Corresponding author: Marconi Souza Silva (
Academic editor: Oana Moldovan
Twenty caves located in a high altitudinal quartzite area in Brazil were examined for invertebrate richness and composition and in terms of environmental factors that determine community structure. We evaluate how distance, altitude, cave extension, environmental stability, number and size of cave entrances and stream presence can act on species composition and richness. The caves presented a high richness of troglophilic (463 spp.) and troglobitic species (6 spp.) in relation to other siliciclastic caves around the world. The average richness was 39.55 species per cave (sd = 21.87), the quantitative similarity among caves was 41% and turnover was βrepl. = 0.769.
Souza Silva M, Iniesta LFM, Ferreira RL (2020) Invertebrates diversity in mountain Neotropical quartzite caves: which factors can influence the composition, richness, and distribution of the cave communities? Subterranean Biology 33: 23–43.
Studies related to ecology and conservation of subterranean fauna have been receiving increasing attention in recent years (
In Brazil, the cave fauna started to be systematically studied in the 1980s (
In Brazil, there are at least 2,300 known sandstone and quartzite caves, but they represent only 1% of the potential occurrence (
Previous ecological studies conducted in 14 Brazilian quartzite caves in the South of Minas Gerais state found 400 species (44.85 species/cave, sd = 24.54), for an average cave extension of 231 m (sd = 219) (
However, a study performed on 33 temperate sandstone caves of the Cape Peninsula in South Africa (approximately 20–90 m long), found only 85 species (
However, the previous studies did not present information on how composition, richness, and distribution cave communities are related to some cave attributes (distance between caves, cave size, number and size of entrances and altitudinal position among others). Such features were proven to be determinant for local and regional species richness and dissimilarity, mainly in the tropics (
The study was conducted in the Ibitipoca mountain quartzite province, south of Minas Gerais state, Brazil. The caves in this region were formed and modeled by hierarchically organized drainages influenced by differences between the local water table and the regional base level. The Ibitipoca Mountain belongs to the Andrelândia geological group mainly composed of quartzite rocks of Mesoproterozoic lithostratigraphic age (
The mountain is located within a protected area, with 1,488 ha of extension and altitude ranging from 1,200 to 1,784 m asl. This reserve was created in 1973 and protects epigean fauna and flora and quartzite caves and their fauna (
Borders of the Ibitipoca Estadual Park (
Most of the caves in this study were mapped by
The altitude above sea level and geographic position of the caves were obtained with a Global Positioning System (
Biotic and abiotic characteristics of the 20 quartzite caves in southeastern Brazil. Cave with stream (S) or dry caves (D), total richness (TS); relative richness (RS), abundance (A), altitude (ALT in meters), geographic coordinates (Lat and Long in decimal degrees), Sampled extension of the caves (
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Catedral III | S | 22 | 0.13 | 145 | 1634 |
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170 | 0 | 5 | 60 | 9.28 |
Bichana II | D | 19 | 0.63 | 580 | 1350 |
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30 | 0 | 1 | 4 | 2.01 |
Bichana I | D | 31 | 1.55 | 132 | 1360 |
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20 | 0 | 1 | 1 | 1.61 |
Catedral I | S | 14 | 0.54 | 89 | 1646 |
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26 | 0 | 5 | 1 | 1.65 |
Manequinho | S | 61 | 0.1 | 940 | 1270 |
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160 | 0 | 4 | 40 | 8.76 |
*Cruz | D | 61 | 1.45 | 344 | 1632 |
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50 | 0 | 3 | 20 | 10.93 |
Dobras1 | D | 26 | 0.19 | 220 | 1600 |
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138 | 1 | 2 | 15 | 8.32 |
*Ponte de Pedra | S | 30 | 0.44 | 103 | 1283 |
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54 | 0 | 2 | 20 | 7.68 |
*Gnomos | S | 23 | 0.38 | 137 | 1363 |
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32 | 0 | 2 | 15 | 6.46 |
Lagarto Teiú | S | 40 | 0.4 | 266 | 1349 |
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40 | 0 | 1 | 10 | 1.40 |
*Monjolinhos | D | 22 | 1.05 | 39 | 1428 |
