodiscus heterophonicus	EM		LP, RP	5	IIA1
Boana botumirim	EM	RP, LP		2	IIA1
Boana cipoensis	EM	RP, LP		2	IIA1
Bokermannohyla alvarengai	QFe, EM	RT		2	IIA1
Bokermannohyla diamantina	EM, CD	AT		4	IIA1
Bokermannohyla flavopicta	CD	RP	RP	2	IIB11
Bokermannohyla itapoty	CD	RP		2	IIB11
Bokermannohyla juiju	CD	RT	RP	?	?
Bokermannohyla martinsi	QFe		RP	2	IIB11
Bokermannohyla nanuzae	EM		RP	2	IIA1
Bokermannohyla oxente	CD	RP	RP	2	IIB11
Bokermannohyla sagarana	EM	RT, RP		?	?
Bokermannohyla saxicola	QFe, EM	RP	RP	2	IIB11
Nyctimantis galeata	CD	RP, LT		?	IIA2
Ololygon machadoi	EM, CD	RP		2	IIB10
Phasmahyla jandaia	QFe, EM		RP	25	IIA3
Pithecopus megacephalus	EM	RT		25	IIB8*
Scinax cabralensis	EM	LT		1, 2	IIA2
Scinax curicica	QFe, EM, CD	LT, LP, RP, RT		1, 2	IIA2
Scinax montivagus	CD	LT, LP, RP, RT	LT, LP, RP, RT	1	IIA2
Hylodidae
Crossodactylus trachystomus	QFe, EM		RP	3	IIA1
Hylodes otavioi	EM		RP	3	IIA1
Hylodes uai	QFe		RP	3	IIA1
Leptodactylidae
Crossodactylodes itambe	EM	BR		26	IIB4a
Crossodactylodes serranegra	EM	BR		26	IIB4a
Leptodactylus avivoca	EM	AT, RT		?	II?
Leptodactylus camaquara	QFe, EM	AT, RT		30	IIA1
Leptodactylus oreomantis	CD	AT, RT		?	IIA1
Physalaemus claptoni	EM		LT	?	II?
Physalaemus deimaticus	EM	RT		?	II?
Physalaemus erythros	QFe	RT		28	IIA1
Physalaemus evangelistai	QFe, EM	LT		28	IIA1
Pseudopaludicola mineira	EM	AT, LT		1	IIA1
Rupirana cardosoi	CD	AT, RT, RP		1	IIA1
Odontophrynidae
Odontophrynus juquinha	EM, CD	LT		1	IIA1
Proceratophrys cururu	EM	RT, RP		2	IIA1
Proceratophrys minuta	CD		RP	2	IIA1
Proceratophrys redacta	CD	RT, RP		2	II?
Proceratophrys velhochico	CD	RT, LT	?	2	II?
Strabomantidae
Pristimantis rupicola	CD	AR		23	I?

Of these, eighteen new endemic species were described after Leite et al. (2008a) [i.e. Boana botumirim (Caramaschi Cruz & Nascimento, 2009); Bokermannohyla juiju Faivovich, Lugli, Lourenço, & Haddad, 2009; Bokermannohyla sagaranaLeite, Pezzuti, & Drummond, 2011; Proceratophrys minuta Napoli, Cruz, Abreu, & Del Grande, 2011; Bokermannohyla flavopictaLeite, Pezzuti, & Garcia, 2012; Nyctimantis galeata (Pombal, Menezes, Fontes, Nunes, Rocha, & Van Sluys, 2012); Proceratophrys redacta Teixeira, Amaro, Recoder, Vechio, & Rodrigues, 2012; Leptodactylus oreomantis Carvalho, Leite, & Pezzuti, 2013; Crossodactylodes itambe Barata, Santos, Leite, & Garcia, 2013; Scinax montivagus Juncá, Napoli, Nunes, Mercês, and Abreu, 2015; Odontophrynus juquinha Rocha, Sena, Pezzuti, Leite, Svartman, Rosset, Baldo, & Garcia, 2017; Physalaemus claptoniLeal, Leite, Costa, Nascimento, Lourenço, & Garcia, 2020; Pristimantis rupicolaTaucce, Nascimento, Trevisan, Leite, Santana, Haddad, & Napoli, 2020 (Figure 2C); Aplastodiscus heterophonicusPinheiro, Pezzuti, Berneck, Lyra, Lima, & Leite, 2021; Leptodactylus avivoca Carvalho, Seger, Magalhães, Lourenço, & Haddad, 2021; Proceratophrys velhochicoMângia, Magalhães, Leite, Cavalheri, & Garcia, 2022; and Crossodactylodes serranegraSantos, Pinheiro, Garcia, Griffiths, Haddad, & Barata, 2023].

In addition, new records of already known species have been accumulated over more than a decade since the last compilation. Six species considered of restricted distribution to the Espinhaço lost their endemic status. Baêta et al. (2009) demonstrated that Pithecopus itacolomi (Caramaschi, Cruz, & Feio, 2006), previously restricted to the Quadrilátero Ferrífero, is a junior synonym of Pithecopus ayeaye Lutz, 1966 and, therefore, is no longer a Espinhaço endemic since P. ayeaye also occurs in other mountainous regions of southeastern Brazil (Magalhães et al. 2017, Del Prette et al. 2024). Taucce et al. (2012), Silva et al. (2013), Thomé et al. (2016), and Santana et al. (2024) expanded the geographic distribution of Ischnocnema izecksohni (Caramaschi & Kisteumacher, 1989), Ololygon tripui (Lourenço, Nascimento, & Pires, 2010), Pleurodema alium Maciel & Nunes, 2010, and Sphaenorhynchus canga Araujo-Vieira, Lacerda, Pezzuti, Leite, Assis, & Cruz, 2015, respectively, far from the limits of Espinhaço Range. Finally, Corythomantis botoqueMarques, Haddad, & Garda, 2021 and Physalaemus orophilus Cassini, Cruz, & Caramaschi were described as endemic to the Espinhaço, but they also occur in Três Marias (Cerrado lowland, Minas Gerais state) and near Mantena (Atlantic Forest, Minas Gerai state), respectively, which are areas far from the mountain range (Cassini et al. 2010, Marques et al. 2021). Thus, these species are not truly endemic to the Espinhaço, despite their core distribution being within the mountain range. Additionally, the occurrence of P. orophilus near Mantena should warrants further investigation, as the geographic information and voucher from this locality are not listed in specimens examined in Cassini et al. (2010).

