Corresponding author: Thais Giovannini Pellegrini ( firstname.lastname@example.org )
Academic editor: Oana Moldovan
© 2016 Thais Giovannini Pellegrini, 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: Pellegrini TG, Ferreira RL (2016) Are inner cave communities more stable than entrance communities in Lapa Nova show cave? Subterranean Biology 20: 15-37. https://doi.org/10.3897/subtbiol.20.9334
Lapa Nova is a dolomitic Brazilian show cave. Invertebrate fauna registered for this cave is quite rich and abundant. During two intensive surveys in 2009, 24,482 invertebrate individuals belonging to 187 species were sampled. We found 160 species in April sampling, while in September sampling richness was considerably lower, 102 species, with a remarkable species turnover. In this paper the species richness, abundance and species diversity is presented. The Shannon`s diversity index was 2.79 and 2.87 for April and September, respectively. Although one would expect less variations to be found in the deep cave community (when compared to those located near the entrances), due to higher environmental stability, this was not observed at Lapa Nova cave. This “paradox” is probably due to the intense tourism that occurs in the cave, which imposes “instability” in all sectors, not only in nearby entrance areas. Visitation at the cave probably altered the expected natural distribution pattern, imposing a new organization of the communities, driven by the unstable conditions imposed by cave tourism.
Cave invertebrates, temporal turnover, beta diversity, tourism impact, Brazil
Despite the well know environmental stability in subterranean systems, it is not homogeneous for the whole extension of a cave. With the use of precise monitoring instruments, certain environmental variability can be detected (
In spite of the differences in stability among caves situated at different latitudes, the range of environmental instability intensity can also vary in different caves located in a same region. Such differences occur according to their physical conditions, presence of large bat populations, human use, among others (
Factors other than microclimate, can determine changes in the distributional patterns of subterranean species. Human use is an important factor that generates instability in the cave environment, especially in cases of high intense tourism. This type of use can modify patterns such as temperature, humidity and speleothem growth (
Studies investigating distribution of cave fauna have only focused on the cavernicolous species (troglobites) (e.g.
Although a recent study indicates the existence of two hotspots of subterranean biodiversity in Brazil (
However, studies that have accessed temporal and spatial variations of the entire subterranean community are scarce. The understanding of seasonal patterns generates subsidies for subterranean ecosystem conservation and management purposes. As such, the objective of the present work was to identify the alterations undergone by the invertebrate community associated to Lapa Nova, a large dolomitic cave of Minas Gerais state, Brazil, in two different sampling periods, considering two main “compartments”: inner communities and those communities associated to areas near entrances. Our main intention was to verify if inner communities are more “stable” than entrance communities considering the mean richness and abundance values in time, and also temporal beta diversity values and species composition variation, which, in theory, are more subject to external variations. It worth stating that in the publication by
The present study was conducted at the Lapa Nova dolomitic show cave, located in Vazante, northwest Minas Gerais state, Brazil (Fig.
In order to confirm if the sectors near entrances are more variable when compared to more isolated sectors, we used humidity and temperature data. This data is available at Lapa Nova Management Plan, and it was measured during four days in April (
The cave was divided into nine sectors, each corresponding to 1/9 of the total linear extension of Lapa Nova. Three sectors were located in entrance areas (Sectors 1, 4 and 5), the other six were in deeper regions of the cave (Sectors 2, 3, 6, 7, 8 and 9) (Figure
Two five-day field trips were carried out for collecting in the nine sectors, the first was in April, and the other in September, both in 2009. The invertebrate collections were conducted by the same team, composed of five biologists with experience in caving and invertebrates collection, and it was done through manual capture (with the aid of tweezers, brushes and hand nets). Sampling was conduced by visual searching throughout all the accessible places in the cave, prioritizing organic deposits (debris, carcasses, guano, etc.) and microhabitats (spaces under rocks, humid soil, cracks, speleothems, etc.). All the invertebrate species found in the sectors had some of their specimens collected. The organisms observed during the collections were counted and plotted on the cave map according to the methodology proposed by
All the collected invertebrates were identified to the lowest taxonomic level possible, using a stereomicroscope. The specimens were separated into morpho-species for determination of species richness. The collected specimens were fixed in 70% alcohol. Subsequently they were deposited in the Centro de Estudos em Biologia Subterrânea collection (Zoology Sector / Biology Department, Federal University of Lavras). Troglomorphic species were considered as troglobite, we performed visual searching outside the cave looking for those species under rocks and wood debris and they were not found, indicating that they are restricted to the subterranean environment.
