Characterization of anuran fauna inside caves in Brazil

Caracterização da anurofauna no interior de cavernas no Brasil

Abstract:

The natural underground environment has unique characteristics when compared to surface environments. These environments feature a reduced complexity food web that includes organisms such as anuran amphibians. This study examines the occurrence of Neotropical anurans in Brazilian caves, utilizing taxonomic, geographic, geological, and environmental data extracted from the scientific literature. A total of 247 anuran records were found in caves across 18 scientific papers covering a 42-years period (from 1980 to 2022). Of these, 177 records (71.6%) displayed the anurans identified to the species level (54 species), with the families Leptodactylidae (13 species; 24.1%), Hylidae (12; 22.2%), and Bufonidae (10; 18.5%) being the most frequently recorded. The anuran records were predominant in the states of Minas Gerais (81 records; 34.8%) and São Paulo (35; 15.0%). The Atlantic Forest had the highest number of records (78; 33.5%), followed by ecotonal zones between the Atlantic Forest and Cerrado (43; 18.5%). Environmental information was scarce in the consulted records, with only 12 providing detail about the cave light zone where the anuran was found (nine in the entrance zone) and 63 indicating the presence/absence of water bodies. Carbonaceous (109; 46.8%) and ferruginous (76; 33.9%) lithology predominated among the caves considered. The low number of sampled caves (55 caves; 0.24%) compared to the total number of caves registered in Brazil (23,278 caves) underscores a knowledge gap regarding Neotropical anurans use of subterranean habitats.

Keywords:
Atlantic Forest; carbonate geology; ecotone; Leptodactylidae; Linnean shortfall; Neotropical region

Resumo:

O ambiente subterrâneo natural possui características únicas quando comparado aos ambientes de superfície. Nesses ambientes, a teia alimentar é simplificada, mas inclui organismos como os anfíbios anuros. Neste estudo é caracterizada a presença de anuros em cavernas na região Neotropical brasileira considerando informações taxonômicas, geográficas, geológicas e ambientais extraídas da literatura científica consultada. Foram encontrados um total de 247 registros de anuros em cavernas, em 18 artigos científicos abrangendo um período de 42 anos. Desse total de registros, 177 (71,6%) apresentaram identificação até o nível de espécie (54 espécies) com destaque para as famílias Leptodactylidae (13 espécies; 24,1%), Hylidae (12; 22,2%) e Bufonidae (10; 18,5%). Os registros de anuros são predominantes nos estados de Minas Gerais (81 registros; 34,8%) e São Paulo (35; 15,0%). O bioma com o maior número de registros é a Mata Atlântica com 78 (33,5%) seguido por zonas ecotonais entre a Mata Atlântica e Cerrado (43 registros; 18,5%). As informações ambientais são escassas nos registros consultados, 12 continham informações sobre a zona de luz da caverna onde o anuro foi encontrado (9 na zona de entrada) e 63 com informações sobre a presença/ausência de corpos d’água na caverna. A litologia carbonática (109; 46,8%) e ferruginosa (76; 33,9%) das cavernas é predominante. O número de cavernas amostradas é baixo (55 cavernas; 0,24%) comparado ao número total de cavernas registradas no Brasil (23.278 cavernas), evidenciando uma lacuna de conhecimento sobre o uso de habitats subterrâneos por anuros neotropicais.

Palavras-chave:
Floresta Atlântica; geologia carbonática; ecótono; Leptodactylidae; lacuna Lineana; região Neotropical

Introduction

Caves are natural subterranean cavities that make up the karst systems, originating from the chemical and physical dissolution of the matrix rock (Gibert et al. 1994). In Brazil, there are records of 23,278 caves accessible to humans (BRASIL, 2008; 2022) out of an estimated total of 100,000 caves (Brasil 2022). Caves have internal characteristics that interact with the external environment, creating photic and aphotic zones. The deeper parts of the cave are aphotic and have a stable average temperature and near-saturation humidity (Culver 1982, Culver & Pipan 2009, Tobin et al. 2013). The absence of natural light leads to the total or partial lack of photosynthetic organisms, limiting primary production. Consequently, available energy within the cave is derived from organic matter originating from the epigean environment, transported by physical and biological agents (Simon et al. 2007). Energy availability varies with cave geomorphology, resulting in unique conditions for each cave due to specific interactions with epigean ecosystems (Poulson & White 1969, Souza Silva et al. 2015, Pellegrini et al. 2016). The cave entrance modulates various characteristics, including nutrient input, acting as a filter for animals that are forcibly introduced by water or floods. These animals may temporarily inhabit the cave environment (Simões et al. 2015). The cave entrance and its surrounding area can serve as nesting sites for birds, pollinating insects, and small non-flying mammals. This shaded area with mild conditions also provides shelter for various animals (Boulton et al. 2008, Medellin et al. 2017).

Cave communities are classified based on species characteristics (morphological, physiological, evolutionary, and behavioral) and their affinity for subterranean habitats (Sket 2008, Culver & Pipan 2009, Díaz 2009). According to Sket (2008), based on the Schinner-Racovitza proposal, organisms are classified as follows: i) trogloxenes, animals regularly found in the underground environment but requiring the surface to complete their life cycle; ii) troglophiles, animals with an affinity for caves, possessing both underground and epigean populations, and potentially completing their life cycle entirely within cavities; iii) troglobites, obligate subterranean species exhibiting morphological, behavioral, and physiological adaptations to the hypogean environment, typically restricted to a specific cave; iv) “accidentals”, animals lacking pre-adaptations, inadvertently entering the underground environment and failing to establish themselves (Barr 1968, Sket 2008, Juan et al. 2010).

Anurans and reptiles are among the animals categorized as “accidental”’ cave fauna, despite recent findings indicating that herpetofauna may systematically utilize these environments (Martins de Andrade et al. 2021, Dos Santos et al. 2022a, b). Concerning amphibians, several species exhibit an affinity for cave-dwelling environments. For instance, Litoria cavernicola Tyler and Davies, 1979 inhabits sandstone caves in Australia, Rana italica Dubois, 1987 is found in Italian caves (Lunghi et al. 2018), Eleutherodactylus cavernicola Lynn, 1954 is endemic to Jamaican caves (Stanley et al. 2021), and Craugastor pelorus Campbell and Savage, 2000 occurs in southern Mexican caves (Couto et al. 2023). In Brazil, Pristimantis cf. fenestratus (Steindachner, 1864) has been classified as a trogloxene in Pará State caves (Trevelin et al. 2021). Additionally, Bokermannohyla martinsi (Bokermann, 1964) exhibits a strong affinity for caves in Minas Gerais (Martins de Andrade et al. 2021). Moreover, Oreobates antrum Vaz-Silva, Maciel, Andrade, and Amaro, 2018 has been described from northwestern Goiás State, inhabiting rocky environments and limestone outcrops, including caves, where it is commonly known as “rãzinha das cavernas” (Vaz-Silva et al. 2020); this species was also recorded in southwestern Tocantins caves (Motta et al. 2020).