Bokermannohyla nanuzae (Bokermann & Sazima, 1973) was synonymized with Bokermannohyla feioi (Napoli & Caramaschi, 2004) by Walker et al. (2015), with the latter having been described from specimens from the Mantiqueira Range, Atlantic Forest domain. Although they overlap the morphological traits originally used to diagnose them (Walker et al. 2015), molecular data and spatially structured patterns of labial tooth row formula and larval coloration types supported the revalidation of B. feioi (Pezzuti et al. 2021, Brunes et al. 2023). Thus, populations of B. nanuzae were once again recognized as endemic to the Espinhaço Range. Despite the increase in studies that resulted in new descriptions of species, the anurofauna of Espinhaço is still not fully known. Brazil is the country with the greatest potential for future discoveries of species, including amphibians (Moura & Jetz 2021), and there are indications that Espinhaço may be a region of great interest and relevance in this regard. Studies have pointed to the existence of possibly new and endemic species, which still lack a formal description (see Pezzuti et al. 2021). Among these, we can mention two species of the genus Ischnocnema (Silveira et al. 2019), one Aplastodiscus aff. arildae (Silveira et al. 2019), one Ololygon aff. machadoi (Leite et al. 2019c, Pezzuti et al. 2021), two species of Proceratophrys (S. Mângia, personal information), three species related to Bokermannohyla saxicola (Oswald et al. 2022), and one to Odontophrynus aff. juquinha (Moroti et al. 2022).

The tadpoles of endemic species are relatively well known and only nine of them have not been described (i.e. Boana botumirim, Bokermannohyla juiju, B. sagarana, Scinax cabralensisDrummond, Baêta, & Pires, 2007, Leptodactylus avivoca, Physalaemus claptoni, P. deimaticus Sazima & Caramaschi, 1988, Proceratophrys redacta, and Crossodactylodes serranegra. As for bioacoustics, only four species do not have the call described (i.e. Boana cipoensis (Lutz, 1968), B. sagarana, C. serranegra, and P. deimaticus).

Of the 42 endemic species, 15 are restricted to Espinhaço Mineiro, 13 to Chapada Diamantina and three to the Quadrilátero Ferrífero (Table 1, Figure 7). Seven species are shared between Espinhaço Mineiro and Quadrilátero Ferrífero and three between Espinhaço Mineiro and Chapada Diamantina (Table 1, Figure 7). Scinax curicica Pugliese, Pombal, and Sazima, 2004 is the only species widely distributed in the three regions, from the Quadrilátero Ferrífero to the south of Chapada Diamantina, in the Pico da Almas region (Table 1, Figures 1, 7).

Figure 7
Venn-Euler diagram indicating the count of exclusive and shared endemic species in each portion of Serra do Espinhaço, in eastern Brazil. The central numbers in the circles indicate the count of species unique to each area and the numbers at the intersections indicate the count of endemic species shared by each delimited region. CD = Chapada Diamantina (blue); EM = Espinhaço Mineiro (orange); QFe = Quadrilátero Ferrífero (yellow).

The greatest richness of endemism is in the south of Espinhaço Mineiro, in areas that correspond to the Serra do Cipó, where a single square can harbor up to 20 endemic species (Figure 8). The southern region of Chapada Diamantina presents intermediate endemism, with a decrease towards the north of Bahia state. The same happens with the central region of Espinhaço Mineiro, which presents moderate values of endemism richness. This richness decreases towards the north of Minas Gerais state, except for the region of Rio Pardo de Minas, which has a high value for this index (Figure 8). Serra do Cabral also has moderate endemism.

Figure 8
Anuran endemism map in Espinhaço Range in 0.3° × 0.3° grids.

Differences in the number of endemic species may be related to the lower sampling effort carried out in the north of Espinhaço Mineiro and Chapada Diamantina in relation to the south of Espinhaço Mineiro and Quadrilátero Ferrífero (Leite et al. 2012). However, the greater endemism in Espinhaço Mineiro may not be just a sampling artifact and may be related to the geographic affinities of this area with the Atlantic Forest, the region with the richest anurofauna in the country (Rossa-Feres et al. 2017, Figueiredo et al. 2021), but this deserves further investigation.

^2.

Ecology, behaviour, and natural history

Anurans endemic to Espinhaço Range are present in grassland/shrublands or in gallery and hillside forests (Table 1). In these environments, they present at least 12 different reproductive modes, and for some of the species, reproductive aspects are not known that allow classification according to Haddad & Prado (2005) (Table 1). Eight reproductive modes reported for Espinhaço Range frogs are typical of Atlantic Forest lineages (modes 2, 3, 5, 19, 21, 25, 26, 28) and the others can be observed in both open and forested lineages (modes 1, 4, 11, 30; Haddad & Prado 2005). Only two species (Haddadus aramunha (Cassimiro, Verdade, & Rodrigues, 2008) and Pristimantis rupicola; Figure 2C-D)) show direct development, that is, the larval stage is suppressed. All other species need water bodies for reproduction (Table 1).

