Research Article |
Corresponding author: Marconi Souza-Silva ( marconisilva@dbi.ufla.br ) Corresponding author: Rodrigo Lopes Ferreira ( brazil.drops@dbi.ufla.br ) Academic editor: Oana Teodora Moldovan
© 2015 Matheus Henrique Simões, Marconi Souza-Silva, Rodrigo Lopes Ferreira.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Simões MH, Souza-Silva M, Ferreira RL (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
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The stability of temperature and humidity in caves is well known. However, little is known if higher or lower cave environmental stability (temperature, humidity, light and others) implies changes in the structure of the biological communities. Number, position and size of entrances, then size, depth, host rock and extent of the cave, the amount and type of food resources are all factors that can have strong influence on the cave biological communities. The objective of the present study was to evaluate the correlation between the presence of water bodies, size of entrances and the linear development of caves with the terrestrial invertebrate richness and species composition in 55 limestone caves located in the Brazilian Savannah, sampled from 2000 to 2011. Invertebrates were sampled by active search throughout the caves, prioritizing micro-habitats (sites under rocks) and organic resources (litter, twigs, feces and bat guano). We recorded 1,451 invertebrate species. Species richness was positively correlated with presence of cave streams, width of entrances and linear development of the caves. The richness of troglomorphic species was positively correlated to the presence of perennial pools and linear development of the caves. The presence of cave streams was a decisive factor for determining the community structure, increasing the number and the similarity of troglophile species among the caves. Flood pulses can cause disturbances that eventually select the same species besides importing resources. However, for the terrestrial troglomorphic species the disturbance caused by cave streams may decrease the number of species.
Cave entrances, linear development, cave streams, puddles, subterranean fauna, invertebrates
Caves are usually dark, have constant temperature and high humidity according to the isolation from the surface, thus resulting in high environmental stability (
Subterranean environmental stability is directly related to how isolated it is from the epigean environment. The number, width, position and distribution of the entrances in relation to the extension of the caves can increase or reduce the environmental stability of the cavity and consequently provoke changes in their biological community structures. Besides influencing environmental stability, these metrics can limit or increase the availability of food resources and likewise influence the number of species colonizing the environment (
Hydrological changes can be another factor that influences the cave fauna. Cave streams and perennial pools can act increasing the humidity and importing organic matter, being determinant for the food resources availability (
Differences in species number between distinct places have puzzled naturalists and ecologists and several hypotheses have been developed to explain these differences (
It is known that the number of troglobitic species increases as the sampled area increases (
Changes in species composition and richness through replacement, loss or gain among different caves of the same area or in the same cave can occur over time and space (
In this paper we verified the influences of cave metrics (width of entrances and linear development) and the presence of water bodies (presence of temporary or perennial puddles and of streams and seasonal flooding) on invertebrate cave fauna of the Neotropical region.
We conducted the study from 2000 to 2011 in 55 limestone caves of the Brazilian Savannah, northwest of Minas Gerais state, Brazil (Figure
We measured the width of entrances and linear development of the caves. We considered the width of entrance as the greatest horizontal length of the entrance profile and cave linear development as the linear development sampled in each cave. Some caves were not sampled throughout their total length. We placed the caves in four categories regarding water bodies: permanently dry, with puddles (perennial or seasonal), dry but subject to seasonal flooding, and with perennial cave streams.
Only terrestrial invertebrates were sampled during the study and each cave was visited once. We carried out the sampling by visual searching across the accessible parts of the cave, prioritizing organic deposits (debris, carcasses, guano, etc.) and microhabitats (spaces under rocks, humid soil, cracks, speleothems). Extensive visual searching and manual collections were made with the aid of tweezers, brushes and entomological nets (
We separated all specimens into morphospecies taxa for all statistical analysis (
We determined the troglobite/troglomorphic species through the identification of troglomorphisms in the specimens. Such characteristics vary among the groups, but frequently are represented by the reduction of melanin pigmentation, reduction of ocular structures and elongation of appendages (
To normalize the variables the values of entrance width and linear development of the caves were log-transformed to reduce the influence of extreme values. The total species richness, was normally distributed (Shapiro Wilk test = 0.918; p = 0.001). The richness of troglomorphic species recorded a lot of zeros, and it was not possible to reach normality for this variable.
