Cave physical attributes influencing the structure of terrestrial invertebrate communities in Neotropics

Abstract

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.

Full text

Cave physical attributes inuencing the structure... 103
Cave physical attributes influencing the structure of
terrestrial invertebrate communities in Neotropics
Matheus Henrique Simões1,2, Marconi Souza-Silva1, Rodrigo Lopes Ferreira1
1 Universidade Federal de Lavras, Departamento de Biologia, Setor de Zoologia Geral, Centro de Estudos em
Biologia Subterrânea, Mailbox 3037 Campus Universitário, Zip Code 37200-000 Lavras, Minas Gerais,
Brazil 2 Universidade Federal de Lavras, Departamento de Biologia, Programa de Pós-Graduação em Ecologia
Aplicada, Mailbox 3037, Campus Universitário, Zip Code 37200 000, Lavras, Minas Gerais, Brazil
Corresponding authors: Marconi Souza-Silva (marconisilva@dbi.ua.br); Rodrigo Lopes Ferreira (drops@dbi.ua.br)
Academic editor: O. Moldovan|Received 19 June 2015|Accepted 10 October 2014|Published 6 November2015
http://zoobank.org/6F716D01-B6ED-4837-BD50-B51A122F9C18
Citation: Simões MH, Souza-Silva M, Ferreira RL (2015) Cave physical attributes inuencing the structure of terrestrial
invertebrate communities in Neotropics. Subterranean Biology 16: 103–121. doi: 10.3897/subtbiol.16.5470
Abstract
e 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
inuence on the cave biological communities. e objective of the present study was to evaluate the cor-
relation 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. e richness of troglomorphic species was
positively correlated to the presence of perennial pools and linear development of the caves. e 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.
Subterranean Biology 16: 103–121 (2015)
doi: 10.3897/subtbiol.16.5470
http://subtbiol.pensoft.net
Copyright Matheus Henrique Simões et al. 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.
RESEARCH ARTICLE
Subterranean
Biology Published by
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Matheus Henrique Simões et al. / Subterranean Biology 16: 103–121 (2015)
104
Keywords
Cave entrances, linear development, cave streams, puddles, subterranean fauna, invertebrates
Introduction
Caves are usually dark, have constant temperature and high humidity according to
the isolation from the surface, thus resulting in high environmental stability (Poulson
and White 1969, Culver 1982). e availability of food resources in caves is limited,
predominantly with allochthonous organic matter being imported by lotic and perco-
lating water, bats and plant roots (Poulson and White 1969, Simon et al. 2003, Culver
and Pipan 2009, Souza-Silva et al. 2011a and 2012).
Subterranean environmental stability is directly related to how isolated it is from
the epigean environment. e number, width, position and distribution of the en-
trances in relation to the extension of the caves can increase or reduce the environ-
mental stability of the cavity and consequently provoke changes in their biological
community structures. Besides inuencing environmental stability, these metrics can
limit or increase the availability of food resources and likewise inuence the number of
species colonizing the environment (Ferreira 2004, Souza-Silva et al. 2012a).
Hydrological changes can be another factor that inuences the cave fauna. Cave
streams and perennial pools can act increasing the humidity and importing organic matter,
being determinant for the food resources availability (Souza-Silva et al. 2012 and 2012a).
Dierences in species number between distinct places have puzzled naturalists
and ecologists and several hypotheses have been developed to explain these dierences
(Williams 1964, MacArthur and Wilson 1967). In general, species number change ac-
cording to the temporal and spatial habitats traits.
It is known that the number of troglobitic species increases as the sampled area
increases (Culver et al. 1999), as well as the total number of species increases with the
size of cave (Culver et al. 2004, Ferreira 2004, Souza-Silva 2008). e cave size also
inuences the number of species at dierent levels according to the cave lithology. For
example, the increase on the number of species as the cave size increased is more intense
in iron core caves when compared to the other lithologies (Souza-Silva et al. 2011b).
Changes in species composition and richness through replacement, loss or gain
among dierent caves of the same area or in the same cave can occur over time and space
(Bento 2011, Souza-Silva et al. 2011b, Souza-Silva et al 2012a). Some methods have been
proposed to evaluate beta diversity, that consider the degree of change in community
composition or the community dierentiation, in relation to a gradient of environment,
or distinct samples (Whittaker 1960, Baselga 2007, 2010, Carvalho et al. 2012, 2013).
In this paper we veried the inuences of cave metrics (width of entrances and
linear development) and the presence of water bodies (presence of temporary or peren-
nial puddles and of streams and seasonal ooding) on invertebrate cave fauna of the
Neotropical region.