A high functional diversity of frogs has been recorded for Espinhaço Range, also reflecting the richness of reproductive environments and phylogenetic diversity. Pezzuti et al. (2021) found that the tadpoles of 67 species from the QF represent 12 of the 15 ecomorphological guilds of exotrophic tadpoles known to the world (Table 1; McDiarmid & Altig 1999). This diversity is considerably greater when compared to the tadpole fauna in other Brazilian regions, both in the Atlantic Forest (Fatorelli et al. 2018, Dubeux et al. 2020) and in the Cerrado (Rossa-Feres & Nomura 2006).

Streams and rivulets are abundant water bodies in the campo rupestre and several endemic species use them for reproduction and larval development (Eterovick & Barata 2006, Pezzuti et al. 2021). The stream volume, the presence and density of tadpole predators, the diversity of microhabitats, and the relative cover of marginal tree vegetation are important characteristics that determine the composition of larval assemblages (Eterovick & Barata 2006). Several species use stream backwaters for oviposition and/or larval development (Eterovick et al. 2020). As this resource is limited, it is common for males of the species that use them to defend these territories. Fidelity of reproductive habitats in lotic environments (Figures 9A, 10A) was reported for males of Bokermannohyla alvarengai (Figure 3C; Centeno et al. 2015a) and Pithecopus megacephalus (Miranda-Ribeiro, 1926) (Figure 9C; Oliveira et al. 2012). Males of B. alvarengai are larger than females, have hypertrophied prepollexes and forelimbs, do not aggregate spatially, and many of them have fight scars on the back (Sazima & Bokermann 1977, Centeno et al. 2015a, 2021), which reinforces the territoriality hypothesis. A similar pattern was observed for Bokermannohyla martinsi (Bokermann, 1964) (Figure 5B-C), in addition to the report of fighting between males (Magalhães et al. 2018). Therefore, it is possible that territoriality is a common behavioural aspect in Espinhaço stream species, as these habitats are essential for the reproduction of many endemic species (Table 1). Morphophysiological adaptations of amphibians to the environmental conditions of Espinhaço Range, such as high levels of solar radiation and extreme conditions of heat and cold are poorly known. Centeno et al. (2015b) investigated the morphology and biochemical aspects of lipid secretions from the skin of B. alvarengai, a species often found resting in sunlight for long periods of the day. This behaviour, called basking, involves changes in light reflectance through changes in skin colour which helps in the thermoregulation of the species (Eterovick et al. 2006, Centeno et al. 2015b). In addition, an extra-epidermal layer, formed by lipid compounds, on the dorsal surface of the animal, well-developed skin folds in the ventral region, and extensive hypervascularization, may play an important role in preventing excessive water loss and reabsorption (Centeno et al. 2015b). Similar adaptive strategies appear to be more common in species that occur in relatively high-altitude regions (Vences et al. 2002). The basking behaviour has already been reported for other species of the genus associated with rocky outcrops (Brandão et al. 2012) and, in Espinhaço, it was also observed in B. sagarana (T. L. Pezzuti, personal observation), which suggests that exposure to the sun is common in rupicolous species of the genus.

Figure 9
(A) Anuran reproductive environment in Itacambira, Minas Gerais; (B) Scinax curicica; (C) Adult, and (D) tadpole of Pithecopus megacephalus. Photos by Tiago L. Pezzuti.

Behavioural studies with tadpoles from endemic species to Espinhaço have demonstrated the adaptive value of coloration patterns to cryptic potential and defence strategies against visually oriented predators. Tadpoles of B. alvarengai (Figure 3D) and Ololygon machadoi (Bokermann & Sazima, 1973) present disruptive colours, due to the presence of golden spots and stripes that break the contour of the body, and when threatened, they choose areas of the stream that maximize their camouflage to the substrate (Eterovick et al. 2010; Espanha et al. 2016, Eterovick et al. 2018). However, such behaviour was not observed for non-disruptive colours tadpoles, such as B. saxicola (Bokermann, 1964) (Figure 4B) and B. martinsi (Figure 5D), that have light brown and dark colours, respectively (Espanha et al. 2016, Eterovick et al. 2018).

Other factors such as high solar incidence or shading of water bodies may be related to the selection of coloration patterns, such as the melanic patterns found in B. martinsi and B. nanuzae tadpoles (Leite & Eterovick 2010), as hypothesized for some mountainous lineages (Faivovich et al. 2013). These and other correlations between habitat use and adaptive strategies of tadpoles from campo rupestre, such as morphologies specialized to rapid streams, and types of development in cold environments, remain to be investigated.

^3.

Biogeography and evolution

Among the endemic species of Espinhaço Range, 65.1% (n = 28) have already been included in broad phylogenetic analyses, and in general presented robust topologies with well-supported nodes (e.g. Aplstodiscus heterophonicus (Pinheiro et al. 2021) and Physalaemus evangelistai (Lourenço et al. 2015)). Although few of these studies have reconstructed the biogeography of the sample groups (e.g. Carvalho et al. 2021, Vasconcellos et al. 2021), we can identify three hypothetical main origins for the endemic anurofauna of Espinhaço. In the first one, the endemic species are derived species in clades composed mostly or exclusively of Atlantic Forest species. Included in the group exclusively of Atlantic Forest are Aplastodiscus heterophonicus (Pinheiro et al. 2021), Crossodactylodes itambe, C. serranegra (Santos et al. 2020a, b, 2023), and in the group of mostly of Atlantic Forest are Thoropa megatympanum Caramaschi & Sazina, 1984 (Figure 4D; Sabbag et al. 2018), Physalaemus evangelistaiBokermann, 1967 (Lourenço et al. 2015), Proceratophrys cururu Eterovick & Sazima, 1998 (Magalhães et al. 2020, Mângia et al. 2020), and Phasmahyla jandaia (Bokermann & Sazima, 1978) (Faivovich et al. 2010). The origin of Pseudopaludicola mineira Lobo, 1994 appears to be the result of the occupation of Espinhaço by an ancestor of Cerrado savannas (Veiga-Menoncello 2014). Finally, Rupirana cardosoi corresponds to an autochthonous endemic genus, being considered a biogeographic relict (Fouquet et al. 2013, Santos et al. 2020a).