Knowledge of the distribution patterns and composition of the cave community is an important tool for measuring the importance of caves as an element of the landscape (Gibert & Deharveng 1994, 2002). The knowledge about tropical cave fauna is still incipient when compared to that of temperate regions. In the last two decades, there has been a significant increase in the number of Brazilian biospeleological studies. These studies have addressed the fauna of invertebrates and cave-dwelling vertebrates (Delgado-Jaramillo et al. 2018, Parizotto et al. 2017, Gallão & Bichuette 2018). Despite this, there are many knowledge gaps (sensu Hortal et al. 2015) in studies of Brazilian anurofauna in caves, with few studies addressing this topic (Guerra et al. 2018, Bichuette et al. 2022). This study aimed to evaluate the obtained scientific knowledge of anurans recorded in Brazilian neotropical caves considering taxonomic, geographic, geological, and environmental data.

Material and Methods

Records from the literature on anurans inhabiting natural cavities within the Brazilian Neotropical region were utilized. The selected scientific publications, including full papers, scientific notes, master’s and doctoral thesis, and book chapters, were published up to December 2022. Google Scholar, Scopus, Web of Science, and AmphibiaWeb, recognized repositories of scientific literature (Falagas et al. 2008, Repiso-Caballero & Delgado-López-Cózar 2013, Martín-Martín et al. 2021), served as the search platforms. Employing multiple databases in the systematic search helped mitigate bias in data collection and subsequent interpretation (Archambault et al. 2009, Mongeon & Paul-Hus 2016).

Keywords were used to search for scientific literature in the indicated repositories, both individually and in combination, without initial time constraints (Silva & Bianchi, 2001, Silva et al. 2011). Individual search keywords included: “anura”, “anurans”, “amphibians”, “frogs”, “Brazilian caves” “underground cavities”, “underground habitat”, “underground environment”, “grotto”, “gruna”, “toca”, “subterranean cavities”, “subterranean habitat”, “subterranean environment”, and “burrow” (all terms were researched with their variations in Portuguese and English). Additionally, combined search keywords, such as “anurans in Brazilian caves” or “frogs in underground cavities” were created through keyword interpolation.

Each record of a species or location identified in the selected literature was treated as an independent unit of data. Consequently, the total number of records represents the sum of these individual records compiled up to December 2022. The collected data included taxonomic (order, family, genus, and specific epithet), geographic (State, municipality, name of the cave, and biome), geological (type of cave lithology), environmental (location of the sampled anuran in the photic (entrance), dim, or aphotic zone; presence of water), and scientific literature information (publication type (full article, short communication, textbook, master’s or doctoral thesis); focus of the study; year of publication). Natural cavities were identified based on explicit cave names from the literature selected, geographic coordinates, or consultation of the Registro Nacional de Informações Espeleológicas (Brasil, 2022). The total number of Brazilian natural cavities was sourced from the Cadastro Nacional de Informações Espeleológicas (Brasil, 2022). In all cases, the absence of information was identified as “not described” (ND). This data formed a general matrix (Appendix I).

The data matrix for descriptive analysis considered only records with identification at the specific epithet level, excluding those identified at the family, genus, or morphotype level. Species nomenclature was verified and updated as needed using the website database Amphibian Species of the World 6.1 (Frost, 2023), and identification guides by Haddad et al. (2008), Freitas (2015), and Vaz-Silva et al. (2020).

The descriptive analysis of the data matrix involved categories of nominal (order, family, genus, specific epithet, cave, State, municipality, lithology, biome, presence or absence of water, type of publication, focus of the study) and ordinal variables (photic zone and year of publication) (Reis & Reis 2002, Silvestre 2007) extracted from each independent record (Table 1). These records reflect individual observations of specimens in the cave environment, thus, the repetition of specific epithets does not indicate species richness, as multiple records for the same species may exist.

Table 1
Absolute and relative frequencies of independent records for nominal and ordinal variables extracted from 18 scientific literature about anuran from Brazilians caves published between 1980 and 2022.

Variable	Absolute	Relative (%)
Order	247	100
Family	240	97.2
Genus	233	94.3
Specific epithet	177	71.7
Cave	99	40.1
State	184	74.5
Municipality	182	73.7
Lithology	246	99.6
Photic zone	12	4.9
Biome	183	74.1
Presence/Absence of water	63	25.5

Graphs were generated using SigmaPlot version 10.0 software.

Results

The literature review yielded 247 records of anurans from Brazilian caves distributed across 18 scientific works (Appendix II). Between the first record in 1980 and the most recent one in 2022, a span of 42 years is represented. Between 1980 and 2008, only four studies recorded anurans in Brazilian Neotropical cavities (22.2% of the total), with a publication rate of one every 5 to 10 years. The number of studies surged to 14 between 2009 and 2022 (77.8% of the total), with 2020 being particularly prolific (Figure 1). The records provided taxonomic information on anurans, cave details, location, and study type (Table 1). These data represent individual specimen observations within cave environments, meaning that repeated species names do not equate to species richness as multiple records per species can occur.

Figure 1
Annual count of scientific publications on anurans found in Brazilian caves, spanning from 1980 to 2022.

Of the 247 records, 177 (71.7%) were identified to the species level (specific epithet). While 70 records (28.3%) were classified by morphotype, 233 (94.3%) by genus, and 240 (97.2%) by family.

The literature review identified 54 anuran species across 11 families within Brazilian caves (Table 2, Figure 2). Leptodactylidae was the most richness family with 13 species (23.6%), followed by Hylidae (12 species, 21.8%), and Bufonidae (10 species, 18.2%). In contrast, Aromobatidae, Odontophrynidae, and Pipidae were represented by a single species each (Figure 2).

Table 2
Anuran species found in Brazilian natural caves by state, lithology, and biome. Number records correspond to scientific publications mentioning each species. BA = Bahia, GO = Goiás, MT = Mato Grosso, MS = Mato Grosso do Sul, MG = Minas Gerais, PA = Pará, PR = Paraná, RN = Rio Grande do Norte, SC = Santa Catarina, SP = São Paulo, SE = Sergipe, TO = Tocantins; Aren = sandstone, Carb = carbonate, Cong = conglomerate, Ferr = ferruginous, Gran = granitic, Quar = quartzite, Marb = marble; Ama = Amazon Rainforest, Caa = Caatinga, Cerr = Cerrado, Atl = Atlantic Forest, Ecot = Ecotone.

