the study was conducted at the mata seca state park ( mssp ) , located in the middle so francisco valley in the manga municipality , northern minas gerais state , brazil ( 144836145659 s and 435512440412 w ; fig .
the mssp was created in 2000 and has a total area of 15,466.44  ha consisting predominantly of deciduous forest ( madeira et al . 2009 ) .
climate in this region is classified as semi - arid according to the kppen system , with an average temperature of 24.4c and average annual rainfall between 242 and 848  mm .
the dry season extends from may to october , in which 9095% of tree species shed their leaves ( pezzini et al .
maps indicating ( a ) plot distribution , ( b ) location of the study area in brazil and ( c ) shape of the mata seca state park . 
  sampling sites at mata seca state park , southeastern brazil .
maps indicating ( a ) plot distribution , ( b ) location of the study area in brazil and ( c ) shape of the mata seca state park .
dung beetles were collected in the beginning , middle , and end of the wet season in december , february , and april of 20092010 ( fig .
the consistent rains start in october , we consider our first sampling ( december ) as the beginning of the rainy season .
we believe that the biotic and abiotic conditions are maintained in the first months of the rainy season due to abundant rainfall during this period ( pezzini et al .
2016 ) presenting vegetation in advanced stages of secondary succession ( over 20 years ) were selected , with plots located at least 0.2  km apart ( fig .
1 ) . to ensure the absence of vegetation structure effects on dung beetle communities we used the database from a prior study to calculate the richness and abundance of plants per plot ( madeira et al .
2009 ) . in each sample period , four traps were placed at the extremes of each plot . 

2.precipitation ( mm ) during july/2009 to june/2010 , data from mocambinho meteorological station , 15  km from mata seca state park ; and sampling periods ( december 2009 , february 2010 , and april 2010 ) indicated by gray bars . 
  precipitation ( mm ) during july/2009 to june/2010 , data from mocambinho meteorological station , 15  km from mata seca state park ; and sampling periods ( december 2009 , february 2010 , and april 2010 ) indicated by gray bars .
dung beetles were collected using pitfall - type traps consisting of plastic containers ( 14  cm in diameter  11  cm in deep ) buried with openings flush with the ground .
traps contained 250  ml of liquid detergent , water and salt solution to kill and preserve the beetles .
the pitfalls remained in the field for 48  h. subsequently the beetles were collected , sorted , and identified to the lowest taxonomic level using keys ( vaz de melo et al .
2011 ) and with the help of the taxonomist fernando vaz - de - melo .
the species were deposited in the collection of fernando vaz - de - melo at the federal university of mato grosso , mato grosso state , brazil .
each plot was considered a sample unit for the calculation of -diversity ( richness of species in a plot ) and dung beetle abundance .
-diversity among plots was calculated by   =  period/plot ( whittaker 1972 ) , where period is the total number of species per sample period ( december , february , april ) , and plot is the average species richness of the four sampling points ( pitfall traps ) within a plot .
only for -diversity calculation , the -diversity was considered as the average of species richness between traps within a plot . using this approach ,
mathematically independent values of  and  allow comparisons of  values between sample periods with different values of -diversity ( chao et al . 2012 ) .
we used generalized mixed linear models ( glmers ; lme4 package in r ) to test whether dung beetle -diversity and abundance were affected by sample period , assuming temporal pseudoreplication .
we used linear mixed models ( lmer ) for analysis of -diversity among sample periods .
plant richness and abundance were added to the models to test for effects of vegetation structure on dung beetles . in this approach , collection period ,
plant richness and abundance were used as explanatory variables , all nested within plot ( random effect ) , which were sampled temporally ( bates et al .
significance was estimated with an anova between the complete ( h1 ) and the null model ( h0 ) . the akaike information criterion ( aic )
was used to rank the models , since it represents the uncertainty of the model , a lower value of the aic represents the more parsimonious model . when significant differences were observed between sample periods ,
the data were submitted to contrast analysis by aggregating levels ( crawley , 2013 ) .
if the level of aggregation was not significant and did not alter the deviance explained by the null model , the levels were pooled together ( contrast analyses ) .
the decomposition of  was performed using the srensen ( sr ) and simpson ( sim ) dissimilarity indices ( baselga 2010 ) .
sim shows only species replacement , or turnover , and does not consider variation in species richness .