In some genera, there are clades composed exclusively of endemic species of the campo rupestre, whether restricted to Espinhaço or not. This is the case of the Physalaemus of the P. deimaticus clade, a monophyletic group that includes P. claptoni, P. deimaticus, P. erythros Caramaschi, Feio, & Guimarães, 2003, and P. rupestris Caramaschi, Carcerelli, & Feio, 1991, the first three being restricted to Espinhaço and the last one endemic to disjunctions of the campo rupestre in the Mantiqueira mountain complex (Lourenço et al. 2015, Leal et al. 2020). Another example includes Boana botumirim and B. cipoensis, sister species that share a Cerrado ancestor and speciate in the Espinhaço Mineiro (Vasconcellos et al. 2021). As the two species inhabit the campo rupestre lato sensu (Caramaschi et al. 2009, Eterovich et al. 2020), it is deduced that their common ancestor also inhabited this type of environment in Cerrado, since there are other areas with this ecosystem in the central region of Brazil (Silveira et al. 2016). It is possible that autochthonous speciation was also responsible for the origin of Proceratophrys minuta, P. redacta, and P. velhochico, a monophyletic and endemic clade to Chapada Diamantina (Magalhães et al. 2020, Mângia et al. 2020, 2022).

Carvalho et al. (2021) reconstructed the phylogeny and biogeography of the clade of Leptodactylus plaumanni Ahl, 1936, which has eight species and includes L. avivoca, L. camaquara, and L. oreomantis, all endemic to Espinhaço Range. According to the authors, the clade emerged in southern Espinhaço during the Miocene (~6.4 Ma; 95% HDP = 10.0-3.6 Ma), with L. camaquara being the first to diverge from the other species. Although the three species do not constitute a clade, the reconstruction of the ancestral areas of L. avivoca and L. oreomantis indicates that the diversification of both species occurred in Espinhaço Range, followed by the colonization of new mountain areas in Brazil, such as Chapada dos Veadeiros, Planalto Central, and Serra da Mantiqueira (e.g. L. tapitiSazima and Bokermann, 1978 and L. cunicularius), as well as low areas of the Atlantic Forest (e.g. L. marambaiae Izecksohn, 1976, which occurs in restingas, and L. plaumanni).

The clade of highland monkey frogs of the genus Pithecopus is composed of six species, with P. rohdei (Mertens, 1926) endemic to the Atlantic Forest (Ramos et al. 2019), P. rusticus (Bruschi, Lucas, Garcia, & Recco-Pimentel, 2014) restricted to natural grasslands in high areas in Santa Catarina (Bruschi et al. 2014, Ernetti et al. 2024), and P. ayeaye, P. centralis (Bokermann, 1965), P. megacephalus, and P. oreades (Brandão, 2002) endemic to the campo rupestre (Faivovich et al. 2010, Magalhães et al. 2018). Pithecopus megacephalus, the only one of these species endemic to Espinhaço Range (Table 1), is more closely related to the Atlantic Forest species than to the other rupicolous species, which form a monophyletic clade (Faivovich et al. 2010). Two biogeographic hypotheses could explain this pattern: (1) the clade has a rupicolous ancestor, and derived lineages expanded to the Atlantic Forest and south highlands or (2) the occupation of the campo rupestre occurred through two independent events, with an ancestor from the Atlantic Forest and an autochthonous diversification. It is notable that, despite not being sisters, the Pithecopus species endemic to the campo rupestre show a series of convergences, including the reticulate colour pattern (Faivovich et al. 2010), the reproductive mode (Table 1; sensu Haddad & Prado 2005), and K reproductive strategy instead of R strategy, which is more common in other species of the genus (Oliveira 2017, De Bastiani et al. 2024).

It can also be said that there are biogeographic uncertainties regarding the origin of Nyctimantis galeata. The tree frog is part of a genus with seven species, most of them associated with forests (Blotto et al. 2021, Frost 2024). Despite this, it integrates a clade with a species that is distributed in the Chaco and Pampas in Argentina, Paraguay, and Uruguay (i.e. N. siemersi (Mertens, 1937) (Cajade et al. 2010, Lajmanovích et al. 2012)), one in the Western Amazon (i.e. N. rugiceps Boulenger, 1882 (Frost 2024)), two species from the Atlantic Forest (i.e. N. bokermanni (Pombal, 1993) and N. pomba (Assis, Santana, Silva, Quintela, & Feio, 2013) (Frost 2024)), and one with distribution in Cerrado forests (i.e. Nyctimantis diadorim Brandão et al. 2024), being the sister of a clade formed by the latter plus N. pomba (Blotto et al. 2021). In this case, it is possible that the ancestral lineage of N. galeata occupied Espinhaço and subsequently spread to the Cerrado and the Atlantic Forest, or that it colonized the campo rupestre from one of these domains. Although aspects of the natural history of N. galeata are poorly known, recent studies indicate that the species prefers open areas (Dias et al. 2020, Magalhães et al. 2021), a characteristic shared, in part, only with N. siemersi (Lajmanovích et al. 2012).

Odontophrynus juquinha is sister of O. toledoi Moroti, Pedrozo, Severgnini, Augusto-Alves, Dena, Martins, Nunes, and Muscat, 2022, distributed in highlands of Serra da Mantiqueira, Atlantic Forest (Moroti et al. 2022). These two frogs form a clade that includes taxa mostly distributed in open subtropical areas of South America (Rosset et al. 2006, Moroti et al. 2022). This pattern of relationship between Espinhaço Range and subtropical domains, such as the Pampas or the Chaco, has already been observed for lineages of Julianus pinimus (Bokermann & Sazima, 1973) (Baldo et al. 2019) and Scinax squalirostris (Lutz, 1925) (Abreu-Jardim et al. 2021). However, it is not known which processes resulted in the occupation of these environments by these species.