Family Genus and species	State	Lithology	Biome	Records
Aromobatidae
Allobates marchesianus (Melin, 1941)	–	Ferr	Ama	1
Brachycephalidae
Ischnocnema guentheri (Steindachner, 1864)	MG	Ferr	–	1
Ischnocnema izecksohni (Caramaschi & Kisteumacher, 1989)	MG	Carb	–	1
Ischnocnema juipoca (Sazima & Cardoso, 1978)	MG	Carb - Ferr – Cong	Ecot (Cerr - Atl)	6
Ischnocnema manezinho (Garcia, 1996)	SC	Gran	Atl	7
Bufonidae
Rhaebo guttatus (Schneider, 1799)	PA	Aren – Ferr	Ama	3
Rhinella crucifer (Wied-Neuwied, 1821)	SP	Carb – Gran	Atl	3
Rhinella diptycha (Cope, 1862)	MG-SE	Aren – Carb	Cerr - Atl	6
Rhinella granulosa (Spix, 1824)	–	Carb	Caa	1
Rhinella icterica (Spix, 1824)	SP	Carb	Atl	2
Rhinella magnussoni Lima, Menin & Araújo, 2007	–	Ferr	Ama	1
Rhinella margaritifera (Laurenti, 1768)	MS	Carb	Cerr	1
Rhinella marina (Linnaeus, 1758)	PA	Ferr	Cerr	2
Rhinella ornata (Spix, 1824)	MG-SC	Gran - Ferr – Quar	Atl	7
Rhinella rubescens (Lutz, 1925)	MG	Ferr – Quar	Atl - Ecot (Cerr - Atl)	7
Craugastoridae
Haddadus binotatus (Spix, 1824)	MG	Ferr – Quar	–	2
Oreobates antrum Vaz-Silva, Maciel, Andrade & Amaro, 2018	GO-TO	Carb	Cerr	2
Oreobates heterodactylus (Miranda-Ribeiro, 1937)	MT	Carb	Cerr	2
Pristimantis fenestratus (Steindachner, 1864)	MT-PA	Cong – Ferr	Ama	5
Cycloramphidae
Cycloramphus eleutherodactylus (Miranda-Ribeiro, 1920)	SP-PR	Carb	Atl	6
Thoropa megatympanum Caramaschi & Sazima, 1984	MG	Ferr	–	2
Thoropa miliaris (Spix, 1824)	MG	Ferr - Gran – Quar	–	6
Thoropa taophora (Miranda-Ribeiro, 1923)	SP	Marm - Quar – Gran	Atl	3
Dendrobatidae
Adelphobates galactonotus (Steindachner, 1864)	PA	Ferr	Ama	2
Ameerega flavopicta (Lutz, 1925)	PA	Aren – Ferr	Ama	3
Hylidae
Boana albopunctata (Spix, 1824)	MG	Carb	Ecot (Cerr - Atl)	1
Boana boans (Linnaeus, 1758)	–	Ferr	Ama	1
Boana faber (Wied-Neuwied, 1821)	MG	Carb	Ecot (Cerr - Atl)	1
Bokermannohyla hylax (Heyer, 1985)	SP-SC	Carb – Gran	Atl	5
Bokermannohyla martinsi (Bokermann, 1964)	MG	Ferr	Cerr - Atl - Ecot (Cerr - Atl)	15
Dendropsophus nanus (Boulenger, 1889)	–	Aren	Cerr	1
Phyllomedusa burmeisteri Boulenger, 1882	–	Carb	Atl	1
Scinax catharinae (Boulenger, 1888)	SC	Gran	Atl	3
Scinax eurydice (Bokermann, 1968)	MG	Carb	–	1
Scinax fuscovarius (Lutz, 1925)	MG-MT	Aren - Carb - Cong – Ferr	Caa - Atl - Ecot (Cerr - Atl)	18
Scinax ruber (Laurenti, 1768)	MS	Carb	Cerr	1
Scinax x-signatus (Spix, 1824)	SE	Carb	Ecot (Caa - Atl)	6
Hylodidae
Hylodes cardosoi Lingnau, Canedo & Pombal, 2008	SP	Carb	Atl	1
Hylodes heyeri Haddad, Pombal & Bastos, 1996	SP	Carb	Atl	1
Leptodactylidae
Leptodactylus flavopictus Lutz, 1926	SP	Carb	Atl	1
Leptodactylus labyrinthicus (Spix, 1824)	MT-MG-RN	Carb - Cong - Ferr – Marm	Cerr - Caa	7
Leptodactylus latrans (Steffen, 1815)	MG	Carb	Ecot (Cerr - Atl)	1
Leptodactylus macrosternum Miranda-Ribeiro, 1926	–	Carb	Cerr - Caa	2
Leptodactylus mystacinus (Burmeister, 1861)	SP-MG	Carb – Ferr	Cerr - Atl	6
Leptodactylus paranaru Magalhães, Lyra, Carvalho, Baldo, Brusquetti, Burella, Colli, Gehara, Giaretta, Haddad, Langone, López, Napoli, Santana, de Sá, and Garda, 2020	SC	Gran	Atl	1
Leptodactylus pentadactylus (Laurenti, 1768)	PA	Ferr	Ama	2
Leptodactylus syphax Bokermann, 1969	–	Carb	Ama - Caa	2
Leptodactylus troglodytes Lutz, 1926	–	Carb	Caa	1
Leptodactylus vastus Lutz, 1930	SE	Carb	Atl - Ecot (Caa - Atl)	4
Physalaemus cuvieri Fitzinger, 1826	SE-BA-MG	Carb – Ferr	Caa - Cerr - Ecot (Caa - Atl)	7
Physalaemus ephippifer (Steindachner, 1864)	–	Ferr	Ama	1
Physalaemus nattereri (Steindachner, 1863)	MG	Ferr	–	1
Odontophrynidae
Proceratophrys boiei (Wied-Neuwied, 1824)	–	Gran	Atl	1
Pipidae
Pipa carvalhoi (Miranda-Ribeiro, 1937)	–	Ferr	Ama	1

Figure 2
Number of species per family of Brazilian Neotropical anurans recorded from caves between 1980 and 2022. Ar = Aromobatidae; Br = Brachycephalidae; Bu = Bufonidae; Cr = Craugastoridae; Cy = Cycloramphidae; De = Dendrobatidae; Hy = Hylidae; Ho = Hylodidae; Le = Leptodactylidae; Od = Odontophrynidae; Pi = Pipidae.

1.

Records by geographic variables

State and municipality information accompanied 184 (74.5%) and 182 (73.7%) of anuran records from Brazilian caves, respectively (Figure 2). Other records included broader geographic regions (e.g., Brazilian Northeast) or cave lithology (e.g., carbonate). Minas Gerais (81 records, 34.8%) and São Paulo State (35 records, 15.0%) housed the most anuran cave records (Figure 3).

