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Formatted: Justified

Turnover structuring the β-diversity and few habitat-generalist species contributed

mainly to metacommunity nestedness in tropical mountaintops

Turnover structuring spatial β-diversity in tropical mountaintops but few habitat-

generalist species drives metacommunity nestedness

Frederico S. Neves1, Pedro G. Silva1, Ricardo R. C. Solar1, Cassio Nunes1, Marina V.

Beirão1, Humberto Brant1, Flávio Castro1, Wesley Dáttilo1, Roger Guevara1, G. Wilson

Departamento de Biologia Geral, Universidade Federal de Minas Gerais, Belo

Horizonte, Brazil.
Graduate School in Ecology, Conservation and Wildlife Management, Federal

University of Minas Gerais, Belo Horizonte, Brazil.

Department of Biodiversity Evolution and Environment, Federal University of Ouro

Preto, Ouro Preto, Brazil

Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ,

Department of Ecology, University of São Paulo, São Paulo, Brazil.

Formatted: English (United States)


Mountains are important systems for the maintenance of endemic species and

ecological and evolutionary processes (Graham et al. 2014, Noroozi et al. 2018, Silveira

et al. 2018, Rangel et al. 2018). Studies in mountains generally find two patterns of

species distribution along altitudinal gradients, a linear pattern of decreasing diversity

with increasing altitude or a hump-shaped pattern peaking at mid-elevations (Peters et al.

2016, Longino and Branstetter 2018). Both patterns generate a high spatial β-diversity

among communities (Fernandes et al. 2016, Mota et al. 2018, Peillo et al. 2018), forming

very diverse metacommunities. A metacommunity refers to a collection of communities

of potentially interacting species that are interconnected by dispersal (Leibold et al. 2004;

Holyoak et al. 2005). There are often large differences in habitat use and movements and

dispersal among species in a metacommunity, which depend on several factors, including

behavior, body size or trophic level (Chase and Bengtsson livro). This variation in

dispersal rates can influence metacommunity structure and the partitioning of diversity.

β-diversity is key in to understanding how communities change across

spatiotemporal scales (Anderson et al. 2011, Silva & Hernández 2018) and it may reflect

two different processes:, species turnover or nestedness among sites (Baselga 2007,

2010). Differences in characteristics among taxa and the use of habtitathabitat use can

determine the formation of the β-diversity in metacommunities. In tropical mountains,

the turnover of species species turnover among elevations is generally the main process

that shapes the β-diversity (Mota et al. 2018, Nunes et al. 2016,a,b, Perillo et al. 2017).

Many species inhabiting mountaintops are geographically restricted and dispersal-limited

and have high rates of endemism (Fujita et al. 2014, Steinbauer et al. 2016, Noroozi et al.

Tropical mountain ranges in South America are fundamental as cradles

andbirthplace and museums of biodiversity (Rangel et al. 2018). Among them, Espinhaço

Range, with about 1200 km of extension, stands out for its diversity and endemism

(Silveira et al. 2016, 2018). In the highest regions of the Espinhaço RangeChain of the

Epinhaço, above 1000 m. a.s.l. are generally found two main habitats are generally found:,

the campo rupestre (rupestrian grassland), intermingled by granite outcrops, surrounding

forest islands, known as capões de mata (Fernandes 2016, Silveira et al. 2018). In these

systems, we will find species that we can be classified classify as habitat use either as

specialists or habitat generalists, based on the estimated relative abundance of species in

two distinguishable habitats (Chazdon et al. 2011). The distribution of these habitats in

the landscape and the dispersal rates of taxa can determine the distribution of species in

the metacommunity and the processes that structure the β-diversity and to the nestedness

of the metacommunity.

Nestedness is common in natural metacommunities and especially in human-

fragmented landscapes (Louzada et al 2010, Solar et al. 2015). Understanding the

processes responsible for nestedness patterns may be important for conservation planning

because it can help to highlight which factors have the greatest influence on species

spatial distribution in natural or anthropic landscapes (Fleishman et al., 2002; MacNally

et al., 2002). Nevertheless, the underlying causal processes linked to the nestedness

patterns in metacommunities are still poorly understood (Fischer and Lindenmayer 2005,

Louzada et al. 2010), especially in tropical mountains.