Pristimantis rupicola represents a biogeographical enigma. The species is a sister to P. gaigei (Dunn, 1931), a leaf litter frog distributed in tropical forests of Costa Rica, Panama, and Colombia (Taucce et al. 2020, Frost 2024). The only other rupestrian species of the genus, P. hoogmoedi Kaiser, Barrio-Amorós, Rivas-Fuenmayor, Steinlein, andSchmid, 2015, does not seem closely related to P. rupicola, as do the other species that inhabit Brazil (Taucce et al. 2020). Therefore, understanding the occupation of Espinhaço Range by P. rupicola is essential to elucidate the origins and processes that resulted in the diversification of the anurofauna endemic to the region.

The Scinaxini tribe has four endemic representatives in Espinhaço Range. Scinax curicica (Figure 9B) is part of a clade with a large polytomy within S. granulatus group (Araujo-Vieira et al. 2023) with species from different domains and physiognomies, such as Pampa [e.g. S. granulatus (Peters, 1871)], Cerrado [S. tigrinus Nunes, Carvalho, and Pereira, 2010], other open areas [e.g. S. rossaferesae Conte, Araújo-Vieira, Crivellari, & Berneck, 2016 and S. caldarum (Lutz, 1968)], Atlantic Forest [e.g. S. duartei (Lutz, 1951)], and campo rupestre (e.g. S. curicica and S. maracaya (Cardoso and Sazima, 1980)). This phylogenetic uncertainty makes it difficult to provide a hypothesis for the origin of species endemic to the Espinhaço. Scinax cabralensis and S. montivagus are also nested within S. granulatus group (Araújo-Vieira et al. 2023), in a clade in which most species probably originated in Atlantic Forest, while others may have originated from an ancestor from the Cerrado, suggesting that the ancestors of the two species may have colonized campo rupestre from both domains. Ololygon machadoi may have originated from an ancestor from the Atlantic Forest. The species forms a clade with some candidate new species, being that poorly supported as a sister species of Ololygon catharinae (Boulenger, 1888) (Araújo-Vieira et al. 2023). Ololygon machadoi + O. catharinae is sister of two clades, one composed by species distributed in Atlantic Forest and other with species from gallery forests in the Cerrado and transitional areas with Atlantic Forest.

Haddadus aramunha is endemic to the campo rupestre in Chapada Diamantina and is one of the only craugastorids that occupy open areas, since most of the group inhabits forests (Cassimiro et al. 2008, Amaro et al. 2013). The genus includes other two species, H. binotatus (Spix, 1824) and H. plicifer (Boulenger, 1888), both with distribution in Atlantic Forest (Frost 2024). Despite some recent phylogenies include this genus (e.g. Portik et al. 2023), H. plicifer was not sampled in any of them. Despite this, the genus may have emerged in the campo rupestre and spread to the Atlantic Forest or vice versa.

Bokermannohyla is a genus composed of 31 species (Frost 2024), being the most diversified in Espinhaço Range, with 10 endemic species (Table 1). Interestingly, the phylogenetic relationship of these species has not yet been tested, but it is possible that the region is a centre of diversification for the genus. Representatives of the Hylodidae family endemic to Espinhaço (Table 1) were also not included in comprehensive phylogenies. Despite this, as most members of this family are found in the Atlantic Forest (Frost 2024), it is likely that the ancestors of Crossodactylus trachystomus (Reinhardt & Lütken, 1862), Hylodes uai Nascimento, Pombal, & Haddad, 2001, and H. otavioi Sazima & Bokermann, 1983 originated from this domain (Heyer 1999).

The origin of endemic frogs was not concomitant with the emergence of Espinhaço Range. The region has a Pre-Cambrian origin and is currently experiencing long-term geological stability (Saadi 1995, Alkmin 2012). Few studies have investigated the time of diversification of endemic species; however, they have estimated relatively recent dates, between the Miocene and Pleistocene (e.g. Sabbag et al. 2018, Santos et al. 2020a, Carvalho et al. 2021, Oliveira et al. 2021). Moreover, the number of phylogeographic studies has grown in recent years (e.g. Oliveira et al. 2021, Magalhães et al. 2021, Oswald et al. 2022, Santana et al. 2024). Despite this, they are still scarce, and much evidence is lacking to improve the understanding of the diversification processes that led to the high richness of endemism in Espinhaço Range (Miola et al. 2021). Distinct and independent processes have been reported as important for the diversification and evolution of the Espinhaço anurofauna, suggesting multiple pulses of diversification throughout its history. The colonization of new areas, for example, was the main process evoked to explain the current geographic distribution of the genetic diversity of B. alvarengai and B. saxicola (Oliveira et al. 2021, Oswald et al. 2022). Fragmentation, an important process for the evolution of several plant species (Silveira et al. 2020), is also involved in the diversification of Crossodactylodes itambe and Rupirana cardosoi (Santos et al. 2020a). On the other hand, gene flow, between different lineages or with non-endemic species, also seems to influence current diversity, having been identified between Pithecopus megacephalus and P. ayeaye (Magalhães et al. 2021).

Although the processes involved in diversification and cladogenetic events do not appear to be coincident among the different endemic species, some spatial patterns have been recovered in recent phylogeographic research (e.g. Ramos et al. 2018, Sabbag et al. 2018, Oliveira et al. 2021, Oswald et al. 2022, Santana et al. 2024). The most recurrent of these phylogeographic breaks is the depression between the Diamantina plateau and the Serra de Itacambira (16S and 42W), in Espinhaço Mineiro, known as the Couto de Magalhães Depression (Figure 1; Saadi 1995). This barrier was observed in Pithecopus megacephalus, in Thoropa megatympanum, and in Scinax curicica (Ramos et al. 2018, Sabbag et al. 2018, Santana et al. 2024). Although Bokermannohyla saxicola and B. alvarengai present structure in this same region, the exact location of the barrier is not identical between them (Nascimento et al. 2018, Oliveira et al. 2021). Biological aspects and the natural history of the species may be related to these differences, but the region and the species must be better investigated to understand the evolution there.