In each sector we determined the richness, abundance and diversity of the invertebrate communities for each sampling period. The diversity calculation was made using the Shannon-Wiener index (
Accessing beta diversity components allow inferring about processes driving species distributions and biodiversity (
The similarity was evaluated among the fauna of all of the sectors of the cave, in the two periods. For that we used the Non-metric Multidimensional Scaling (n-MDS). The n-MDS was built based on the quantitative composition of the invertebrate fauna using the Bray-Curtis index. The existence of significant differences of the groups generated by the n-MDS was evaluated through ANOSIM, also done by the Bray-Curtis index. Finally, the SIMPER analysis was used to evaluate which species were responsible for such differences. All of the above analyses were conducted through the PRIMER 6.0 program.
In Lapa Nova, a total of 24,482 individuals were recorded distributed in 187 species. From this total, 16,996 were registered in the April sampling, and 7,486 in the September sampling. The richness found in April was 160 species, while in September, that number was lower, 102 species. Of the total of 187 species, 85 were only observed in the first sampling event, 26 only in the second and 76 occurred in both periods. Diversity values were 2.79 and 2.87 for the first and second sampling events, respectively.
In April, Diptera was the order that presented the highest richness, with 33 species, followed by Araneae and Coleoptera with 31 and 29 species respectively. In September, the richness was much lower, the highest values being presented by Diptera and Araneae, both with 15 species, followed by Coleoptera with 12 species (Table
Invertebrates collected and their abundance in the different sections in both seasons.
|SECTORS IN APRIL SAMPLING||SECTORS IN SEPTEMBER SAMPLING|
|Anystidae (Erythracarus sp.1)||1||19||6||2||4||1||5||1||4||2|
|Bdellidae (Bdellodes sp.1)||3||1||1||1||1|
|Teneriffiidae (Neoteneriffiola xerophila)||11||3|
|Ixodidae sp. 1||1|
|Laelapidae sp. 1||1|
|Laelapidae (Stratiolaelaps sp.1)||1||2||2||1|
|Melicharidae (Proctolaelaps sp.1)||1||8||9|
|Podocinidae (Podocinum sp.1)||8|
|Ctenidae (Isoctenus sp.1)||320||2||2||11||6||12||7||18||12||20||4||1||22||12||11||7||47||19|
|Sicariidae (Loxosceles variegata)||71||8||8||180||72||34||57||855||932||115||3||12||144||49||29||139||995||917|
|Sicariidae (Loxosceles sp.2)||1|
|Caponiidae (Nops sp.1)||1||2||1||1||4||2|
|Theridiidae (Theridium sp.1)||10||11||18||7||3||1||21||2||1||1||10|
|Eukoeneniidae (Eukoenenia sp.1)||9||3||31||1||4|
|Eukoeneniidae (Eukoenenia virgemdalapa)||1|
|Opiliones sp.1 (juvenile)||3||1||1|
|Platyarthridae (Trichorhina sp.1)||10||4|
|Pseudonannolenidae (Pseudonannolene sp.1)||1||1||1||6||1|
|Hypogastruridae (Acherontides sp.1)||1||10||3||5||1|
|Arrhopalitidae (Arrhopalites sp.1)||4||2||3||1||2||1||4||1||1||1|