the difference between these indices indicates the total loss of species due to nestedness ( nes ) , such that ( nes  =  sr 
the study was conducted at the mata seca state park ( mssp ) , located in the middle so francisco valley in the manga municipality , northern minas gerais state , brazil ( 144836145659 s and 435512440412 w ; fig .
the mssp was created in 2000 and has a total area of 15,466.44  ha consisting predominantly of deciduous forest ( madeira et al . 2009 ) .
climate in this region is classified as semi - arid according to the kppen system , with an average temperature of 24.4c and average annual rainfall between 242 and 848  mm .
the dry season extends from may to october , in which 9095% of tree species shed their leaves ( pezzini et al .
maps indicating ( a ) plot distribution , ( b ) location of the study area in brazil and ( c ) shape of the mata seca state park . 
  sampling sites at mata seca state park , southeastern brazil .
maps indicating ( a ) plot distribution , ( b ) location of the study area in brazil and ( c ) shape of the mata seca state park .
dung beetles were collected in the beginning , middle , and end of the wet season in december , february , and april of 20092010 ( fig .
the consistent rains start in october , we consider our first sampling ( december ) as the beginning of the rainy season .
we believe that the biotic and abiotic conditions are maintained in the first months of the rainy season due to abundant rainfall during this period ( pezzini et al .
2016 ) presenting vegetation in advanced stages of secondary succession ( over 20 years ) were selected , with plots located at least 0.2  km apart ( fig .
1 ) . to ensure the absence of vegetation structure effects on dung beetle communities we used the database from a prior study to calculate the richness and abundance of plants per plot ( madeira et al .
2009 ) . in each sample period , four traps were placed at the extremes of each plot . 

2.precipitation ( mm ) during july/2009 to june/2010 , data from mocambinho meteorological station , 15  km from mata seca state park ; and sampling periods ( december 2009 , february 2010 , and april 2010 ) indicated by gray bars . 
  precipitation ( mm ) during july/2009 to june/2010 , data from mocambinho meteorological station , 15  km from mata seca state park ; and sampling periods ( december 2009 , february 2010 , and april 2010 ) indicated by gray bars .
dung beetles were collected using pitfall - type traps consisting of plastic containers ( 14  cm in diameter  11  cm in deep ) buried with openings flush with the ground .
traps contained 250  ml of liquid detergent , water and salt solution to kill and preserve the beetles .
the pitfalls remained in the field for 48  h. subsequently the beetles were collected , sorted , and identified to the lowest taxonomic level using keys ( vaz de melo et al .
2011 ) and with the help of the taxonomist fernando vaz - de - melo .
the species were deposited in the collection of fernando vaz - de - melo at the federal university of mato grosso , mato grosso state , brazil .
each plot was considered a sample unit for the calculation of -diversity ( richness of species in a plot ) and dung beetle abundance .
-diversity among plots was calculated by   =  period/plot ( whittaker 1972 ) , where period is the total number of species per sample period ( december , february , april ) , and plot is the average species richness of the four sampling points ( pitfall traps ) within a plot . only for -diversity calculation ,
the -diversity was considered as the average of species richness between traps within a plot . using this approach , mathematically independent values of  and 
allow comparisons of  values between sample periods with different values of -diversity ( chao et al . 2012 ) .
we used generalized mixed linear models ( glmers ; lme4 package in r ) to test whether dung beetle -diversity and abundance were affected by sample period , assuming temporal pseudoreplication .
we used linear mixed models ( lmer ) for analysis of -diversity among sample periods .
plant richness and abundance were added to the models to test for effects of vegetation structure on dung beetles . in this approach , collection period ,
plant richness and abundance were used as explanatory variables , all nested within plot ( random effect ) , which were sampled temporally ( bates et al .
significance was estimated with an anova between the complete ( h1 ) and the null model ( h0 ) .
the akaike information criterion ( aic ) was used to rank the models , since it represents the uncertainty of the model , a lower value of the aic represents the more parsimonious model . when significant differences were observed between sample periods ,
the data were submitted to contrast analysis by aggregating levels ( crawley , 2013 ) .
if the level of aggregation was not significant and did not alter the deviance explained by the null model , the levels were pooled together ( contrast analyses ) .