Another phylogeographic barrier is the depression between the Chapada Diamantina and the Espinhaço Mineiro. In addition to the different endemic species occurring in the two portions (Figure 7, Table 1), studies have revealed different lineages of S. curicica and O. juquinha in the two portions (Moroti et al. 2022, Santana et al. 2024). This deserves further and integrative investigation to confirm whether they are distinct species. The low areas between Serra do Cabral and the central ridge of Espinhaço Mineiro (Figure 1) may have acted as a continuous barrier between different populations and species. It seems to be an important limit for the distribution of some anuran species along the Espinhaço. Bokermannohyla sagarana and S. cabralensis (Figure 4C), for example, are restricted to Serra do Cabral, while B. alvarengai, B. nanuzae, and S. curicica do not occur in this mountain range (Oliveira et al. 2021, Santana et al. 2024). Although other species, such as B. saxicola and T. megatympanum, are widely distributed in Serra do Cabral and in the central ridge of Espinhaço Mineiro, there are genetic structure in populations between these areas (Sabbag 2013, Oswald et al. 2022).

^4.

Conservation

Amphibians are indicator species and are sensitive to environmental changes (Hopkins 2007). Their reproduction strategies, behaviour, and physiology make them vulnerable to different threats at different life stages (Bolochio et al. 2020). As a result, approximately 41% of the world’s amphibian species are under some degree of threat (Luedtke et al. 2023). In the Espinhaço Range, among the endemic species, 12 (28.6%) are categorized in some level of threat of extinction in IUCN assessment (Table 2; IUCN 2023). Another five (i.e. B. flavopicta, C. trachystomus, L. camaquara, P. erythros, and P. evangelistai) are categorized as near threatened (Table 2; IUCN 2023). The Brazilian Red List (Brasil 2022, ICMBio 2024), which had assessments carried out between 2017 and 2018, includes Crossodactylus itambe in the list of threatened species, as Critically Endangered, and Bokermannohyla flavopicta (Figure 10B), B. sagarana, Hylodes otavioi, and S. cabralensis in the list of Near Threatened (Brasil 2022, ICMBio 2024). The landscape in Espinhaço Range is undergoing constant changes, and the difference in assessment between the national and global red lists may reflect these, since the lists were elaborated five years apart. However, this may not be the only reason for this instability, and the lists and assessment need to be compared more closely.

Table 2
Endemic species, threat categories in the latest IUCN (2023) and Brazilian (Brasil 2022) assessments, and occurrence within fully Protected Areas (PA). Threat Categories: LC = Least Concern, NE = Not Evaluated, NT = Near Threatened, EN = Endangered, CR = Critically Endangered, DD = Data Deficient. National Protected Area in Minas Gerais: 1 – Parque Nacional (PARNA) da Serra do Gandarela, 2 – PARNA da Serra do Cipó, 3 – PARNA das Sempre-Vivas, in Bahia: 4 – PARNA da Chapada Diamantina, 5 – PARNA do Boqueirão da Onça; Regional Protected area: Minas Gerais: 1 – Parque Estadual (PE) da Serra do Ouro Branco, 2 – Monumento Natural Estadual (MONA) do Itatiaia, 3 – PE do Itacolomi, 4 – Estação Ecológica (EE) do Tripuí, 5 – MONA da Serra da Moeda, 6 – EE de Arêdes, 7 – EE dos Fechos, 8 – PE da Serra do Rola Moça, 9 – EE do Cercadinho, 10 – PE do Limoeiro, 11 – PE da Serra do Intendente, 12 – MONA da Várzea do Lageado, 13 – PE do Pico do Itambé, 14 – PE do Rio Preto, 15 – PE Biribiri, 16 – PE da Serra do Cabral, 17 – PE da Serra Negra, 18 – PE de Botumirim, 19 – EE de Acauã, 20 – PE de Grão Mogol, 21 – PE de Serra Nova e Talhado, 22 – PE de Montezuma, 23 – EE Mata dos Ausentes, 24 – PE Serra Verde, 25 – PE Serra do Sobrado, 26 – PE Cerca Grande, 27 – PE Caminho das Gerais, 28 – PE Sumidouro, 29 – MONA Serra do Gambá, 30 – MONA Gruta Rei do Mato, 31 – MONA Experiência do Jaguara, 32 – MONA Peter Lund, 33 – MONA Santo Antônio, 34 – MONA Lapa Vermelha, 35 – MONA Vargem da Pedra, 36 – MONA Várzea da Lapa, 37 - Refúgio de Vida Silvestre (REVIS) Estadual Macaúbas, 38 – REVIS Estadual Serra das Aroeiras; Bahia: 39 – PE do Morro do Chapéu, 40 – PE das Sete Passagens, 41 – MONA da Cachoeira do Ferro Doido, 42 – REVIS da Serra dos Montes Altos, 43 – PE da Serra dos Montes Altos.