We evaluated the influence of the entrances width and cave linear development on the species richness through linear regression. Influences of the presence/absence of different categories of water bodies were evaluated with ANOVA one-way for total richness and non-parametric ANOVA (Kruskal-Wallis test) for richness of troglomorphic species. One of the sampled caves (Deus Me Livre Cave) possesses a singular condition: despite being dry throughout the year, it is subject to seasonal flooding, and was not considered in the analyses.
We used the Jaccard index to compare the fauna composition in different caves (
We performed the DistLM test to verify the influence of metric parameters and the presence/absence of different categories of water bodies on species composition of the caves (
The higher entrance width was recorded for Marcela Cave (125 m; Table
Municipalities, caves, water bodies (WB) (CS: cave streams, P: puddles, SF: dry caves subject to seasonal flooding, D: dry), width of entrances (WE), sampled linear development (LD), total number of species (S), number of troglomorphic species/troglobitic (TS) in the studied area.
Municipalities | Caves | WB | WE (m) | LD (m) | S | TS |
---|---|---|---|---|---|---|
Arinos | Camila | CS | 5 | 120 | 98 | 2 |
Capa | CS | 17 | 480 | 101 | 0 | |
Marcela | CS | 125 | 400 | 78 | 0 | |
Suindara | D | 16.9 | 160 | 56 | 0 | |
Salobo | P | 6.8 | 40 | 47 | 2 | |
Taquaril | CS | 5 | 150 | 70 | 1 | |
Velho Juca | D | 7.2 | 70 | 47 | 2 | |
Cabeceira Grande | Caidô | D | 30 | 400 | 71 | 1 |
Porco Espinho | D | 4 | 17 | 36 | 0 | |
Coromandel | Huguinho | D | 4 | 35 | 38 | 0 |
Urubu | D | 2 | 50 | 34 | 0 | |
João do Pó | D | 4 | 180 | 48 | 0 | |
Ronan | D | 10 | 1000 | 46 | 0 | |
Ronan II | D | 6.5 | 160 | 25 | 0 | |
D’água | P | 9 | 80 | 33 | 0 | |
Morcegos | D | 3 | 86 | 31 | 0 | |
João Pinheiro | Sapecado | D | 1.5 | 20 | 26 | 0 |
Tauá | D | 15.4 | 26 | 22 | 0 | |
Lagamar | Vendinha | D | 7 | 300 | 72 | 0 |
Matutina | Cachoeira | P | 13.3 | 20 | 59 | 0 |
Nove | D | 1.6 | 7.85 | 48 | 0 | |
Campo de Futebol | D | 15 | 25 | 42 | 0 | |
Paracatu | Lagoa Rica | P | 5 | 200 | 53 | 6 |
Tamanduá II | D | 2 | 38 | 41 | 0 | |
Cava | D | 3.3 | 38 | 48 | 0 | |
Santa Fé | D | 21 | 78 | 30 | 0 | |
Brocotó | D | 4.5 | 30 | 72 | 0 | |
Brocotó II | D | 5 | 60 | 73 | 0 | |
Santo Antônio | P | 13.8 | 67 | 51 | 0 | |
Presidente Olegário | Caieira | D | 22 | 200 | 61 | 0 |
Juruva | CS | 15 | 250 | 105 | 1 | |
Vereda da Palha | CS | 14 | 250 | 107 | 0 | |
Unaí | Abriguinho | D | 6.5 | 8 | 34 | 0 |
Barth Cave | D | 14 | 160 | 47 | 1 | |
Cachoeira do Queimado | D | 52 | 160 | 57 | 2 | |
Encosta | D | 2 | 40 | 52 | 0 | |