the decomposition of  was performed using the srensen ( sr ) and simpson ( sim ) dissimilarity indices ( baselga 2010 ) .
sim shows only species replacement , or turnover , and does not consider variation in species richness .
the difference between these indices indicates the total loss of species due to nestedness ( nes ) , such that ( nes  =  sr  sim ) .
we collected a total of 2,018 dung beetles across 39 species , distributed among 15 genera .
the december collection had the highest species richness , with 34 species ( 1,706 individuals ) .
february and april collections yielded 15 and 16 species ( 143 and 169 individuals , respectively ) .
six species were shared among all sample periods , and no species was sampled only in february .
hirculus , and deltochilum verruciferum were the most abundant species , representing together > 61% of the samples . 

table 1.abundances of scarabaeinae species sampled in the beginning , middle and end of the wet season ( december 2009 , february , and april 2010 ) in a tdf at the mata seca state park , minas gerais , braziltaxondecemberfebruaryaprilagamopus unguicularisharold , 18832200atheucus aff .
piluliformes5212canthon callybaeusblachard , 1846710canthon carbonariusharold , 1868300canthon histrioservile , 18284682453canthon lituratusgermar , 1813810canthon obscurielusschimidt , 1922500canthon sp1012canthon unicolorblanchard , 1846001coprophanaeus pertyiolsufieff , 1924100coprophanaeus cyanescensolsoufieff , 19242113deltochilum aff .
calcaratunbates , 187041171deltochilum enceladuskolbe , 18933020deltochilum pseudoicarusblathasar , 1939110deltochilum sp137260deltochilum verruciferumfelshe , 1911174449diabroctis mimaslinnaeus , 1758900dichotomius aff .
cuprinusfelche , 1901300dichotomius bosblanchard , 18461500dichotomius carbonariusmannerheim , 18296300dichotomius geminatusarrow , 1913011dichotomius glaucusharold , 18691400dichotomius nisusoliver , 1789002dichotomius puncticolisluederwaldt , 19353102eurysternnus caribaeusherbst , 1789600genieridium cryptopsarrow , 19131200ontherus appendiculatusmannerheim,18291130ontherus aztecaharold , 18692100ontherus dentatusluederwaldt , 1930008ontherus digitatusharold , 18683310onthophagus aff .
hirculusmannerheim , 18293851968trichillum externepunctatumborre,1880500uroxix bahianusboucomont , 192766010zoonocropi smachadoivaz - de - melo , 20072800total1706143169 abundances of scarabaeinae species sampled in the beginning , middle and end of the wet season ( december 2009 , february , and april 2010 ) in a tdf at the mata seca state park , minas gerais , brazil we found no effects of plant species richness and abundance on the dung beetle community ( - and -diversity , and abundance ) ( table 2 ) .
scarabaeinae -diversity and abundance were higher in december , and did not differ between february and april ( tables 2 , fig .
3a and b ) , while -diversity among plots was lowest in december ( table 2 ; fig .
3.dung beetles -diversity ( a ) , abundance ( b ) , and -diversity ( c ) ( mean    se ) along a rainy season at the mata seca state park , southeastern brazil . 
 table 2.results of the models ( glmer and lmer ) , showing temporal variation in -diversity , abundance and -diversity of dung beetles in a tdfresponse variablesexplanatory variablesaic ( h1)aic ( h0)pdung beetle -diversityplant richness135.68133.990.579  plant abundance134.0131.990.981 
month169.48180.20<0.001significance was estimated with an anova between the complete ( h1 ) and the null model ( h0 ) .
the aic represents the uncertainty of the model , thus a low value of the aic represents the more parsimonious model .
dung beetles -diversity ( a ) , abundance ( b ) , and -diversity ( c ) ( mean    se ) along a rainy season at the mata seca state park , southeastern brazil .
results of the models ( glmer and lmer ) , showing temporal variation in -diversity , abundance and -diversity of dung beetles in a tdf significance was estimated with an anova between the complete ( h1 ) and the null model ( h0 ) .
the aic represents the uncertainty of the model , thus a low value of the aic represents the more parsimonious model .
the decomposition of -diversity revealed that the relative importance of nestedness and species turnover varies between pairs of sample periods .
nestedness was the main process between december and february , while turnover was more important between february and april ( table 3 ) . between december and april ,
the two processes were equally important for structuring dung beetle communities ( table 3 ) . 