Taxon	Red List		Presence in Protected area
	IUCN 2023	Brazil 2022	Federal	Regional
Craugastoridae
Haddadus aramunha	VU	LC	4	40
Cycloramphidae
Thoropa megatympanum	LC	LC	2, 3	11, 13, 14, 16, 17, 18, 20, 21
Hylidae
Aplastodiscus heterophonicus	NE	NE	–	–
Boana botumirim	LC	LC	3	13, 14 16, 18, 21
Boana cipoensis	LC	LC	2	11
Bokermannohyla alvarengai	LC	LC	1, 2, 3	1, 11, 13, 14, 18, 20, 21, 27
Bokermannohyla diamantina	LC	LC	–	21, 42
Bokermannohyla flavopicta	NT	NT	–	–
Bokermannohyla itapoty	LC	LC	4	–
Bokermannohyla juiju	EN	LC	4	–
Bokermannohyla martinsi	VU	NT	1	1, 2, 3, 5
Bokermannohyla nanuzae	LC	LC	2, 3	11, 13, 14, 17
Bokermannohyla oxente	LC	LC	4	40
Bokermannohyla sagarana	EN	NT	–	16
Bokermannohyla saxicola	LC	LC	1, 2, 3	11, 13, 14, 15, 16, 17, 18, 19, 20, 21
Nyctimantis galeata	EN	DD	–	41
Ololygon machadoi	LC	LC		11, 13, 14, 16, 17, 18, 20, 21
Phasmahyla jandaia	LC	LC	1	1
Pithecopus megacephalus	LC	LC	2, 3	11, 14, 18, 20, 21
Scinax cabralensis	EN	NT	–	16
Scinax curicica	LC	LC	1, 2, 3, 4	1, 2, 3, 11, 13, 14
Scinax montivagus	LC	LC	4	40, 41
Hylodidae
Crossodactylus trachystomus	NT	LC	2, 3	1, 13, 14, 21
Hylodes otavioi	VU	NT	–	11
Hylodes uai	VU	LC	–	3
Leptodactylidae
Crossodactylodes itambe	CR	CR	–	13
Crossodactylodes serranegra	NE	NE	–	17
Leptodactylus avivoca	NE	NE	3	21
Leptodactylus camaquara	NT	LC	2, 3	11, 13, 14, 18, 20, 21
Leptodactylus oreomantis	LC	LC	4	–
Physalaemus claptoni	DD	NE	–	–
Physalaemus deimaticus	LC	LC	2	13
Physalaemus erythros	NT	LC	1	3
Physalaemus evangelistai	NT	LC	1, 2	1, 3, 11, 14
Pseudopaludicola mineira	LC	LC	2, 3	11, 13, 14, 16
Rupirana cardosoi	VU	LC	4	39, 41
Odontophrynidae
Odontophrynus juquinha	LC	LC	–	11, 18, 21
Proceratophrys cururu	VU	LC	2, 3	11, 13, 14
Proceratophrys minuta	LC	LC	4	40
Proceratophrys redacta	EN	LC	–	39, 41
Proceratophrys velhochico	NE	NE	–	–
Strabomantidae
Pristimantis rupicola	NE	NE	–	–

Figure 10
(A) Anuran reproductive environment in Chapada Diamantina, Bahia, Brazil; (B) Bokermannohyla flavopicta; (C) Bokermannohyla itapoty; (D) Egg clutch of Bokermannohyla sp. Photos by A-B. Leandro Drummond; C-D Tiago L. Pezzuti.

Habitat loss and fragmentation are major threats to amphibian distribution and persistence (Baillie 2004), and this is not different in Espinhaço Range. Most of threatened species in this mountain range suffer a continuous decline in their areas of occupancy and in the quality of their habitats, highlighted by the most used criteria to categorize these species (i.e. B1ab criteria - Geographic range in the form of either extant of occurrence and/or area of occupancy; Brasil 2022, IUCN 2023). Threats to the integrity and quality of habitats and the persistence of anurans endemic to the Espinhaço may vary in source and intensity, according to the particularities of the places where they are distributed. The campo rupestre is under great pressure from activities such as mining, silviculture, agriculture, and urbanization (Fernandes et al. 2018), activities that are harmful to the quality of anuran habitats distributed there. Serra do Cabral, for example, is heavily used for the cultivation of Eucalyptus and Pinus. Even with a protected area (i.e. Parque Estadual da Serra do Cabral) in the region, these activities are significantly altering the landscapes and have been identified as the main threats to B. sagarana populations (Leite et al. 2011). Similarly, human activities in Serra do Cabral may be threatening other species distributed in the area, including the genetic diversity of species distributed in other regions of Espinhaço (Sabbag 2013, Oswald et al. 2022) and other restricted ones, such as Scinax cabralensis (Drummond et al. 2007).

Phytotelmata species, such as Crossodactylodes itambe and C. serranegra, suffer additional threats to the extent and quality of their habitat as the plants with which they are associated (i.e. bromeliads) suffer natural or anthropic impacts. Fire and the selective removal of commercially valuable plants can decimate the microhabitats where the species lives and reproduces (Barata et al. 2013 Santos et al. 2020a). Despite the fire being pointed out as a threat to some anuran species from campo rupestre, when Drummond et al. (2018) analyzed an area of Parque Estadual do Itacolomi, they found an increase in the total richness of the anuran assemblage after a fire event. The authors suggest that generalist species occupied post-fire areas and that the heterogeneity of the campo rupestre may provide different local environments for frogs protect themselves from fires (Drummond et al. 2018). However, this is a one-off observation, and this may not be generalized to non-generalists’ species, other sites, and/or assemblies in Espinhaço Range. Landscapes of scenic beauty and waterfalls along the Espinhaço Range attract countless people annually. However, disordered, and unregulated tourism can negatively affect the habitats of campo rupestre species, as identified for Bokermannohyla juiju (Taucce et al. 2015) and B. flavopicta (Figure 10B; Leite et al. 2012).

The chytrid fungus [Batrachochytrium dendrobatidis (Bd)], responsible for causing large declines in anurans populations around the globe (Berger et al. 2016), adds to the list of threats identified to endemic anurans of Espinhaço. Amorim et al. (2019) found positive samples for the fungus in Chapada Diamantina, in Rhinella rubescens (Lutz, 1925) and in tadpoles of an unidentified Bokermannohyla. However, little is known about the distribution of Bd along the mountain range and how it is affecting endemic species. Added to these direct threats, climate change could play a crucial role in the loss of the campo rupestre by 2070, with an estimated retraction of 68% of the current areas climatically suitable for the ecosystem (Fernandes et al. 2018), causing fragmentation and habitat loss of endemic anurans of the Espinhaço range.