Cave physical attributes inuencing the structure... 105
Methods
Study area
We conducted the study from 2000 to 2011 in 55 limestone caves of the Brazilian
Savannah, northwest of Minas Gerais state, Brazil (Figure 1). According to climatic
classication of Köppen-Geiger, the region is classied as Aw with two distinct sea-
sons, rainy and dry. e region presents an average annual temperature between
20and 26 °C and maximum relative humidity around 80% and minimum around
50% (Alvares 2014).
Cave metrics and water bodies
We measured the width of entrances and linear development of the caves. We consid-
ered the width of entrance as the greatest horizontal length of the entrance prole 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 ooding, and with perennial cave streams.
Sampling terrestrial cave fauna
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
(Ferreira 2004, Souza-Silva et al. 2011b). e collection team was always composed by
ve biologists (always the same team) with experience in caving and manual collection
of invertebrates, as recommended by Weinstein and Slaney (1995). To ensure that the
sample was the most standardized as possible, the sampling time was approximately 10
minutes in 10 m² for each biologist (Souza-Silva et al 2011b).
We separated all specimens into morphospecies taxa for all statistical analysis
(Oliver and Beattie 1996, Derraik et al. 2002, Ward and Stanley 2004, Derraik et
al. 2010, Souza-Silva et al. 2011b). Oliver and Beattie (1996) showed that morphos-
pecies identied by non-specialists can provide estimates of richness and turnover
consistent with those generated using species identied by taxonomic specialists.
e use of morphospecies or corrected morphospecies inventories in the analyses
provided results generally concordant with conventional species inventories (Oliver
and Beattie 1996a).

Matheus Henrique Simões et al. / Subterranean Biology 16: 103–121 (2015)
106
Determination of troglobite/troglomorphic species
We determined the troglobite/troglomorphic species through the identication of troglo-
morphisms 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 (Culver and Wilkens 2000, Culver and Pipan 2009).
Statistical analyses
To normalize the variables the values of entrance width and linear development of the
caves were log-transformed to reduce the inuence of extreme values. e total species
Figure 1. Cave distribution at Minas Gerais state, Brazil (black triangle), where terrestrial invertebrates
were sampled.

Cave physical attributes inuencing the structure... 107
richness, was normally distributed (Shapiro Wilk test = 0.918; p = 0.001). e rich-
ness of troglomorphic species recorded a lot of zeros, and it was not possible to reach
normality for this variable.
We evaluated the inuence of the entrances width and cave linear development
on the species richness through linear regression. Inuences of the presence/absence
of dierent categories of water bodies were evaluated with ANOVA one-way for total
richness and non-parametric ANOVA (Kruskal-Wallis test) for richness of troglomor-
phic 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 ooding, and
was not considered in the analyses.
We used the Jaccard index to compare the fauna composition in dierent caves
(Magurran 2004). is index is the most suitable for presence/absence data since it
does not assign weight to the species abundance, such as the Bray-Curtis index com-
monly used in ecological studies. Beta diversity has been calculated in accordance with
the proposals of Carvalho et al. (2012, 2013) and Cardoso et al. (2015), in which it
is possible to perform the partition of this measure by means of the contribution of
replacement and dierences in species richness. We performed the partition of beta
diversity using BAT package developed by Cardoso et al. (2015). e objective of this
analysis was to assess whether the dissimilarity between the communities was inu-
enced more by replacement than by dierences in species richness.
We performed the DistLM test to verify the inuence of metric parameters and
the presence/absence of dierent categories of water bodies on species composition of
the caves (Anderson 2004). is test shows which variable or variables can inuence
the fauna composition (McArdle and Anderson 2001). We used non-metric multidi-
mensional scaling (nMDS), based on the Jaccard index, to visualize groups of caves
according to the variables that best explained the species composition identied in the
DistLM test. We performed the ANOSIM one-way (Jaccard index) analysis to test the
signicance of the separation of groups (Clarke 1993).
Results
e higher entrance width was recorded for Marcela Cave (125 m; Table 1). Lapa
Nova Cave, with 4,000 meters sampled, presented the longest linear development (Ta-
ble 1). Most of the caves (n = 38) were dry throughout the year and others had water
bodies. Nine caves had puddles, one was subject to seasonal ooding and seven of
them had rivers (Table 1).
We recorded 1,451 invertebrate taxa, distributed in at least 174 families (Table 2).
Diptera presented the highest richness (326 taxa), followed by Coleoptera (250 taxa) and
Araneae (169 taxa) (Figure 2). Families with the highest number of taxa recorded were
Chironomidae (45taxa), Staphylinidae (79) and eridiidae (24) respectively (Table 2).
e average richness was 58 morfospecies (SD = 26). Lapa Nova cave presented the
highest richness (153 taxa), followed by the Vereda da Palha cave (107 taxa) (Table 1).