Mata dos Paulista | CS | 1.5 | 30 | 63 | 0 | |
Frangas | D | 3 | 13 | 41 | 0 | |
Deus Me Livre | SF | 9 | 50 | 106 | 0 | |
Rio Preto | D | 4.6 | 38 | 56 | 2 | |
Malhadinha | D | 5 | 70 | 98 | 2 | |
Sapezal | P | 15 | 130 | 78 | 0 | |
Vazante | Abrigo da Escarpa | D | 10 | 4 | 36 | 0 |
Escarpa | D | 3 | 63.3 | 63 | 0 | |
Urtigas | D | 30 | 369 | 70 | 2 | |
Urubus | D | 24 | 61.3 | 93 | 3 | |
Não Cadastrada | D | 2 | 18.4 | 49 | 1 | |
V01 | D | 2 | 5 | 15 | 0 | |
V02 | D | 1.5 | 10 | 38 | 2 | |
Delza | P | 4 | 1400 | 46 | 5 | |
Mata Velha | P | 7 | 160 | 61 | 0 | |
Guardião Severino | D | 15 | 50 | 47 | 0 | |
Lapa Nova | P | 45 | 4000 | 153 | 6 | |
Lapa Nova II | D | 4.5 | 600 | 55 | 3 | |
Sumidouro da Vaca Morta | D | 7 | 16.1 | 72 | 0 |
We recorded 1,451 invertebrate taxa, distributed in at least 174 families (Table
Higher taxa and families recorded in 55 limestone caves in the Brazilian Savannah. Un: unidentified. Species numbers recorded for the families are inside the parentheses.
Higher taxa | Families | |
---|---|---|
Annelida | Oligochaeta | Un |
Arachnida | Acari | Ameroseiidae (1), Anoetidae (1), Anystidae (1), Argasidae (2), Bdellidae (3), Cheiletidae (1), Erythraidae (4), Ixodidae (3), Laelapidae (6), Macrochelidae (5), Macronyssidae (4), Melicharidae (1), Ologamasidae (1), Opilioacaridae (1), Otopheidomenidae (1), Parasitidae (1), Phthiracaridae (1), Podocinidae (1), Rhagidiidae (3), Teneriffidae (1), Veigaiidae (2). |
Amblypygi | Phrynidae (1) | |
Araneae | Actinopodidae (1), Araneidae (16), Caponiidae (1), Ctenidae (12), Deinopidae (3), Dictynidae (1), Dipluridae (1), Filistatidae (1), Gnaphosidae (1), Leiodidae (1), Nemesiidae (2), Ochyroceratidae (2), Oonopidae (12), Palpimanidae (1), Pholcidae (7), Prodidomidae (3), Pisauridae (1), Salticidae (10), Scytodidae (2), Segestriidae (1), Sicariidae (1), Sparassidae (1), Symphytognathidae (2), Tetrablemmidae (1), Tetragnathidae (1), Theraphosidae (1), Theridiidae (24), Theridiosomatidae (2), Trechaleidae (2), Uloboridae (2) | |
Opiliones | Gonyleptidae (12), Escadabiidae (2). | |
Palpigradi | Eukoeneniidae (2) | |
Pseudoscorpiones | Chernetidae (4), Chthoniidae (6), Garypidae (2). | |
Scorpiones | Buthidae (1) | |
Crustacea | Isopoda | Armadillidae (2), Dubioniscidae (3), Philosciidae (2), Platyarthridae (5), Porcellionidae (4), Styloniscidae (5) |
Insecta | Archaeognatha | Meinertellidae (4) |
Blattodea | Blaberidae (1), Blattellidae (15), Blattidae (8) | |
Coleoptera | Bostrichidae (1), Carabidae (29), Cholevidae (3), Chrysomelidae (4), Curculionidae (6), Dermestidae (6), Dryopidae (3), Elateridae (9), Elmidae (3), Endomychidae (1), Histeridae (3), Lampyridae (2), Nitidulidae (1), Omophronidae (1), Pselaphidae (9), Ptiliidae (3), Ptylodactilidae (6), Scarabaeidae (6), Staphylinidae (79), Tenebrionidae (16) | |