Figure 3
Number of anuran records in caves by Brazilian state between 1980 and 2022. BA = Bahia; GO = Goiás; MG = Minas Gerais; MS = Mato Grosso do Sul; MT = Mato Grosso; PA = Pará; PR = Paraná; RN = Rio Grande do Norte; SC = Santa Catarina; SE = Sergipe; TO = Tocantins; ND = Not available.

In 99 records (40.1%) the natural cavity was identified. Compared to Brazil’s total recorded caves in 2022 (Brasil, 2022), this study represents 0.24% of those with documented anurans (Figure 4).

Figure 4
Registered caves in Brazil based on the Cadastro Nacional de Informações Espeleológicas CANIE/Cecav (Brasil, 2022) (green dots), and caves with recorded anurans compiled in this study (yellow triangles) between 1980 and 2022. Detailed locations of caves in Rio Grande do Norte (A), Sergipe (B); Minas Gerais (C), São Paulo (D), and Santa Catarina state (E) are displayed.

The Atlantic Forest, with 78 records (33.5%), was the predominant biome, followed by the Atlantic Forest/Cerrado ecotone (43 records, 18.5%) and Caatinga (16 records, 6.9%). Additionally, 19 records originated from the Amazon, 17 from Caatinga, and 24 from Cerrado (8.2%, 7.3%, and 10.3% respectively).

2.

Records by environmental variables

Water presence or absence was reported in 63 of 233 records (25.5%), categorized as intermittent (47, 20.2%), perennial (15, 6.4%), or absent (1, 0.4%). Photic zone information was available for only 12 records (4.9%), with nine in the entrance zone (3.9%), one in the dysphotic zone (0.4%), and one in the aphotic zone (0.4%).

3.

Records by geological variables

Lithological information was available for 246 records (99.6%; Figure 5), predominantly from carbonate (109 records, 46.8%) and ferruginous (76 records, 33.9%) caves. Conglomerate caves were less common, with only six records (2.4%).

Figure 5
Number of records by type of Brazilian cave lithology between 1980 and 2022. Aren = sandstone; Carb = carbonate; Cong = conglomerate; Ferr = ferruginous; Gran = granitic; Quar = quartzite; Marm = marble; ND = Not available.

4.

Records by type of scientific literature

Anuran amphibian records from Brazilian natural cavities were distributed across four publication formats: full articles (11 records, 61.1%), scientific notes (4 records, 22.2%), book chapters (2 records, 11.1%), and master’s theses (1 record, 5.6%). Most studies (14 records, 77.8%) focused on community ecology, often including other taxonomic groups like endemics or troglobites. Three records (16.6%) investigated specific populations. Taxonomy was addressed in only one record (5.6%).

Discussion

In the Brazilian region, 1114 species of anurans have been described (Segalla et al. 2021), of which the 54 species surveyed in this study represent 4.8%. This percentage is low when considering that anurans possess ecophysiological characteristics favoring the use of the underground environment (Eterovick et al. 2010, Matavelli et al. 2015).

The species distribution of anurans in this study aligns with the general distribution pattern of anuran families in Brazil. Hylidae is the most species rich family in the Brazilian region (373 species), a characteristic shared by all Neotropical subregions. This family predominantly comprises arboreal species exhibiting broad morphological, behavioral, and ecological niche plasticity (Duellman 1999, Cohen et al. 2020). Leptodactylidae is another diverse family with 181 species in Brazil (Segalla et al. 2021). These anurans are typically terrestrial or semi-aquatic, with sizes ranging from 20 to 150mm, demonstrating a wide ecological niche (Cohen et al. 2020). Bufonidae, with 100 species in Brazil, is characterized by water-resistant and robust individuals with thicker integuments (Cohen et al. 2020). Compared to Leptodactylidae (7.2%) and Hylidae (3.2%), the Bufonidade family has a higher proportion of cave-dwelling species reaching 10%. All three families exhibit diverse behaviors, size ranges, and inhabit various phytophysiognomies across the Neotropical region (Duellman 1999, Bernarde 2012, Cohen et al. 2020). Families with few representatives are smaller than those with more species. The Pipidae family, with four species in Brazil (Segalla et al. 2021), one of which has been recorded in caves (Matavelli et al. 2015) consists of aquatic amphibians with dorsoventrally flattened bodies. The Odontophrynidae family, endemic to South America, includes 48 species (Segalla et al. 2021). These terrestrial species frequently forage in leaf litter or underground, environments that can present conditions like caves, that is, with low light levels or complete darkness and high humidity (Bernarde 2012). The Aromobatidae family, with 31 species in the Amazon and Atlantic Forest (Segalla et al. 2021), is composed of individuals up to 35mm in size with diurnal habits (Bernarde 2012). For this family, caves may serve as refuges from sunlight or favorable areas for foraging.

A significant challenge in studying Brazilian cave anuran fauna is the Linnean shortfall, which, in this study, hinders taxonomic identification not only at the species level (morphotypes) but also at higher levels, such as genus and family. Many species exhibit similar physical characteristics, hindering accurate field identification. This issue is exacerbated when specimens cannot be collected and compared to reference collections for definitive taxonomic classification, impeding advancements in anuran taxonomy (Bernarde 2012, Haddad et al. 2013).

São Paulo and Minas Gerais, states with the highest cave densities in Brazil, have long histories of tourism and research in these subterranean environments. Examples include the Alto Ribeira State Tourist Park (established in 1958) in São Paulo and the Ibitipoca State Park (established in 1973) in Minas Gerais. Additionally, the Cavernas do Peruaçu National Park (1999), the State Natural Monuments Peter Lund (2005), and Gruta do Rei do Mato (2009), all in Minas Gerais, are significant. The Peter Lund site is particularly notable for its historical connection to the 19th-century explorer who studied local carbonate caves (Holten & Sterll 2017). Given their relatively undisturbed conditions, permanent preservation areas in Brazil are more frequently studied. The establishment of conservation units within these areas has contributed significantly to the documentation of anuran species in Brazilian caves. All these factors can explain the predominance of anuran records found in caves of São Paulo and Minas Gerais states. However, given the low number of caves sampled compared to the total in Brazil, this study suggests a gap in our knowledge regarding the use of cavities as habitat by anurans.

The predominance of anurans in Atlantic Forest caves observed in this study aligns with this biome’s overall amphibian diversity. As Brazil’s most biodiverse biome for amphibians housing 543 species (88% endemic) (Haddad et al. 2013), the Atlantic Forest’s combination of closed forests, abundant water bodies, and high precipitation and humidity creates optimal conditions for anurans (Haddad et al. 2013, Bichuette et al. 2022).