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21 | 0 | 1 | 5 | 1.44 |
Martiniano | D | 35 | 0.16 | 270 | 1360 |
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240 | 0 | 4 | 40 | 2.3 |
Martiniano II | D | 18 | 0.36 | 96 | 1340 |
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50 | 0 | 4 | 50 | 2.53 |
*Viajantes | D | 33 | 0.2 | 333 | 1660 |
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166 | 0 | 2 | 50 | 9.5 |
Fugitivos | D | 33 | 0.08 | 842 | 1669 |
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440 | 0 | 4 | 80 | 7.45 |
*Pião1 | D | 34 | 0.27 | 270 | 1643 |
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126 | 1 | 1 | 4 | 3.45 |
*Coelhos | D | 67 | 0.84 | 488 | 1358 |
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80 | 0 | 2 | 10 | 9.46 |
Bromélias2 | D | 96 | 0.19 | 2869 | 1450 |
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500 | 1 | 3 | 10 | 5.11 |
Moreiras3,4 | D | 75 | 0.13 | 3735 | 1651 |
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600 | 2 | 6 | 80 | 9.33 |
Casas1, 4,5,6 | S | 47 | 0.07 | 249 | 1340 |
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650 | 4 | 1 | 7 | 4.53 |
Species richness and composition of the invertebrate communities were assessed in 20 caves (Table
The determination of potentially obligate cave species was conducted by identifying the specimens with troglomorphic traits (
Human modifications were determined in relation to uses and impacts. Tourist and religious activities were considered uses while real impacts were trampling, illumination and construction resulting from these activities (
The components of beta diversity were calculated using the BAT package developed by
The average taxonomic distinctness (∆+) analysis was conducted with the software Primer 7 using 297 from the 463 morphotypes because they were identified up to family level (
The Environmental stability of each cave was determined using the Environmental Stability Index (
A non-parametric multivariate analysis (DistLM – Distance-based Linear Model) was used to evaluate the influences of the distance between caves (dist), the extension of the sampled cave (
The distance-based redundancy analysis (
Similarity analysis (
Caves are located at altitudes between 1270 and 1669 m asl (sd = 150 m). Sampled cave extension varied from 20 to 650 m in length (sd = 202 m), presenting one to six entrances. Surface of entrances varied from 1 to 80 m2 (sd = 26 m). Environmental stability varied from 1.4 to 10.93 (Table
We found a total of 12,123 individuals distributed in 463 morphotypes and at least 117 families. The composition considering higher taxa is presented in Figure
Invertebrate taxa, richness and distribution in the 20 studied caves of the Ibitipoca quartzite speleological province, Brazil. Gruta Catedral III (1), Gruta Beira de Estrada II (2), Gruta Beira de Estrada I (3), Gruta Catedral I (4), Gruta Manequinho (5), Gruta da Cruz (6), Gruta das Dobras (7), Ponte de Pedra (8), Gruta dos Gnomos (9), Gruta do Lagarto Teiú (10), Gruta do Monjolinhos (11), Gruta do Martiniano (12), Gruta do Martiniano II (13), Gruta dos Viajantes (14), Gruta dos Fugitivos (15), Gruta do Pião (16), Gruta Coelhos (17), Gruta das Bromélias (18), Gruta dos Moreiras (19), Gruta das Casas (20). Total Richness (TS).
Order | Family | TS | 1 | 2 | 3 | 4 | 5 | 6 | 7 | 8 | 9 | 10 | 11 | 12 | 13 | 14 | 15 | 16 | 17 | 18 | 19 | 20 |
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The richest higher taxa in the sampled caves were the orders
Higher taxa invertebrate abundance, taxonomic diversity (richness) (
The average richness of the caves was 39.55 spp. (sd= 21.87). The Bromélias (95 spp.) and Moreiras (75 spp.) caves presented the highest invertebrate richness, contrasting with Martiniano II (18 spp.) and Catedral I (14 spp.) caves, which presented the lowest richness values (Table
Six invertebrate species, distributed in five caves, presented troglomorphic traits.Casas cave had four troglobitic species ((
Obligate cave species found in the Ibitipoca Estadual Park, Brazil.
The quantitative similarity among cave communities was low (< 41%) and the βtotal was 0.952, βrepl = 0.769 and βrich = 0.178.
Average taxonomic distinctness Δ+ varied between 58 to 70, and 18 caves were placed within the 95% confidence interval of the average taxonomic distinctness (∆+) (Figure
Average taxonomic distinctness with respective lambda and significance values (% sig) of the 20 mountain quartzite caves in southeastern Brazil and the 297 morphotypes that were identified to family level.