Collembola | Arrhopalitidae (4), Dicyrtomidae (2), Hypogastruridae (1) | |
Dermaptera | Labiidae (2) | |
Diplura | Japygidae (1) | |
Diptera | Agromyzidae (4), Anthomyzidae (1), Asilidae (2), Calliphoridae (1), Cecidomyiidae (36), Ceratopogonidae (15), Chironomidae (45), Chloropidae (1), Culicidae (2), Dixidae (1), Dolichopodidae (7), Drosophilidae (19), Empididae (1), Keroplatidae (1), Lauxaniidae (1), Milichiidae (6), Muscidae (6), Mycetophilidae (12), Phoridae (18), Psychodidae (18), Sarcophagidae (1), Sciaridae (13), Simuliidae (3), Stratiomyidae (5), Streblidae (1), Syrphidae (1), Tabanidae (1), Tipulidae (25) | |
Hemiptera | Cydnidae (6), Hebridae (10), Ploiariidae (8), Reduviidae (7), Cicadellidae (17), Cixiidae (12), Thyreocoridae (1) | |
Hymenoptera | Apidae (1), Braconidae (1), Eupelmidae (1), Encyrtidae (1), Evaniidae (2), Formicidae (57), Halictidae (1), Ichneumonidae (2), Mutillidae (1), Pteromalidae (2), Vespidae (2) | |
Isoptera | Termitidae (3) | |
Lepidoptera | Arctiidae (3), Geometridae (2), Hesperiidae (3), Noctuidae (24), Pyralidae (7), Satyridae (1), Tineidae (54) | |
Neuroptera | Ascalaphidae (1), Mantispidae (1), Myrmeleontidae (5) | |
Orthoptera | Gryllidae (2), Phalangopsidae (3), Tettigoniidae (1) | |
Psocoptera 4 | Lepidopsocidae (2), Liposcelididae (3), Psyllipsocidae (9), Ptiloneuridae (6) | |
Zygentoma 4 | Atelurinae (2), Lepidotrichidae (1), Lepismatidae (1), Nicoletiidae (4) | |
Mollusca | Gastropoda | Un |
Myriapoda | Geophilomorpha 1 | Geophilidae (2) |
Lithobiomorpha 1 | Lithobiidae (1) | |
Polydesmida 2 | Chelodesmidae (1), Paradoxosomatidae (1) | |
Polyxenida | Polyxenidae (5) | |
Scolopendromorpha 2 | Cryptopidae (1), Scolopendridae (1) | |
Scutigeromorpha 1 | Scutigeridae (2) | |
Spirobolida 1 | Rhinocricidae (1) | |
Spirostreptida 1 | Pseudonannolenidae (6) | |
Symphyla 2 | Scolopendrellidae (2), Scutigerellidae (2) | |
Nematoda | Nematoda | Un |
Platyhelminthes | Temnocephalida | Un |
Turbellaria | Turbellaria | Un |
Only 2.3% of the invertebrates presented troglomorphic traits (33 taxa), distributed in 18 of the 55 sampled caves. Such taxa included Araneae (eight species), Isopoda (six species), Collembola (six species), Polydesmida (five species), Acari, Hirudinea, Coleoptera, Opiliones, Palpigradi, Polyxenida, Pseudoscorpiones and Turbellaria (one species each) (Table
List of troglomorphic/troglobitic species recorded in the sampled caves in the Brazilian Savannah, Minas Gerais state, Brazil, in the years 2000, 2009, 2010 and 2011. Un: unidentified.