However, the predominance of records in São Paulo and Minas Gerais, as well as the overrepresentation of Atlantic Forest anurans, might be linked to geologic aspects. The two most common lithologies in our dataset are associated with the geology of specific regions. In Brazil, ferruginous caves are primarily found in the iron quadrangle of Minas Gerais, regions with Cerrado vegetation, in ecotones between Cerrado/Atlantic Forest, and the Carajás iron region in Pará (predominance of Amazon Forest). Conversely, carbonate formations, such as the Bambuí group, extend across various biomes (Caatinga, Cerrado, Atlantic Forest) and states (Minas Gerais, Goiás, Tocantins, Bahia; Rubbioli et al. 2019, Dos Santos 2022b). The higher frequency of records (109) in carbonate caves aligns with the well-known correlation between this lithology and extensive cave systems (Rubbioli et al. 2019).

Results indicate that water presence information is more redly available in most records compared to light information. Water presence significantly influences reproduction, feeding (especially in tadpoles), and water loss rate in anurans. Thus, it is crucial for understanding their life history and for their biospeleological classification (Eterovick et al. 2010, Matavelli et al. 2015, dos Santos et al. 2022). The luminosity zones (photic, dysphotic, aphotic) provide valuable information for understanding anuran use of cave space. For instance, occupation of the cave entrance area by anurans likely facilitates escape, nocturnal foraging, and access to a rich food supply due to the ecotone environment. Additionally, it offers shelter from predators and desiccation (Eterovick et al. 2010, Simões et al. 2015). In contrast, the presence of anurans in deeper, low-light (dysphotic) or no-light (aphotic) zones might indicate refuge from visual predators (Bernarde 2012) or feeding opportunities (dysphotic zone, personal observation Francisco L. Tejerina-Garro). However, the current limited data evidenced by this study highlights a significant knowledge gap in anuran cave ecology.

Since the first publication documenting anuran presence in cavities by Dessen et al. (1980), 42 years have passed (until 2022). Between 1980 and 2008, research on cave-dwelling anurans was scarce, with only four studies published (one every 5-10 years). This changed significantly after the implementation of Normative 6640 in 2008, which mandated environmental impact assessments for caves (Brasil 2008). Consequently, from 2009 to 2022 the number of studies increased (14 records), including pioneering works on populations. For instance, Martins de Andrade et al. (2021) investigated the occupancy of ferruginous cavities by Bokermannohyla martinsi in Minas Gerais, Lima et al. (2012) studied the vocalization activity of Cycloramphus eleutherodactylus in São Paulo’s carbonate caves, and Motta et al. (2020) examined the distribution and seasonal activity of Oreobates antrum in southeastern Tocantins’ carbonate caves. Additionally, taxonomic studies emerged, such as the description of a Bolivian species related to O. antrum by Pansonato et al. (2020). Furthermore, Vaz-Silva et al. (2020) confirmed the occurrence of O. antrum in the Brazilian Cerrado. The last three years mark the first period with multiple publications annually (full articles, scientific notes book chapters, master’s theses) reflecting a growing recognition of the importance of documenting and scientifically communicating anuran occupation of Brazilian Neotropical caves.

Final Considerations

This paper reveals a significant increase in anuran cave studies since 2008, when legislation classifying Brazilian caves by speleological rank and requiring environmental impact assessments was implemented. This led to increased academic training in biospeleology and subsequent growth in scientific data and publications. Records concentrated on carbonate and ferruginous lithologies, prevalent in commercially valuable caves of Minas Gerais and São Paulo, within the Atlantic Forest and Cerrado biomes. Cave amphibian families mirrored surface diversity. To enhance knowledge, future studies should explore underrepresented regions, expanding species occurrence records and refining data collection protocols. Biospeleologists can contribute by collecting specimens for reference collections and high-quality photographs to address taxonomic challenges and reduce knowledge gaps.

Supplementary Material

The following online material is available for this article:

Appendix I - Scientific literature compiled and used in this study related to anurans in Brazilian natural cavities between 1980 and 2022.

Appendix II - Data extracted from the literature compiled.

Acknowledgments

We thank the Postgraduate Program in Ecology and Natural Resources at the Federal University of São Carlos. This work was partially funded by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) – Code 001. We also thank the anonymous reviewers for their valuable suggestions.

Data Availability

Supporting data are available at <https://doi.org/10.48331/scielodata.LVRZ6R>.