Matheus Henrique Simões et al. / Subterranean Biology 16: 103–121 (2015)
108
Table 1. Municipalities, caves, water bodies (WB) (CS: cave streams, P: puddles, SF: dry caves subject to
seasonal ooding, 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

Cave physical attributes inuencing the structure... 109
Municipalities Caves WB WE (m) LD (m) S TS
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
Figure 2. List of sampled higher taxa and their species richness.
Only 2.3% of the invertebrates presented troglomorphic traits (33 taxa), distribut-
ed in 18 of the 55 sampled caves. Such taxa included Araneae (eight species), Isopoda
(six species), Collembola (six species), Polydesmida (ve species), Acari, Hirudinea,
Coleoptera, Opiliones, Palpigradi, Polyxenida, Pseudoscorpiones and Turbellaria (one
species each) (Table 3). e caves with the highest richness of troglobitic species were
the Lagoa Rica and Lapa Nova caves, with six species each one.
A signicant dierence 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 pres-
ence 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 3).

Matheus Henrique Simões et al. / Subterranean Biology 16: 103–121 (2015)
110
Table 2. Higher taxa and families recorded in 55 limestone caves in the Brazilian Savannah. Un: uniden-
tied. 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), Teneridae (1), Veigaiidae (2).
Amblypygi Phrynidae (1)
Araneae
Actinopodidae (1), Araneidae (16), Caponiidae (1), Ctenidae (12), Deinopi-
dae (3), Dictynidae (1), Dipluridae (1), Filistatidae (1), Gnaphosidae (1),
Leiodidae (1), Nemesiidae (2), Ochyroceratidae (2), Oonopidae (12), Pal-
pimanidae (1), Pholcidae (7), Prodidomidae (3), Pisauridae (1), Salticidae
(10), Scytodidae (2), Segestriidae (1), Sicariidae (1), Sparassidae (1), Symphy-
tognathidae (2), Tetrablemmidae (1), Tetragnathidae (1), eraphosidae (1),
eridiidae (24), eridiosomatidae (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), Cur-
culionidae (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), Scara-
baeidae (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), Ceci-
domyiidae (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), Syrphi-
dae (1), Tabanidae (1), Tipulidae (25)
Hemiptera Cydnidae (6), Hebridae (10), Ploiariidae (8), Reduviidae (7), Cicadellidae
(17), Cixiidae (12), yreocoridae (1)
Hymenoptera
Apidae (1), Braconidae (1), Eupelmidae (1), Encyrtidae (1), Evaniidae (2),
Formicidae (57), Halictidae (1), Ichneumonidae (2), Mutillidae (1), Ptero-
malidae (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)

Cave physical attributes inuencing the structure... 111
Higher taxa Families
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
Figure 3. Correlation between total richness and width of entrances, linear development and water body
presence/absence. e barr represents the average and the trace the standard deviation. Dierent letters
indicate signicant dierences in average richness.