Higher taxa | Family | Morphospecies | Caves |
---|---|---|---|
Acari | Un | Trombidiforme sp8 | Rio Preto |
Annelida | Un | Hirudinea sp3 | Salobo |
Araneae | Ochyroceratidae | Araneae sp24 | Barth cave |
Ochyroceratidae sp1 | Urubus cave | ||
Oonopidae | Oonopidae sp3 | Lapa Nova cave | |
Oonopidae sp4 | Lagoa Rica cave | ||
Prodidomidae | Prodidomidae sp3 | Cachoeira do Queimado cave | |
Prodidomidae sp1 | Delza cave | ||
Tetrablemmidae | Tetrablemmidae sp1 | Lagoa Rica cave | |
Un | Araneae sp17 | Não Cadastrada cave | |
Coleoptera | Pselaphidae | Pselaphidae sp10 | Rio Preto |
Collembola | Arrhopalitidae | Arrhopalites sp1 | Delza, Lapa Nova, Lapa Nova II |
Un | Collembola sp5 | V02 | |
Hypogastruridae | Acherontides sp1 | Lapa Nova, Lapa Nova II | |
Un | Collembola sp12 | Lagoa Rica | |
Un | Collembola sp32 | Camila | |
Un | Collembola sp34 | Malhadinha | |
Isopoda | Platyarthridae | Trichorhina sp1 | Lagoa Rica, Urtigas, Delza, Lapa Nova |
Trichorhina sp3 | Urubus | ||
Trichorhina sp5 | Camila | ||
Trichorhina sp. | Velho Juca, Malhadinha | ||
Styloniscidae | Styloniscidae sp1 | Urtigas, Delza | |
Styloniscidae sp5 | Juruva | ||
Opiliones | Escadabiidae | Spelaeoleptes sp1 | Lagoa Rica |
Palpigradi | Eukoeneniidae | Eukoenenia virgemdalapa | Lapa Nova |
Polydesmida | Un | Polydesmoidea sp1 | Lapa da Delza |
Un | Polydesmoidea sp2 | Lagoa Rica | |
Un | Polydesmoidea sp3 | Caidô, Cachoeira do Queimado | |
Un | Polydesmoidea sp4 | Velho Juca | |
Un | Polydesmida sp2 | Urubus | |
Polyxenida | Polyxenidae | Polyxenidae sp5 | Taquaril |
Pseudoscorpiones | Chthoniidae | Chthoniidae sp2 | V02 |
Turbellaria | Un | Turbellaria sp6 | Salobo |
A significant difference was observed between the total richness of taxa and width of entrances (R: 0.424, p: 0.001), linear development (R: 0.519, p < 0.001) and presence of water bodies in the caves (R²: 0.279, F: 9.876, p < 0.001), and the richness of taxa was higher in caves with rivers (Figure
No significant relation was observed between the richness of troglomorphic species and width of entrances. However, there was a significant relation between the richness of troglomorphic species and the linear development (R: 0.460, p < 0.001) and presence/absence of water bodies (H: 4.722, p < 0.013), with higher values in caves with puddles (Figure
In general the faunal troglophile composition was quite dissimilar between the caves (average Btotal: 0.9786; variance: 0.0007). The recorded dissimilarity is explained by the replacement of species (Brepl: 0.9786705). The contribution of differences between number of species is near-zero (Brich < 0.0000001).
Despite the general high dissimilarity, the presence of water bodies significantly influenced the species composition (DistLM Test, Pseudo-F: 1.901, R²: 0.054, p < 0.001). The non-metric multidimensional scaling analysis (nMDS) showed that among the water body categories, cave with streams were more similar regarding the faunal composition (Figure
Non-metric multidimensional scaling (Jaccard index) using presence and absence of species sampled in 55 limestone caves of the Brazilian Savannah. The figure shows that the cave, despite dry most of the year, is subject to seasonal flooding (Deus Me Livre cave), and then was more similar to caves with streams.
Little is known about the effects of physical characteristics determining the cave community richness and composition. Most of the studies regarding this topic showed that number of species increases in large caves and with more entrances (
The relation observed between width of entrances and number of species (Figure
It is valid to note that the tropical region presents external conditions milder than those observed in temperate climate regions. Entrances of tropical caves provide excellent shelter sites and even permanence for several species (
The increase in the linear development of caves was related to total number of taxa (Figure
Lotic systems, besides increasing the humidity, import organic matter from the surrounding epigean environment to the inner parts of the caves. This provides food resources for the fauna (
Caves are oligotrophic environments and the increasing resource availability allows more species to colonize and remain (Schneider et al. 2001). The amount of organic matter imported by cave streams changes depending on the season, with larger amounts during the rainy period (
Streams can cause disturbances in the caves, mainly during the rainy period (floods), leading to changes in the cave community (Souza-Silva et al. 2011). These disturbances are comparable to those predicted by the Flood pulse concept, initially proposed for flood plains (
Despite of the stress caused by flood pulses, cave streams maintain high species diversity, similar to what occurs in aquatic/terrestrial zones in flooded plains, a fact that corroborates the intermediate disturbance hypothesis (
The number of troglobitic species was higher in caves with puddles (Figure
Cave streams, in spite of maintaining the high humidity and increasing the availability of resources (
One of the main physiological adaptations of the troglobites is the resistance to starvation, and such organisms are more resistant to oligotrophic environments than non-troglobitic species (
The largest number of terrestrial troglobitic species in caves with puddles indicate that these organisms are specialized to live in places with high humidity, but the disturbance caused by the presence of cave streams can eventually decrease the chances of troglobitic species to emerge. It is important to emphasize that there are exceptions, especially considering caves with large extensions. Such environments can allow distinct species to escape to areas out of the river and such big subterranean extensions certainly “filters” external fauna that could be brought during flooding pulses. However, in small caves with streams and few dry channels, terrestrial species can be severely affected and the troglobitic richness can decrease.