References

• ARAUJO, C.D.O., CONDEZ, T.H., BOVO, R.P., CENTENO, F.D.C. & LUIZ, A.M. 2010. Amphibians and reptiles of the Parque Estadual Turístico do Alto Ribeira (PETAR), SP: An Atlantic Forest remnant of southeastern Brazil. Biota Neotropica 10(4):257–274. https://doi.org/10.1590/S1676-06032010000400031.
  » https://doi.org/10.1590/S1676-06032010000400031
• ARCHAMBAULT, É., CAMPBELL, D., GINGRAS, Y. & LARIVIÈRE, V. 2009. Comparing bibliometric statistics obtained from the Web of Science and Scopus. Journal of the American Society for Information Science and Technology 60(7):1320–1326. https://doi.org/10.1002/asi.21062.
  » https://doi.org/10.1002/asi.21062
• BARR, T.C. 1968. Cave ecology and the evolution of troglobites. In T. Dobzhansky, M. K. Hecht, & W. C. Steere, (Orgs.) Evolutionary Biology (pp. 35–102). Springer US. https://doi.org/10.1007/978-1-4684-8094-8_2.
  » https://doi.org/10.1007/978-1-4684-8094-8_2
• BERNARDE, P. S. 2012. Anfíbios e répteis: Introdução ao estudo da herpetofauna brasileira (1st ed). Anolis Books.
• BICHUETTE, M.E., SPERANDEI, V. DE F., BERTOLINI, D.L.V.B.V., SIMÃO, P.X.A. & SABBAG, A.F. 2022. Frogs of seven granitic caves on Santa Catarina Island, Florianópolis Municipality, Santa Catarina State, southern Brazil. Herpetology Notes 15:353–359.
• BOULTON, A.J., FENWICK, G.D., HANCOCK, P.J. & HARVEY, M.S. 2008. Biodiversity, functional roles and ecosystem services of groundwater invertebrates. Invertebrate Systematics 22(2):103–116. https://doi.org/10.1071/IS07024.
  » https://doi.org/10.1071/IS07024
• BRASIL. 2008. Decreto N° 6.640, de 7 de Novembro de 2008. http://www.planalto.gov.br/ccivil_03/_Ato2007-2010/2008/Decreto/D6640.htmRetrieved February 22, 2022.
  » http://www.planalto.gov.br/ccivil_03/_Ato2007-2010/2008/Decreto/D6640.htm
• BRASIL. 2022. Instituto Chico Mendes de Conservação da Biodiversidade. Cadastro Nacional de Informações Espeleológicas (ICMBio/CANIE/Cecav). https://www.gov.br/icmbio/pt-br/assuntos/centros-de-pesquisa/cavernas/cadastro-nacional-de-informacoes-espeleologicas/canie Retrieved February 22, 2022.
  » https://www.gov.br/icmbio/pt-br/assuntos/centros-de-pesquisa/cavernas/cadastro-nacional-de-informacoes-espeleologicas/canie
• BRASIL. 2023. Instituto Chico Mendes de Conservação da Biodiversidade - Statistical yearbook of Brazilian speleological heritage 2023. https://www.gov.br/icmbio/pt-br/assuntos/centros-de-pesquisa/cecav/anuario-estatistico-do-patrimonio-espeleologico-brasileiro/cecav-anuario-estatistico-speleologico-2022.pdf Retrieved January 25, 2024.
  » https://www.gov.br/icmbio/pt-br/assuntos/centros-de-pesquisa/cecav/anuario-estatistico-do-patrimonio-espeleologico-brasileiro/cecav-anuario-estatistico-speleologico-2022.pdf
• COHEN, G.J., PAREDERO, R.C.B., KANASIRO, A. & SUGIHARA, V.S. 2020. Herpetofauna da cuesta paulista Anolis Books.
• COSTA, J.C.R., MARCHI, G.H., SANTOS, C.S., ANDRADE, M.C.M., CHAVES JUNIOR, S.P., SILVA, M.A.N., MELO, M.N. & ANDRADE, A.J. 2021. First molecular evidence of frogs as a food source for sand flies (Diptera: Phlebotominae) in Brazilian caves. Parasitology Research 120(5):1571–1582. https://doi.org/10.1007/s00436-021-07154-3.
  » https://doi.org/10.1007/s00436-021-07154-3
• COUTO, H., MADEIRA, M.M., HERNÁNDEZ ORDÓÑEZ, O., REYNOSO, V.H. & ROSA, G.M. 2023. Cave-dwelling populations of the monstrous rainfrog (Craugastor pelorus) from Mexico. Diversity 15(2):189. https://doi.org/10.3390/d15020189.
  » https://doi.org/10.3390/d15020189
• CULVER, D.C. 1982. Cave life HUP.
• CULVER, D.C. & PIPAN, T. 2009. The biology of caves and other subterranean habitats Oxford University Press.
• DE ARAÚJO, J.P.M., BASÍLIO, G.H.N., KRAMER, M.A. DE F., MOURA, T.H.S., NETO, M.R. & DA SILVA, M. 2017. Fauna cavernícola e os impactos ambientais ao patrimônio espeleológico do município de Martins, Rio Grande do Norte, Brasil. Speleo-Tema 28(2):107–123.
• DELGADO-JARAMILLO, M., BARBIER, E. & BERNARD, E. 2018. New records, potential distribution, and conservation of the Near Threatened cave bat Natalus macrourus in Brazil. Oryx 52(3):579–586. https://doi.org/10.1017/S0030605316001186.
  » https://doi.org/10.1017/S0030605316001186
• DESSEN, E.M.B., ESTON, V.R., SILVA, M.S., TEMPERINI-BECK, M.T. & TRAJANO, E. 1980. Levantamento preliminar da fauna de cavernas de algumas regiões do Brasil. Ciência e Cultura 32(6):714–725.
• DIÍAZ, A.R. 2009. Cave biology: Life in darkness Cambridge University Press.
• DONATO, C.R. 2011. Caracterização dos impactos ambientais de cavernas do município de Laranjeiras, Sergipe. [Master’s Thesis, Universidade Federal de Sergipe]. https://ri.ufs.br/handle/123456789/534
  » https://ri.ufs.br/handle/123456789/534
• DOS SANTOS, T., SOUZA, A.M. DE, BONDEZAN, F.L. & ETEROVICK, P.C. 2022a. Going underground: What the natural history traits of cave users can tell us about cave use propensity. Journal of Herpetology 56(2):153–163. https://doi.org/10.1670/20-055.
  » https://doi.org/10.1670/20-055
• DOS SANTOS, T., FERREIRA, R.L., DE SOUZA, A.M., ANDRADE, M.C.M., COSTA, J.C.R. & ETEROVICK, P.C. 2022b. Amphibians and reptiles in caves. In R. A. Zampaulo, (Ed.) Fauna cavernícola do Brasil (v.01, pp. 492-508). Rupestre.
• DUELLMAN, W. E. 1999. Distribution patterns of amphibians in South America. In W. E. Duellmann, (Ed.) Patterns of distribution of amphibians: a global perspective (v 01, pp 255–327). Johns Hopkins University Press.
• ETEROVICK, P.C., RIEVERS, C.R., KOPP, K., WACHLEVSKI, M., FRANCO, B.P., DIAS, C.J., BARATA, I.M., FERREIRA, A.D.M. & AFONSO, L.G. 2010. Lack of phylogenetic signal in the variation in anuran microhabitat use in southeastern Brazil. Evolutionary Ecology 24(1):1–24. https://doi.org/10.1007/s10682-008-9286-9.
  » https://doi.org/10.1007/s10682-008-9286-9