Matheus Henrique Simões et al. / Subterranean Biology 16: 103–121 (2015)
112
Table 3. List of troglomorphic/troglobitic species recorded in the sampled caves in the Brazilian Savan-
nah, Minas Gerais state, Brazil, in the years 2000, 2009, 2010 and 2011. Un: unidentied.
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
No signicant relation was observed between the richness of troglomorphic species
and width of entrances. However, there was a signicant relation between the richness
of troglomorphic species and the linear development (R: 0.460, p < 0.001) and pres-
ence/absence of water bodies (H: 4.722, p < 0.013), with higher values in caves with
puddles (Figure 4).
In general the faunal troglophile composition was quite dissimilar between the
caves (average Btotal: 0.9786; variance: 0.0007). e recorded dissimilarity is explained

Cave physical attributes inuencing the structure... 113
Figure 4. Correlation between the richness of troglomorphic species and linear development and water
body presence/absence. e barr represents the average and the trace the standard deviation. Dierent
letters indicate signicant dierences in average richness.
Figure 5. Non-metric multidimensional scaling (Jaccard index) using presence and absence of species sam-
pled in 55 limestone caves of the Brazilian Savannah. e gure shows that the cave, despite dry most of the
year, is subject to seasonal ooding (Deus Me Livre cave), and then was more similar to caves with streams.

Matheus Henrique Simões et al. / Subterranean Biology 16: 103–121 (2015)
114
by the replacement of species (Brepl: 0.9786705). e contribution of dierences be-
tween number of species is near-zero (Brich < 0.0000001).
Despite the general high dissimilarity, the presence of water bodies signicant-
ly inuenced the species composition (DistLM Test, Pseudo-F: 1.901, R²: 0.054, p
< 0.001). e non-metric multidimensional scaling analysis (nMDS) showed that
among the water body categories, cave with streams were more similar regarding the
faunal composition (Figure 5, Stress: 0.18). is separation was conrmed by ANO-
SIM (one-way). A signicant dierence was observed between caves with streams and
dry caves (R: 0.443, p < 0.001) and caves with streams and with puddles (R: 0.541, p:
0.002), while dry caves and caves with puddles were not signicantly dierent.
Discussion
Little is known about the eects of physical characteristics determining the cave com-
munity richness and composition. Most of the studies regarding this topic showed
that number of species increases in large caves and with more entrances (Culver et al.
2003, Culver et al. 2004, Ferreira 2004, Souza-Silva et al. 2011b, Souza-Silva et al.
2012). Corroborating these previous studies our results demonstrated the eects of the
cave metric parameters on the number of terrestrial invertebrate species associated to
limestone caves in Brazil. Regarding the inuence of the presence of water bodies into
the caves, our ndings are new since no previous studies have shown similar results.
e relation observed between width of entrances and number of species (Figure
3) can be due to the fact that large entrances probably function as “windows” that
facilitate the colonization of hypogean systems by external invertebrates as well as the
input of organic matter. Caves with large entrances may have more interface areas with
the surrounding epigean system, thus increasing the establishment of para-epigean
communities (Ferreira and Martins 2001, Prous et al. 2004). It is worth noting that
caves with more entrances potentially may be capable to receive a greater amount
of organic material from the epigean environment, then increasing the food resource
availability inside the caves.
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 excel-
lent shelter sites and even permanence for several species (Prous et al. 2004), dierent
from what occurs in many temperate caves, in which the entrances, especially in the
winter, are almost as severely aected by the cold as the external environment (Culver
and Pipan 2009).
e increase in the linear development of caves was related to total number of taxa
(Figure 3) and number of troglobitic species (Figure 4). is tendency was also observed
in previous studies (Culver et al. 2003, Culver et al. 2004, Ferreira 2004, Souza-Silva
et al. 2011a). Larger caves present higher habitat and resource availability, which are
decisive factors for the subterranean fauna (Culver et al. 2006), thus allowing higher
number of species to establish (Culver et al. 2004, Ferreira 2004, Souza-Silva 2008). As