Beta diversity among the caves was high. The contributing factor was the replacement of species and the differences in species richness was near-zero. As we have recorded, the richness of terrestrial species is influenced by the area of the cave, size of the entrances and presence of water. These added parameters can generate strong and unique environmental filters within each cave, making it a highly heterogeneous environment. These can be some of the variables responsible for the high turnover of species between the caves. One may also consider that in tropics high values of beta diversity are expected when compared to temperate regions (
All factors here seen lead us to expect high beta diversity values. This confirms the prior predictions that high degree of micro-endemism occurs among subterranean groups (White and Culver 2012). It is important to mention that we only assessed the diversity of taxa. Considering other types of diversity such as phylogenetic and functional diversity, one would expect other still hidden patterns of diversity to emerge (
Despite the general high dissimilarity, the presence of cave streams influenced the species composition (Figure
An example is the Deus Me Livre cave. Despite it is dry during part of the year, it is subject to seasonal flooding caused by runoff during the rainy season, since its entrance is located in the bottom of a sinkhole. The fauna of this cave is more similar to the caves with streams (Figure
In the different Brazilian regions, the litter invertebrate fauna is composed mainly of Acari, Coleoptera, Gastropoda, Oligochaeta, Isopoda, Arachnida, Diplopoda, Chilopoda and Blattaria (e.g.
Another important factor is that the separation of the species according to the level of association with the cave is not always so simple (for details see
Due to the high similarity between the litter and cave fauna and the difficulty on accurately separate which species are associated to the cave, how can we actually separate the cave fauna from the soil fauna in Neotropics? Many species carried by streams with the organic matter can contain accidental groups, although a lot of species has certainly shown to be pre-adapted to the subterranean systems. Even though these species may use the carried organic matter as shelter and food resource (
The highlight in this study is the increase in the terrestrial species richness according to metric parameters and the presence of streams, since largest entrances and water courses can influence cave colonization and detritus input. The input of organic matter by streams is important for the maintenance of cave fauna, serving as shelter and food for several species. Caves with puddles presented higher richness of terrestrial troglobites indicating that the humidity maintenance throughout the year is an important factor for the evolution and maintenance of these species. The beta diversity was high among caves, thus indicating physical and environmental heterogeneity that may be unique to each cave. Our findings highlight that big and wet caves shelter more diverse and complex terrestrial invertebrate communities, what enhances the need for conservation, management and restoration of the cave surroundings in tropical caves.
We would like to thank the Fundação de Amparo à Pesquisa e Extensão de Minas Gerais (FAPEMIG) for financial support, project APQ-01854-09. To all the team from the Centro de Estudos em Biologia Subterrânea of Universidade Federal de Lavras. We would like to thank Carla Ribas, Thaís Pellegrini and Nelson Curi for their suggestions. To Pedro Cardoso (Finnish Museumof Natural History, University of Helsinki/ Azorean BiodiversityGroup) and Vanessa Martins for the help with data analyses. To the Espeleo Grupo de Brasília for information about some caves in the area. RLF is grateful to the National Council of Technological and Scientific Development (CNPq) (grant n° 3046821/2014-4).