• FALAGAS, M.E., PITSOUNI, E.I., MALIETZIS, G.A. & PAPPAS, G. 2008. Comparison of Pubmed, Scopus, Web of Science, and Google Scholar: Strengths and weaknesses. The FASEB Journal 22(2):338–342. https://doi.org/10.1096/fj.07-9492LSF.
  » https://doi.org/10.1096/fj.07-9492LSF
• FREITAS, M.A. 2015. Herpetofauna no Nordeste brasileiro: Guia de campo (1st ed). Technical Books Editora.
• FERREIRA, R.L., SOUZA-SILVA, M. & ZAMPAULO, R.A. 2022. A vida subterrânea no Carste de Pains: biodiversidade, ameaças e conservação de fauna em uma notável paisagem cárstica tropical. In L. B. Piló & J.B. Cruz, (Orgs.) A região cárstica de Pains (v01, pp 151–177). Instituto Chico Mendes – ICMBio.
• FROST, D.R. 2023. Amphibian Species of the World: an Online Reference. Version 6.2 https://amphibiansoftheworld.amnh.org/index.php Retrieved September 10, 2023.
  » https://amphibiansoftheworld.amnh.org/index.php
• GALLÃO, J.E. & BICHUETTE, M.E. 2018. Brazilian obligatory subterranean fauna and threats to the hypogean environment. ZooKeys 746:1–23. https://doi.org/10.3897/zookeys.746.15140.
  » https://doi.org/10.3897/zookeys.746.15140
• GIBERT, J., DANIELOPOL, D. & STANFORD, J.A. (Orgs.). 1994. Groundwater ecology Academic Press.
• GIBERT, J. & DEHARVENG, L. 2002. Subterranean ecosystems: A truncated functional biodiversity. BioScience 52(6):473–481. https://doi.org/10.1641/0006-3568(2002)052%5B0473:SEATFB%5D2.0.CO;2.
  » https://doi.org/10.1641/0006-3568(2002)052[0473:SEATFB]2.0.CO;2
• GOUVEIA, S.F., ROCHA, P.A., MIKALAUSKAS, J.S. & SILVEIRA, V.V. 2009. Rhinella jimi (Cururu toad) and Leptodactylus vastus (Northeastern pepper frog). Predation on bats. Herpetological Review 40(2):210.
• GUERRA, V., LLUSIA, D., GAMBALE, P.G., MORAIS, A.R.D., MÁRQUEZ, R. & BASTOS, R.P. 2018. The advertisement calls of Brazilian anurans: Historical review, current knowledge and future directions. PLOS ONE 13(1):e0191691. https://doi.org/10.1371/journal.pone.0191691.
  » https://doi.org/10.1371/journal.pone.0191691
• HADDAD, C.F.B., TOLEDO, L.F. & PRADO, C.P.A. 2013. Anfíbios da Mata Atlântica: Guia dos anfíbios anuros da Mata Atlântica. Guide for the Atlantic Forest anurans Editora Neotropica.
• HADDAD, N.M., BRUDVIG, L.A., CLOBERT, J., DAVIES, K.F., GONZALEZ, A., HOLT, R.D., LOVEJOY, T.E., SEXTON, J.O., AUSTIN, M.P., COLLINS, C.D., COOK, W.M., DAMSCHEN, E.I., EWERS, R.M., FOSTER, B.L., JENKINS, C.N., KING, A.J., LAURANCE, W.F., LEVEY, D.J., MARGULES, C.R., … TOWNSHEND, J.R. 2015. Habitat fragmentation and its lasting impact on Earth’s ecosystems. Science Advances 1(2):e1500052. https://doi.org/10.1126/sciadv.1500052.
  » https://doi.org/10.1126/sciadv.1500052
• HOLTEN, B. & STERLL, M. 2017. Peter Wilhelm Lund: life and work. In P. Da-Gloria, W. A. Neves & M. Hubbe, (Orgs.) Archaeological and Paleontological Research in Lagoa Santa (p. 11–26). Springer International Publishing. https://doi.org/10.1007/978-3-319-57466-0_2.
  » https://doi.org/10.1007/978-3-319-57466-0_2
• HORTAL, J., DE BELLO, F., DINIZ-FILHO, J.A.F., LEWINSOHN, T.M., LOBO, J.M. & LADLE, R.J. 2015. Seven shortfalls that beset large-scale knowledge of biodiversity. Annual Review of Ecology, Evolution, and Systematics 46(1):523–549. https://doi.org/10.1146/annurev-ecolsys-112414-054400.
  » https://doi.org/10.1146/annurev-ecolsys-112414-054400
• JUAN, C., GUZIK, M.T., JAUME, D. & COOPER, S.J.B. 2010. Evolution in caves: Darwin’s ‘wrecks of ancient life’ in the molecular era. Molecular Ecology 19(18):3865–3880. https://doi.org/10.1111/j.1365-294X.2010.04759.x.
  » https://doi.org/10.1111/j.1365-294X.2010.04759.x
• LIMA, A.M.X., ARAUJO, C.O. & VERDADE, V.K. 2012. Cycloramphus eleutherodactylus (Alto Button Frog): calling among rocks and caves. Herpetological Bulletin 120:39–42.
• LUNGHI, E., BRUNI, G., FICETOLA, F.G. & MANENTI, R. 2018. Is the Italian stream frog (Rana italica Dubois, 1987) an opportunistic exploiter of cave twilight zone? Subterranean Biology 25:49–60. https://doi.org/10.3897/subtbiol.25.23803.
  » https://doi.org/10.3897/subtbiol.25.23803
• MARTÍN-MARTÍN, A., THELWALL, M., ORDUNA-MALEA, E. & DELGADO LÓPEZ-CÓZAR, E. 2021. Google Scholar, Microsoft Academic, Scopus, Dimensions, Web of Science, and OpenCitations’ COCI: a multidisciplinary comparison of coverage via citations. Scientometrics 126(1):871–906. https://doi.org/10.1007/s11192-020-03690-4.
  » https://doi.org/10.1007/s11192-020-03690-4
• MARTINS DE ANDRADE, M.C., COSTA, J.C.R. & ETEROVICK, P.C. 2021. Fidelity in the use of iron caves by Bokermannohyla martinsi (Anura: Hylidae): a step further in unveiling the importance of Brazilian caves for the herpetofauna. Salamander 57(4):502–512.
• MATAVELLI, R., CAMPOS, A.M., FEIO, R.N. & FERREIRA, R.L. 2015. Occurrence of anurans in brazilian caves. Acta Carsologica 44(1):107–120. https://doi.org/10.3986/ac.v44i1.649.
  » https://doi.org/10.3986/ac.v44i1.649
• MEDELLIN, R.A., WIEDERHOLT, R. & LOPEZ-HOFFMAN, L. 2017. Conservation relevance of bat caves for biodiversity and ecosystem services. Biological Conservation 211:45–50. https://doi.org/10.1016/j.biocon.2017.01.012.
  » https://doi.org/10.1016/j.biocon.2017.01.012
• MONGEON, P. & PAUL-HUS, A. 2016. The journal coverage of Web of Science and Scopus: A comparative analysis. Scientometrics 106(1):213–228. https://doi.org/10.1007/s11192-015-1765-5.
  » https://doi.org/10.1007/s11192-015-1765-5
• MOTTA, A., LYRA, M., GAZONI, T., PARISE-MALTEMPI, P.P. & HADDAD, C. F. 2020. New distribution records of Oreobates antrum Vaz-Silva, Maciel, Andrade and Amaro, 2018, a cave-associated species from the seasonally dry Tropical Forest in the Brazilian Cerrado (Anura: Brachycephaloidea: Craugastoridae). Herpetology Notes 13:561–563.