|Coleoptera sp.10 (Larvae)||1|
|Coleoptera sp.12 (Larvae)||1|
|Coleoptera sp.8 (Larvae)||1|
|Dermestidae sp.1 (Larvae)||1|
|Dermestidae sp.2 (Larvae)||1|
|Staphylinidae sp.2 (Larvae)||8|
|Staphylinidae sp.6 (Larvae)||200|
|Tenebrionidae sp.1 (Larvae)||1||1||1||1|
|Tenebrionidae sp.2 (Larvae)||1||1||1||3||3||5||2||13|
|Tenebrionidae (Zophobas sp.1)||1||8||10||2||4||1|
|Chironomidae sp.1 (Larvae)||1||50|
|Chironomidae sp.2 (Larvae)||19||10||1|
|Chironomidae sp.3 (Larvae)||2||1||3||4|
|Diptera sp.1 (Larvae)||61||100||3||16||25||2||2550||125||2||50|
|Diptera sp.2 (Larvae)||61||100||1||16||25||1||2250||125||3||50|
|Diptera sp.3 (Larvae)||8|
|Diptera sp.4 (Larvae)||1|
|Diptera sp.5 (Larvae)||1|
|Keroplatidae sp.1 (Larvae)||1||1|
|Mycetophilidae sp.1 (Larvae)||1||2|
|Psychodidae (Pericoma sp.1)||2176||39||61||50||5||2||7||18||10||3||72||2||9|
|Psychodidae (Lutzomyia sp.1)||2||1||1||2||1|
|Diptera sp.1 (Pupae)||1|
|Phalangopsidae (Eidmanacris sp.1)||9||16||6||7||33||2||38||1||12||1|
|Phalangopsidae (Endecous sp.1)||87||47||14||43||10||14||31||149||124||26||17||42||20||10||16||16||125||31|
|Reduviidae (Zelurus sp.1)||5||2|
|Formicidae (Acromyrmex sp.1)||1|
|Noctuidae (Hypena sp.1)||21||3||98||9||12||82||75||1||131||19||187||35||10||39||13|
|Lepidoptera sp.1 (Larvae)||1|
|Tineidae sp.1 (Larvae)||5||10||38||6||40||17||104||22||342||58||1||3||3||19|
|Tineidae sp.2 (Larvae)||1||1|
|Erebidae (Latebraria sp.1)||1||2||1||4|
|Lepidoptera sp.1 (Pupae)||1|
|Ptiloneuridae (Euplocania sp.1)||6|
|Ptiloneuridae (Euplocania sp.2)||6|
|Lepidopsocidae (Nepticulomima sp.1)||8||3||5|
|Psocoptera juvenile sp.4||3||5||4|
|Psocoptera juvenile sp. 5||8||11||9|
|Psyllipsocidae (Psyllipsocus sp.1)||8||14||9||5||21||15||81||7||49||64||5||31||117||29||117|
|Psyllipsocidae (Psyllipsocus falcifer)||14||24||15||2||7||35||24||137||11||83||109||8||52||198||48||198|
|Psyllipsocidae (Psyllipsocus sp.3)||1||2||1||3||3||14||1||8||11||5||20||5||20|
|Psyllipsocidae (Psyllipsocus sp.4)||3||13|
Six troglomorphic species were found: Arrhopalites sp. (Collembola: Arrhopalitidae) (Fig.
A Passage in Lapa Nova Cave B, C, D, E Examples of troglomorphic species recorded in the Northwest region of the state of Minas Gerais, Brazil. B Collembola: Arrhopalitidae: Arrhopalites sp.1 C Collembola: Poduromorpha, Acherontides sp.1 D Araneae: Ochyroceratidae sp.1 and E Pseudoscorpiones: Chthoniidae, Pseudochthonius sp.1.
The sectors of the cave did not present significant differences when comparing the two sampling events. There was a large overlap of species abundance in both sampling events by the similarity analysis conducted through n-MDS. Similarly, the ANOSIM test between the two periods was not significant (p=0.062) (Figure
Multidimensional scaling (n-MDS) of sectors collected in April (circles) and September (triangles) periods, by the Bray-Curtis quantitative similarity index.