Cave names | Richness | Delta+ | Delta+ Sig % | Lambda+ | Lambda+ Sig % |
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Catedral III | 14 | 67.25 | 94.1 | 197.95 | 57.1 |
Bichana II | 17 | 68.53 | 47 | 215.48 | 77.1 |
Bichana I | 22 | 67.79 | 67.1 | 233.65 | 91.5 |
Catedral I | 11 | 66.18 | 75.9 | 187.24 | 56.1 |
Manequinho | 41 | 66.07 | 45 | 249.46 | 57.3 |
Cruz | 37 | 64.05 | 5.8 | 280.86 | 12.2 |
Dobras | 14 | 66.59 | 84.9 | 255.43 | 53.3 |
Ponte de Pedra | 23 | 65.77 | 52.3 | 271.84 | 30.2 |
Gnomos | 22 | 63.81 | 15.4 | 317.96 | 5.6 |
Lagarto Teiú | 32 | 68.31 | 36 | 208.42 | 39.4 |
Monjolinhos | 14 | 70.11 | 21.8 | 240.65 | 72.3 |
Martiniano | 23 | 68.06 | 55.9 | 279.65 | 22 |
Martiniano II | 12 | 63.33 | 24.2 | 261.62 | 50.5 |
Viajantes | 16 | 58.17 | 1 | 333.31 | 6.6 |
Fugitivos | 22 | 68.83 | 31.4 | 233.7 | 93.3 |
Pião | 18 | 68.5 | 49.8 | 191.86 | 34.4 |
Coelhos | 44 | 67.02 | 99.5 | 238.26 | 84.9 |
Bromélias | 70 | 69.16 | 1 | 234.78 | 96.9 |
Moreiras | 46 | 68.12 | 35.2 | 228.62 | 85.7 |
Casas | 34 | 68.91 | 17 | 210.05 | 36.4 |
The Distance-based linear models (DistLM) revealed in marginal tests that the sampled extension (
Distance-based redundancy analysis (
Finally, Figure
Metric multidimensional scaling (
Organic resources were composed of plant debris deposited close to vertical or horizontal entrances, as well as sparse roots, root stalagmites, termite galleries, guano of carnivorous bats (
The bat guano piles were always small and scarce, but were colonized by
All impacts observed in the caves were the consequences of tourism. Impacts like graffiti on the cave walls, trails and trampled soil were the most common, which were observed in almost all the studied caves. In some caves, the entrances located near the touristic trails garbage (organic and plastics) was found. In the Cruz cave, a wooden ladder was installed to facilitate the access of visitors. Currently, only three caves in the Park are open to tourist visitation: Pião, Coelhos and Monjolinhos caves. Other caves, like Bichana I and II, showed no signs of visitation, although they are located near the access road. Although few impacts were found inside the Park boundaries, the surrounding forests were removed for pastures and monocultures (such as
Besides the influence of potential epigean colonizers, the higher average richness found in the present work (39.55 spp., SD = 21.87 spp.) may have been influenced by the size of the studied caves (average: 180 m in length), which can promote a greater heterogeneity of habitats and support richer fauna. Furthermore, the dissimilarity and turnover may also have been determined by a higher variation in the heterogeneity of caves in terms of number and size of entrances, microhabitats and trophic conditions, which can promote diverse and heterogeneous communities (
Many troglophilic species do not occur randomly in caves, being preferentially found in humid, deep and dark areas (
It is known that cave extension represents an important environmental component determining species richness, since it can eventually provide more habitat heterogeneity (
The influence of big cave entrances is well known since cave entrances act as ecotones between epigean and hypogean sites, sheltering rich communities, with representatives of both epigean and hypogean fauna (
The presence of streams increase humidity and bring organic matter inside caves, and can also transport epigean species inside caves (
In Brazil, with exception of the iron ore cavities (
However the 37 species with troglomorphic traits sampled by
The use of caves for tourism is not uncommon and can be extremely important for the local economy worldwide (
Ibitipoca is a State Park and represents one of the most visited areas in the state of Minas Gerais. Nevertheless, its caves are not arranged for tourists. The management plan of the Park included caves, but cave species were not considered for planning conservation strategies (
Areas deforested for cattle ranching were observed in the surroundings of Ibitipoca Mountain and may have directly influenced the abundance of
The present study revealed a rich and diverse invertebrate community sheltered in Ibitipoca quartzite caves, influenced mainly by the extension of the caves and presence of streams. This relationship has been recurrent in several other studies conducted with caves associated with different lithologies in Brazil and can be considered a keystone element for the maintenance of cave biodiversity.
This work was sponsored by the FAPEMIG agency (Fundação de Amparo à Pesquisa de Minas Gerais) () (CRA APQ 01046-12). We thank Leda Zogbi for speleology assistance, Parque Estadual do Ibitipoca and the employees Rose, João Carlos, Alcino, Carlos, José Geraldo, Elias and José Luiz for provide accommodation and help with sample permission. RLF is grateful to the National Council of Technological and Scientific Development (CNPq) for the research grant No. 308334/2018-3. The authors are also grateful to the editors and reviewers for theirs valuable suggestions. Ross Martin Thomas reviewed the English. Lucas Mendes Rabelo contributed to this work as a Master degree student