• PANSONATO, A., MOTTA, A., CACCIALI, P., HADDAD, C.F.B., STRÜSSMANN, C. & JANSEN, M. 2020. On the identity of species of Oreobates (Anura: Craugastoridae) from Central South America, with the description of a new species from Bolivia. Journal of Herpetology 54(4):393–412. https://doi.org/10.1670/20-001.
  » https://doi.org/10.1670/20-001
• PARIZOTTO, D.R., PIRES, A.C., MISE, K.M. & FERREIRA, R.L. 2017. Troglobitic invertebrates: Improving the knowledge on the Brazilian subterranean biodiversity through an interactive multi-entry key. Zootaxa 4365(4):401–409. https://doi.org/10.11646/zootaxa.4365.4.1.
  » https://doi.org/10.11646/zootaxa.4365.4.1
• PELLEGRINI, T., SALES, L.P., AGUIAR, P. & FERREIRA, R.L. 2016. Linking spatial scale dependence of land-use descriptors and invertebrate cave community composition. Subterranean Biology 18:17–38. https://doi.org/10.3897/subtbiol.18.8335.
  » https://doi.org/10.3897/subtbiol.18.8335
• PINTO-DA-ROCHA, R. & SESSEGOLO, G.C. 2001. Estudo da fauna de Gruta de São Miguel I, Serra da Bodoquena (MS), como subsídio para o plano de manejo. In L. F. S. Rocha, K. L. de Oliveira & G. C. Sessegolo, (Orgs.) Conservando Cavernas. Cinquenta anos de espeleologia GEEP-Açungi, 125–135. Grupo de Estudos Espeleológicos do Paraná.
• POULSON, T.L. & WHITE, W.B. 1969. The Cave Environment: Limestone caves provide unique natural laboratories for studying biological and geological processes. Science 165(3897):971–981. https://doi.org/10.1126/science.165.3897.971.
  » https://doi.org/10.1126/science.165.3897.971
• REIS, E.A. & REIS, I.A. 2002. Análise Descritiva de Dados Relatório Técnico. Departamento de Estatísticas, Instituto de Ciências Exatas, Universidade Federal de Minas Gerais.
• REPISO-CABALLERO, R. & DELGADO-LÓPEZ-CÓZAR, E. 2013. The impact of scientific journals of communication: Comparing Google Scholar metrics, Web of Science and Scopus. Comunicar 21(41):45–52. https://doi.org/10.3916/C41-2013-04.
  » https://doi.org/10.3916/C41-2013-04
• RUBBIOLI, E., AULER, A., MENIN, D. & BRANDI, R. 2019. Cavernas. Atlas do Brasil Subterrâneo ICMBio /CECAV.
• SEGALLA, M., BERNECK, B., CANEDO, C., CARAMASCHI, U., CRUZ, C.A.G., GARCIA, P.C.A., GRANT, T., HADDAD, C.F.B., LOURENÇO, A.C., MANGIA, S., MOTT, T., NASCIMENTO, L., TOLEDO, L.F., WERNECK, F. & LANGONE, J.A. 2021. List of brazilian amphibians. Herpetologia brasileira 10(1):121–216. https://doi.org/10.5281/ZENODO.4716176.
  » https://doi.org/10.5281/ZENODO.4716176
• SILVA, J.A.D. & BIANCHI, M.D.L. P. 2001. Cientometria: A métrica da ciência. Paidéia (Ribeirão Preto) 11(21):5–10. https://doi.org/10.1590/S0103-863X2001000200002.
  » https://doi.org/10.1590/S0103-863X2001000200002
• SILVA, M.S., MARTINS, R.P. & FERREIRA, R.L. 2011. Cave lithology determining the structure of the invertebrate communities in the Brazilian Atlantic Rain Forest. Biodiversity and Conservation 20(8):1713–1729. https://doi.org/10.1007/s10531-011-0057-5.
  » https://doi.org/10.1007/s10531-011-0057-5
• SILVESTRE, A. 2007. Análise de dados e estatística descritiva. Escolar Editora.
• SIMÕES, M.H., SOUZA-SILVA, M. & LOPES FERREIRA, R. 2015. Cave physical attributes influencing the structure of terrestrial invertebrate communities in Neotropics. Subterranean Biology 16:103–121. https://doi.org/10.3897/subtbiol.16.5470.
  » https://doi.org/10.3897/subtbiol.16.5470
• SIMON K.S., PIPAN T. & CULVER D.C. 2007. A conceptual model of the flow and distribution of organic carbon in caves. Journal of Cave and Karst Studies 69(2):279–284.
• SKET, B. 2008. Can we agree on an ecological classification of subterranean animals? Journal of Natural History 42(21–22):1549–1563. https://doi.org/10.1080/00222930801995762.
  » https://doi.org/10.1080/00222930801995762
• SOUZA SILVA, M., MARTINS, R.P. & FERREIRA, R.L. 2015. Cave conservation priority index to adopt a rapid protection strategy: A case study in Brazilian Atlantic rain forest. Environmental Management 55(2):279–295. https://doi.org/10.1007/s00267-014-0414-8.
  » https://doi.org/10.1007/s00267-014-0414-8
• STANLEY, L., MURRAY, C.M., MURRAY, J.J. & CROTHER, B.I. 2021. Areas of endemism of Jamaica: Inferences from parsimony analysis of endemism based on amphibian and reptile distributions. Biogeographia – The Journal of Integrative Biogeography 36: a006. https://doi.org/10.21426/B636052803.
  » https://doi.org/10.21426/B636052803
• TOBIN, B., HUTCHINS, B. & SCHWARTZ, B. 2013. Spatial and temporal changes in invertebrate assemblage structure from the entrance to deep-cave zone of a temperate marble cave. International Journal of Speleology 42(3):203–214. https://doi.org/10.5038/1827-806X.42.3.4.
  » https://doi.org/10.5038/1827-806X.42.3.4
• TRAJANO, E. 1986. Fauna cavernícola brasileira: composição e caracterização preliminar. Revista Brasileira de Zoologia 3(8):533–561.
• TRAJANO, E. & GNASPINI, P.N. 1991. Composição da fauna cavernícola brasileira, com uma análise preliminar da distribuição dos táxons. Revista Brasileira de Zoologia 7(3):383–407.
• TREVELIN, L.C., SIMÕES, M.H., PROUS, X., PIETROBON, T., BRANDI, I.V. & JAFFÉ, R. 2021. Optimizing speleological monitoring efforts: insights from long-term data for tropical iron caves. PeerJ 9:e11271. https://doi.org/10.7717/peerj.11271.
  » https://doi.org/10.7717/peerj.11271
• VAZ-SILVA, W., MACIEL, N.M., NOMURA, F., MORAIS, A.R.D., BATISTA, V.G., SANTOS, D.L., ANDRADE, S.P., OLIVEIRA, A.Â.B.D., BRANDÃO, R.A. & BASTOS, R.P. 2020. Guia de identificação das espécies de anfíbios (Anura e Gymnophiona) do estado de Goiás e do Distrito Federal, Brasil Central Sociedade Brasileira de Zoologia. https://doi.org/10.7476/9786587590011.
  » https://doi.org/10.7476/9786587590011

Edited by

Associate Editor

Denise de Cerqueira Rossa-Feres

Publication Dates

• Publication in this collection
  14 Oct 2024
• Date of issue
  2024

History

• Received
  18 June 2024
• Accepted
  02 Sept 2024