The average richness in entrance sectors and inner sectors was quite distinct. In entrance areas the average richness corresponded to 66 species in the first sampling event and 54 species in the second. Inner areas of the cave present an average of 28 species in April and 24 species in September (Table
Richness and Diversity values of the ten sectors in both sampling events.
|Sector||April Richness||September Richness||Total Richness||Mean Richness||Turnover||Nestedness||β-Diversity|
Entrance sectors and inner sectors also did not present significant differences among species composition and relative abundance between both sampling events (Figure
Multidimensional scaling (n-MDS) of sectors in entrance areas in April (A-black triangles), and sectors in deep areas of the cave in April (A-black circles), and sectors in entrance areas in September (S-white triangles), and sectors in deep areas of the cave in September (S-white circles), by the Bray-Curtis quantitative similarity index.
The species that mostly contributed to the dissimilarity observed in the entrance sectors between both sampling events were: Pericoma sp. (Psychodidae, Diptera), responsible for approximately 24.5% of such differences; followed by Hypena sp, responsible for 7%; Loxosceles variegata (Sicariidae, Araneae), with 5.5%; Psyllipsocus falcifer (Psocoptera), with 5.3%; Collembola sp2, with 4.3% and Isoctenus sp (Ctenidae, Araneae) 3.6% (Table
SIMPER analysis. Species that mostly contributed to dissimilarity presented by entrance sectors in both sampling events.
|Taxa||Individual Contribution||Cumulative %||September||April|
Deeper regions of the cave presented a different pattern. The species that most contributed to differences presented by such sectors were Loxosceles variegata, responsible for approximately 25.5% of such differences; followed by two species of dipteran larvae that together are responsible for 20% and Psyllipsocus falcifer (7.5%). Those species, together, were responsible for more than 50% of the similarities among the inner sectors in both periods (Table
SIMPER analysis. Species that mostly contributed to dissimilarity presented by deep sectors in both sampling events.
|Taxa||Individual Contribution||Cumulative %||September||April|
|Tineidae sp.1 (Larvae)||4.21||66.57||4.33||88.83|
The most common species found in Lapa Nova were those most ubiquitous in northwestern Minas Gerais limestone caves (
Despite the common statement that caves are stable environments, such environments can have strong responses to changing surface climate (
Considering other biological parameters such as richness and diversity: richness usually increases in the rainy period; diversity, in turn, does not show a well-established pattern (
Cave and subterranean mine entrance areas present a greater density of many populations (
Beyond the higher richness in entrance areas, one would expect less variation to be found in the inner communities when compared to those located near the entrances, due to higher environmental stability. However, at the Lapa Nova cave such tendency was not observed. Despite the higher climatic differences at entrances areas, inner communities did not vary less, in composition, than those located near entrances, as observed though temporal beta diversity. The high species turnover in all sampled sectors reflects species replacements (
The touristic use of a cave, if uncontrolled, can potentially lead to population size reduction of some species, and this is especially dramatic considering troglobitic species. At Areias Cave System in Brazil, intense tourism led to a strong reduction in the population size of the cavefish, Pimelodella kronei (
It worth stating that at La Verna chamber (France), cave tourism did not impose any negative impact on the troglobitic species, which include 18 endemic hypogean invertebrates (
Lapa Nova cave revealed to be a quite peculiar system, not only regarding its dimensions and geology, but also as to the patterns existent in the associated fauna. Visitation at the cave probably altered the expected natural community distribution pattern, as has already been stated in Romania show caves studies (
To colleagues Érika Linzi Taylor, Maysa Fernanda de Souza and Marconi Souza Silva, for their help with field work. We also would like to thank Mr. Severino, that for many years ensured the protection of the Lapa Nova cave. To the researchers, for the identification of taxonomic groups: Thaís Oliveira do Carmo (Psocoptera), Leopoldo Bernardi (Acari), Maysa Fernanda de Souza (Palpigradi) and Daniele Pompeu (Pseudoscorpiones). To Professor Paulo Pompeu, for his assistance with statistical analyses. To Professor Júlio Louzada and Rogério Parentoni Martins, for their suggestions. To Votorantim Metais and Carste Consultores Associados Ltda for the financial support given to this work. This work was supported by the FAPEMIG under Grant [no. APQ-01854-09]; Conselho Nacional de Pesquisa (CNPq) provided funding to R.L.F. under Grant [CNPq grant nr. 304682/2014-4].