Cave physical attributes inuencing the structure... 115
an example, one can mention that larger caves allow the establishment of more species
and larger populations of bats (Brunet and Medelin 2001), then increasing the produc-
tivity of guano. Adding our ndings to the above mentioned studies we can say that
there is a positive relationship among the linear development, availability and variety
of habitats, resource availability and the number of species colonizing the cave environ-
ment. However, these variables work together and can inuence in dierent ways and
levels. One example is that a cave with a linear development of 200 m (Lagoa Rica) has
a similar number of total species (53 species) to Delza cave, with a linear development of
1400 m (46 species) and a similar number of troglobitic species (6 and 5, respectively).
Lotic systems, besides increasing the humidity, import organic matter from the
surrounding epigean environment to the inner parts of the caves. is provides food
resources for the fauna (Poulson and Lavoie 2001, Souza-Silva et al. 2011a).
Caves are oligotrophic environments and the increasing resource availability al-
lows more species to colonize and remain (Schneider et al. 2001). e amount of
organic matter imported by cave streams changes depending on the season, with larger
amounts during the rainy period (Souza-Silva et al. 2011a, 2012). Furthermore, dur-
ing the rains many invertebrate species can be carried into the caves and, since they use
organic matter as food and shelter, many species can remain throughout the year, thus
increasing the local richness (Souza Silva et al. 2012).
Streams can cause disturbances in the caves, mainly during the rainy period (oods),
leading to changes in the cave community (Souza-Silva et al. 2011). ese disturbances
are comparable to those predicted by the Flood pulse concept, initially proposed for
ood plains (Junk et al. 1989). is theory predicts that the system responds in func-
tion of the range, duration, frequency and regularity of the pulses. Regular pulses (that
can be the case of cave streams) lead terrestrial species to adapt to the conditions of the
aquatic/terrestrial transition zones. Furthermore, regular ood pulses can prevent all of
the ecological succession stages, as well as may lead to competitive exclusion.
Despite of the stress caused by ood pulses, cave streams maintain high species
diversity, similar to what occurs in aquatic/terrestrial zones in ooded plains, a fact that
corroborates the intermediate disturbance hypothesis (Connell 1978). It is important to
emphasize that temperate and tropical areas will respond dierently to the ood pulses
and that the ow rate of the cave stream is also a decisive factor (Tockner et al. 2000).
e number of troglobitic species was higher in caves with puddles (Figure 4).
Terrestrial invertebrates more specialized to the cave environment (troglobitic) present
adaptations to live under extreme moist conditions, as, for instance, cuticular reduc-
tion that increases the tegument permeability (Culver 1982). If the permeability of
the cuticle is increased, the terrestrial troglobitic are sensitive to low humidity levels,
losing water quickly (Howarth 1980). erefore, the higher richness of troglobitic spe-
cies recorded in the caves with puddles poses a new question: if the presence of rivers
maintains high humidity throughout the year and increase the availability of trophic
resources, why do those caves did not present more terrestrial troglobitic species?
Cave streams, in spite of maintaining the high humidity and increasing the avail-
ability of resources (Souza-Silva et al. 2011a), can cause disturbances that may eventually

Matheus Henrique Simões et al. / Subterranean Biology 16: 103–121 (2015)
116
prevent (or make dicult) the emergence of troglobitic species. Caves that undergo vio-
lent oods usually do not present many troglobitic species (Elliott 2004). One hypothesis
is that the disturbance caused by cave streams can cause constant exchange of terrestrial
specimens carried by streams and, consequently, increase the genetic ow, decreasing the
occurrence of speciation. is hypothesis still needs to be tested.
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 (Huppop 2012). In caves without streams with low availability
of resources the troglobitic species are certainly the best competitors. However, in caves
with high availability of food resources in association with the presence of epigean spe-
cies, this high availability of food may indirectly be a serious threat to troglobites (Sket
1977). Cave streams can also increase competition, especially in small caves, since
more species will be brought from the external environments.
e 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 dis-
turbance 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, es-
pecially 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
“lters” external fauna that could be brought during ooding pulses. However, in small
caves with streams and few dry channels, terrestrial species can be severely aected and
the troglobitic richness can decrease.
Beta diversity among the caves was high. e contributing factor was the replace-
ment of species and the dierences in species richness was near-zero. As we have re-
corded, the richness of terrestrial species is inuenced by the area of the cave, size
of the entrances and presence of water. ese added parameters can generate strong
and unique environmental lters within each cave, making it a highly heterogeneous
environment. ese 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 (Kole et al. 2003). While
in the epigean temperate regions the turnover of species suers strong environmental
inuence, tropics seem to suer more inuence of spatial variations that can limit the
dispersal (Myers et al. 2013). Furthermore the turnover can be higher in caves when
compared to epigean areas (Cardoso 2012).
All factors here seen lead us to expect high beta diversity values. is conrms
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
(Cardoso et al. 2014).
Despite the general high dissimilarity, the presence of cave streams inuenced the
species composition (Figure 5). is inuence can be explained by two factors: i) the
carried organic resource is similar and ii) the ood pulse selects the same species that are