No presente trabalho temos o objetivo de verificar a importância do turnover and

nestednsess na determinação da β-diversity spatial de uma metacomunidade altiontana, e

verificar a importância desses processos para espécies especialistas e generalistas de

habtiat. Esperamos encontrar um elevado turnover na determinação da β-diversity

espacial independente do taxpnomic group (ants, butterflies or dung beetles) e que a

importância do turnover na determinação da β-diversity seja menor em espécies

generalistas de habitats se comparadas a espécies especialistas de habitat. Vamos também

verificar como características do habitat e do taxa podem determinar o aninhamento da

metacomundiade. Esperamos encontrar uma diferença entre os habitats, onde um habitat

mais permeável, como o campo rupestre, deve contribuir mais para o aninhamento da

metacomunidade se comparado a ilhas de florestas. Esperamos verificar também que

espécies generalistas de habitat devam ser mais importantes no aninhamento da

metacomunidade se comparadas às espécies especialistas de habitats, independente do

taxonomic group.

Here, we analyze the patterns of β-diversity and characteristics that contributed to

the metacommunity nestedness for three taxonomic groups; ants (Hymenoptera:

Formicidae), butterflies (Lepidoptera: Nymphalidae) and dung beetles (Coleoptera:

Scarabaeidae: Scarabaeinae). These insects are highly abundant, diverse and have a wide

geographical distribution (Davis et al. 2002, Gibb et al. 2017) and fulfil a suite of play

many important ecological roles functions (Folgarait 1998, Nichols et al. 2008, Nunes et

al. 2018). These taxa are dominant components of terrestrial biomes worldwide, are

highly sensitive to habitat gradients and have been used as bioindicators of environmental

conditions (Bonebrake et al. 2010, Nichols et al. 2007, Parr 2010, Spector 2006). In

addition also, a multi-taxa responses study as it can provide valuable information for the

development of effective conservation strategies in tropical mountains systems. Commented [DFV1]: Não entendi muito bem essa parte,
seria bom ver o texto original em português para poder
fazer uma correção mais precisa


Study area

The study was performed in the southern portion of the Espinhaço mountain range, called

Serra do Cipó, in Minas Gerais, southeast Brazil (19º14’19”S, 43º31’35”W; Fig. 1). The
Espinhaço formation extends almost continuously along 1200 km from northeast to

southeast Brazil, crossing two states (Bahia and Minas Gerais) and acting as a barrier

separating two Brazilian biomes, the Cerrado (Brazilian savanna) in the west and the

Atlantic Forest in the east. This mountain chain hosts high species richness, several

threatened and endemic species (Echternacht et al. 2011; Fernandes 2016; Silveira et al.

2016) in approximately 1% of the Brazilian territory (Bitencourt and Rapini 2013). Above

900 m a.s.l., there is the predominance of a grassland matrix called campo rupestre. The

campo rupestre is classified as an old, climate-buffered and infertile landscape (OCBIL)

(Hopper et al. 2016; Silveira et al. 2016). Immersed in the matrix of campo rupestre, there

are the Capões de Mata (hereafter called forest islands), which are natural patches of

forest islands emerging in mountaintops. These forest islands occur mainly above 1200

m a.s.l., with a floristic composition similar to seasonal semideciduous forests associated

with the Atlantic Forest domain (Coelho et al. 2018). The occurrence of forest islands is

restricted to erosion valleys without boulders, generally associated with headwaters and

small streams (Coelho et al. 2018). Average annual rainfall ranged between 1300 and

1600 mm with higher values in summer.

Sampling design

The study was performed in the two main systems found above 1000 m a.s.l. in

the Serra do Cipó, the campo rupestre and forests islands (Figure 1). We sampled 26 sites,

totaling an area of 66.149 km2, of which 11 sites of forests islands and 15 of campo

rupestre, and all sites are at least 200 m apart. Samplings occurred in two seasons in each

system, between 2013 and 2014, in the beginning and ending of rainy and dry seasons.