Species with restricted distribution are more vulnerable to extinctions (Sodhi et al. 2008, González-del-Pliego 2019), and therefore, conservation actions are necessary. Given the diversity of herpetofauna, knowledge gaps, and high threat, a National Action Plan (PAN for the conservation of endangered reptiles and amphibians in Espinhaço Range) was proposed in 2012 to increase knowledge about target species and minimize the effect of human actions on them (ICMBio 2012). The first cycle of the PAN Herpetofauna do Espinhaço Mineiro ended in 2017 with 55% of the actions completed, so in 2018 a second cycle was approved, with the objective of implementing measures that favour the conservation of species and their habitats (ICMBio 2018).

One of the ways to minimize threats and guarantee the conservation of biodiversity has been the creation of Protected Areas. Espinhaço Range has a wide network of fully Protected Areas (PAs) (IUCN categories I-IV; Brasil 2000), such as national and regional parks, natural monuments, and ecological stations. In all, 48 Fully Protection PAs are distributed along the Espinhaço Range, of which five have federal and 43 regional administrations (Table 2; MMA 2021a). The portion of Espinhaço in Minas Gerais state (Espinhaço Mineiro and Quadrilátero Ferrífero) has three federal and 38 regional PAs, while the portion in Bahia has two federal and five regional PAs (Table 2). However, not all PA have records of species endemic to the Espinhaço Range (Table 2). In view of the set of PAs in the Espinhaço Range, mosaics were proposed with the objective of creating integrated management between PA managers and the local population, to make compatible, integrate and optimize activities developed in the PAs with the aim of maintaining biodiversity, socio-diversity, and regional sustainable development (MMA 2021b). Three mosaics were recognized by the Environment Ministry for the Espinhaço Range area: (1) Espinhaço – Alto Jequitinhonha – Serra do Cabral Mosaic by ordinance n° 444 (Brasil 2010); (2) Serra do Cipó Mosaic by ordinance No. 368 (Brasil 2018a), and (3) Serra do Espinhaço – Quadrilátero Ferrífero Mosaic, through ordinance No. 473 (Brasil 2018b). Despite the high number of PAs, few species were evaluated for distribution within their limits (e.g. Barata et al. 2016; Ramos et al. 2018). Among the species restricted to the Espinhaço range, only six were not sampled in any PA of integral protection, while 10 species were sampled in only one (Table 2). However, the presence in PAs does not guarantee, in isolation, the effective protection of the species that occur in them, especially in non-forest areas such as the campo rupestre (Françoso et al. 2015, Geldmann et al. 2019). Many protected areas in Brazil suffer from external pressures and incompatible uses in their surroundings, in addition to the lack of human and financial resources, land regularization and adequate demarcation, directly compromising the effective protection of biodiversity (ICMBio & WWF 2010). Even for those areas without governance problems and effectively protected, diseases, overexploitation, effects of climate change and other human activities can affect the anuran species (Luedke et al. 2023). Mining activity, for example, is present in several key areas for the conservation of biodiversity and PAs of Espinhaço and in their surroundings, chronically contaminating water bodies through the continued deposition of tailings (Kamino et al. 2020).

The exploitation of species can significantly threaten amphibians, especially when combined with other factors, such as habitat loss, however, limited information is available, and therefore the real impact of the use and trade of species on their conservation status (Luedtke et al. 2023). Distinct Brazilian amphibian species have been identified in hunting events and pet trade (Maximo et al. 2021, Nehemy et al. 2022, Bizri et al. 2024), but among them, no endemic species of the Espinhaço range was identified. Despite the current lack of records, some Espinhaço endemics species were identified as potential for future trade (Mohanty & Measey 2019), therefore monitoring and inspection must be constant to prevent and avoid this.

The research focused on the conservation of endemic amphibians’ species to Espinhaço has emerged in recent years, including investigations into effectiveness of PA in safeguarding endemic amphibians (Barata et al. 2016), conservation genetics (Eterovick et al. 2016, Ramos et al. 2018), and the effects of environmental stressors on the ontogeny of adults and tadpoles (Eterovick et al. 2016, Lima et al. 2019), but they are still scarce.

Conclusion

Espinhaço Range is considered a natural laboratory for ecology and evolution research (Silveira et al. 2016, Miola et al. 2021). Despite this, knowledge on biological aspects of endemic anuran species to the area is still scarce. Many of the studies on ecology, evolution, biogeography, and conservation are incipient, revealing the need and opportunities for scientific investigations. There are still no studies on the effects of environmental gradients (e.g. altitudinal and latitudinal) on amphibian diversity in the region, for example. There is also a great lack of research on adaptations of endemic species to the environmental conditions of the campo rupestre (Miola et al. 2021). The lack of basic data on the biology of endemic species as well as undescribed endemic species are a worrying factor for the conservation and maintenance of the local fauna. With this paper, we emphasize the importance of periodic compilations to update the state of knowledge of the endemic species of Espinhaço Range, and we hope to facilitate and encourage the realization of new studies in the region.

Acknowledgments

We thank Marcus Tadeu T. Santos for reviewing and contributing to the text. CBO thanks FAPEMIG and CAPES for their doctoral scholarships. TLP thanks CAPES for the PNPD grant (88887.468027/2019-00). FSFL thanks FAPEMIG and Fundação Vale (FAPEMIG/VALE: RDP-00004-17) and FAPEMIG (APQ-01796-15; APQ-00413-16). RFM thanks FAPEMIG (APQ-00325-21) and UFSJ (APO209) for research funding.

Data Availability

Supporting data are available at https://doi.org/10.48331/ scielodata.FDXSI7.

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Edited by

• Associate Editor
  Denise de Cerqueira Rossa-Feres

Publication Dates

• Publication in this collection
  27 Jan 2025
• Date of issue
  2024

History

• Received
  12 Apr 2024
• Accepted
  27 Nov 2024