Cave physical attributes inuencing the structure... 117
carried into the caves (turnover). Visually, most of the organic matter carried into the
caves was composed of plant debris (leaves and branches). Resources of similar origin
are exploited by similar cave communities (Schneider et al. 2011), in this case, mainly
detritivores. Flood pulses can carry soil species together with the organic matter (Souza-
Silva et al. 2012a) and only those ones adapted to the oods and the cave environment
can survive. us, eventually the same species have being selected in dierent caves.
An example is the Deus Me Livre cave. Despite it is dry during part of the year, it
is subject to seasonal ooding caused by runo during the rainy season, since its en-
trance is located in the bottom of a sinkhole. e fauna of this cave is more similar to
the caves with streams (Figure 5), demonstrating that ood pulses caused by runo are
probably selecting the same species, supporting the previous hypothesis.
In the dierent Brazilian regions, the litter invertebrate fauna is composed main-
ly of Acari, Coleoptera, Gastropoda, Oligochaeta, Isopoda, Arachnida, Diplopoda,
Chilopoda and Blattaria (e.g. Ferreira and Marques 1998, Moreira et al. 2006). ese
are also the main groups recorded in caves (Pinto-da-Rocha 1995, Romero 2009),
what makes high the similarity between groups of cave invertebrates (especially those
with streams) and soil invertebrate fauna in the Tropical region.
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 Sket 2008),
demanding a deep knowledge of the biology of each group, as well as of their presence
(or not) in the epigean systems. Novak et al. (2012), in a study on species distribution
in the cave environment, separated the groups in only two categories, troglobitic and
non-troglobitic (including all other categories), precisely because of the diculty on
separating the other categories (troglophile, trogloxene and accidental).
Due to the high similarity between the litter and cave fauna and the diculty on
accurately separate which species are associated to the cave, how can we actually sepa-
rate 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 spe-
cies may use the carried organic matter as shelter and food resource (Souza-Silva et al.
2012a), only with more detailed long term studies it will be possible to determine the
degree of association of those species with the cave environment.
e highlight in this study is the increase in the terrestrial species richness accord-
ing to metric parameters and the presence of streams, since largest entrances and water
courses can inuence cave colonization and detritus input. e 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 troglo-
bites indicating that the humidity maintenance throughout the year is an important
factor for the evolution and maintenance of these species. e beta diversity was high
among caves, thus indicating physical and environmental heterogeneity that may be
unique to each cave. Our ndings highlight that big and wet caves shelter more diverse
and complex terrestrial invertebrate communities, what enhances the need for conser-
vation, management and restoration of the cave surroundings in tropical caves.

Matheus Henrique Simões et al. / Subterranean Biology 16: 103–121 (2015)
118
Acknowledgements
We would like to thank the Fundação de Amparo à Pesquisa e Extensão de Minas Gerais
(FAPEMIG) for nancial support, project APQ-01854-09. To all the team from the Cen-
tro de Estudos em Biologia Subterrânea of Universidade Federal de Lavras. We would like
to thank Carla Ribas, aís Pellegrini and Nelson Curi for their suggestions. To Pedro Car-
doso (Finnish Museumof Natural History, University of Helsinki/ Azorean Biodiversity-
Group) and Vanessa Martins for the help with data analyses. To the Espeleo Grupo de Bra-
sília for information about some caves in the area. RLF is grateful to the National Council
of Technological and Scientic Development (CNPq) (grant n° 3046821/2014-4).
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