To quantify the ant metacommunity we used a set of 20 x 50 m plots in the central

region of each forest island a set of 20 x 50 m plot, where five pitfall traps were installed,
one in the center of the plot and four at its vertices. Along sites of campo rupestre we

used transects separated by at least 250 m apart, each consisting of five traps separated

by 50 m (25 traps per elevation). Iin each site we placed five soil pitfalls separated by 50

m. Pitfalls were 9 cm deep and 15 cm in diameter, contained 250 ml of a salt and detergent

solution and each trap was left in the field for 48 hours. To quantify the fruit-feeding

butterflies metacommunity we used five Van-Someren Rydon traps baited with fermented

banana with sugar cane juice. We sampled the fruit-feeding butterflies per for five

consecutive days in each season. Finally, to quantify the dung beetle metacommunity we

used in the central region of each forest island a set of 20 x 50 m plot where four pitfall

traps were installed at its vertices to collect dung beetles. Along sites of campo rupestre

sites we used transects separated by at least 250 m, each consisting of three traps separated

by 100 m (nine traps per elevation). Iin each site we placed five soil pitfalls separated

from each other by 50 m. Pitfalls were 9 cm deep and 15 cm in diameter, contained 250

ml of a salt and detergent solution, and were baited with 25 g of fresh human feces. Each

pitfall was left in the field for 48 h.

All taxa were collected, preserved and transported to the laboratory where all

captured individuals were identified to the lowest taxonomical level possible. We used

identification guides (Baccaro et al. 2015, BUTTERFLY, Vaz-de-Mello et al. 2011) and

consultation ofconsulted taxonomic experts. Dr. Rodrigo Feitosa for ants, Dr, Andre? for

buterflies and Dr. Fernando Vaz-de-Mello for dung beetles. All sampled material is

deposited kept at in the Centro de Coleções Taxonômicas of Instituto de Ciências

Biológicas of Universidade Federal de Minas Gerias and duplicated in Laboratório de

Ecologia de Insetos at the Universidade Federal de Minas Gerais (LEI-UFMG), and in

institutions where the specialists of each taxa are associated. Ants were deposited kept in

the Universidade Federal do Paraná, butterfly were deposited kept in the XXX and dung
beetles were deposited kept in the Zoological Collection of Universidade Federal de Mato

Grosso. All necessary sampling permits were issued by Instituto Chico Mendes de

Conservação da Biodiversidade (SISBIO #57764-1).

Data analyses

First, the species were classified based on their habitat use using the multinomial

classification models proposed by Chazdon et al. (2011). This analysis is based on the

relative abundance of individuals per taxa (ants, butterflies and dung beetles), minimizing

bias due to differences in sampling intensities between habitats and insufficient sampling

within each habitat (Chazdon et al. 2011). Using this analysis per taxa, these models

classifyies species into four groups: campo rupestre specialists (CRS), forest island

specialists (FIS), generalists and too rare to classify. We used a cutoff point of K = 0.5

for a simple majority rule or liberal threshold and a conservative P value of 0.005. We

used a conservative approach because our goal was to analyze the whole community

(Chazdon et al. 2011). We carried out the CLAM analysis using vegan v 2.4-0 (Oksanen

et al. 2015).

After that we calculated patterns of spatial distribution of insects

metacommunities using the β-diversity partitioning method (Baselga 2010). We modeled

β-diversity in two ways: between communities using a taxonomic approach, including all

taxonomic groups and per taxa (ants, buttlerflies and dung beetles) and a second analysis

using a habitat use approach (CRS, FIS, generalists and too rare). In all cases,

dissimilarity was measured partitioning the contribution of species turnover and

nestedness to β-diversity using the Sørensen (βSOR) and Simpson (βSIM) indices (Baselga

et al. 2010), to analyseanalyze changes to community structure. In both cases, we also

partitioned total β-diversity (βSOR) into the component derived from species turnover
(βSIM) and the component derived from species gain and loss or nestedness (βnest). We

performed analysies using taxonomic approach and habitat use approach using the

functions beta.multi of the R package betapart for species composition (Jaccard

coefficient) (Baselga & Orme 2012). For each data set, we also calculated pairwise

dissimilarity measures using the function beta.pair from the same R package.

In order to identify non-random insect species distribution patterns we conducted

the analysis in two steps. First, we tested if metacommunities of all species and per

taxonomic groups (ants, butterflies and dung beetles) were significantly nested with

respect to habitats (campo rupestre and forests islands) and to species. We estimated

nestedness using the NODF metric (Almeida-Neto et al. 2008) in the software program

ANINHADO (Guimarães and Guimarães 2006). NODF values for the whole

metacommunity ranged from 0 (non-nested) to 100 (perfectly nested). To verify the

significance of nestedness, we tested the empirical values against null distributions of

these values. In this case, we computed 1000 simulated networks generated by the Null

Model II (Bascompte et al. 2003). In this null model, the probability of occurrence of a

species is proportional to the number of species for of both sites and insect species. We

estimated the extent of contribution to nestedness, in which the metacommunity increase

or decrease the overall network nestedness, and compared this to our random

expectations, following Saavedra et al. (2011).

Since if the metacommunity was significantly nested, we explored the relative

contributions of habitats (campos rupestre or forest islands) using all insects or separately

by taxonomic group (ants, butterflies or dung beetles) and after that we explored the

relative contributions of species classification per habitat use (CRS, FIS, generalists or

too rare) to the nested pattern of the network. To test the predictions that the campo

rupestre contributes more to the nestedness of the metacommunity if compared to the

forests islands, we used the contribution to nestedness of each habitat using all insects,

and in each of the three taxonomic groups as response variables and the habitat (campo

rupestre or forest island) as explanatory factor using generalized linear models (GLMs).

To test if habitat generalist species contributes more to the nestedness of the

metacommunity if compared to the habitat specialist species we used a GLM, using

contribution to nestedness as response variable and the group taxonomic (ants, buttlerflies

and dung beetles), species classification (CRS, FIS, generalists or too rare) and the

interaction between these variables as explanatories factors. In all GLMs we used

Gaussian distribution, and we checked for the distribution of errors and over-dispersion

in the data. The minimal model was defined as the removal of non-significant variables

(p > 0.05) and when significant differences were observed in variables more than two

levels (group taxonomic or species habitat classification), we performed contrast analyses

analysis to determine differences among levels (Crawley 2013). For residual and contrast

analyses analysis we used the RT4Bio package in R (Reis Jr. et al. 2013). All analyses

analysis were performed using R 3.2.5 software (https://www.r-project.org).

We recorded 211 insect species/morphospecies in this landscape, involving 128

ants, 33 butterflies and 50 dung beetles (Table 1). In this metacommunity CLAM

classified 20 insect species (9.5 %) as campo rupestre specialists, 20 species (9.5 %) as

forest island specialists, seven species (3.3 %) as generalists of habitats and 164 species

(77.7 %) were indicated as too rare to classify (Table 1). Of the ant species recorded,

CLAM classified 10 species as campo rupestre specialists, 11 as forest island specialists,

six as generalists of habitats and 101 species were indicated as too rare to classify (Table

1). By the butterflies, CLAM classified only one specie as campo rupestre specialist, one

specie as forest island specialist, 31 species were indicated as too rare to classify and no
species was classified as habitat generalist (Table 1). Finally, for dung beetles CLAM

classified nine species as campo rupestre specialists, eight as forest island specialists,

only one specie as generalist of habitats and 32 species were indicated as too rare to

classify (Table 1).

The β-diversity in this landscape is determined mainly by species turnover, using

a taxonomic or a habitat use approach (Table 2). Turnover was the main component of β-

diversity, representing more than 90%, including all taxonomic groups or per taxa (Fig.

2a). When analyzing the metacommunity after habitat use classification, the β-diversity

continues to be determined mainly by species turnover, representing more than 55% of

β-diversity (Fig. 2b). However, we found an increase in the importance of nestedness in

forest island species (FIS), representing 44.4% of β-diversity.

We found that the metacommunity network was significantly nested, using all

species and per taxonomic groups (p < 0.05, Table 3), indicating that the species

composition at species-poor sites tends to be a subset of that in species-rich sites. Using

the GLMs was possible to verify that there is no difference in contribution between

habitats to nestedness pattern (p> 0.05) when comparing campo rupestre and forest

islands, using all species and per taxonomic groups (Table 4). To habitat use classification

we found that species generalists that most contributed to metacommunity nested pattern

(p < 0.05, Table 4). We also verified that the taxonomic group does not differ in relation

to contributed to nested (p > 0.05, Fig. 3). Although the number of generalist species

represents only 3.3% of the total, we confirm the prediction that these species contributed

more to nestedenns pattern, when compared to habitat specialists or too rare species. We

also verified that of forest islands specialists (FIS) contributed more to nested pattern,

when compared to campo rupestre specialists or too rare species.