table 3.results from decomposition of dung beetle -diversity in the beginning , middle and end of wet season ( december 2009 , february , and april 2010 ) in a tdf at the mata seca state park , minas gerais , brazilparameterperiodsimnessrspecies presencedecember  february0.133 ( 28.4%)0.336 ( 71.6%)0.469december  april0.312 ( 55.9%)0.248 ( 44.3%)0.56february  april0.466 ( 96.5%)0.017 ( 3.5%)0.483 results from decomposition of dung beetle -diversity in the beginning , middle and end of wet season ( december 2009 , february , and april 2010 ) in a tdf at the mata seca state park , minas gerais , brazil
dung beetle communities changed dramatically throughout the wet season , and the importance of nestedness and species turnover varies between pairs of sample periods as the main process of temporal -diversity .
individuals sampled at the beginning of the wet season accounted for nearly 85% of the total number collected .
species richness showed a similar pattern ; out of 39 species , > 90% were sampled in the beginning of the wet season .
andersen ( 2005 ) found similar results for dung beetle abundance in a tdf in mexico , with more than twice as many individuals found at the beginning of the wet season compared with the middle .
of the 34 species sampled at the beginning of the wet season , 32 either had reduced abundances or were not sampled in later periods .
these results indicate a peak adult emergence of the vast majority of species at the beginning of the wet season .
hence our study contradicts the hypothesis raised by andersen ( 2008 ) , which suggests that the dung beetles are likely to experience drastic fluctuations in abundance , with different peaks during different periods .
lack of rainfall , high solar radiation , and low humidity are typical of tdfs for at least 3 months during the dry season ( murphy and lugo 1986 ) .
these conditions affect the availability of resources and limit reproduction and survival of many animals , including dung beetles , which synchronize their life cycle to tolerate these adversities ( andersen 2005 , neves et al .
for example , the guinean savannas in africa have two wet seasons , so dung beetles have two peaks in emergence during the year ( cambefort 2014a ) .
many species weather unfavorable environmental conditions ( i.e. , during droughts ) in diapause ( hibernation ) or in larval stages in the soil ( doube 2014 ) .
the adults emerge with the onset of the rains , and immediately concentrate efforts on accumulation of resources for making nests , reproduction , and subsequent oviposition ( cambefort 2014a ) .
we found the greatest within - plot -diversity in the middle and end of the wet season . in the middle and end of the wet season
only 1347% of the collected species were present in individual plots , compared with 4774% of species per plot at the beginning of the wet season . with the emergence of most species of dung beetles due to improved abiotic conditions and the increased availability of resources
the community becomes more homogeneous at the beginning of the wet season . as the season advances , higher resource scarcity limits population size , which likely results in a smaller foraging range , increasing -diversity .
decomposition of -diversity demonstrated that the dung beetle community sampled in the middle of the wet season is indeed a subset of the species present at the beginning of the wet season . at the end of wet season turnover and nestedness were equally important , due to some species that were exclusively found in this period .
these results reinforce the pattern of peak adult emergence found in most dung beetle species at the start of the wet season , since the community changes little ( i.e. , in terms of species composition ) throughout the season .
the high turnover value between the beginning and end of the wet season was due to only five species not sampled at the beginning , which only represented 8% of the total individuals at the end of the wet season .
our results demonstrate a peak in adult emergence for most dung beetle species at the beginning of the wet season .
additionally , most species present in the middle and end of the wet season were also sampled at the beginning , whereas only a few species with few individuals were absent in the beginning .
these results suggest strong synchronism between the life cycle of these organisms and the seasonality of environmental conditions throughout the year , where the onset of the rains determines adult emergence in most species in the tdf studied .
 dung beetle community dynamics are determined by regional rainfall patterns . however , 
 little is known about the temporal dynamics of these communities in tropical dry forests ( tdfs ) . 
 this study was designed to test the following predictions : 1 ) peak diversity of dung beetle species occurs early in the wet season , with a decrease in diversity (  and  ) and abundance throughout the season ; 2 ) nestedness is the primary process determining -diversity , with species sampled in the middle and the end of the wet season representing subsets of the early wet season community . 
 dung beetles were collected in a tdf in the northern minas gerais state , brazil over three sampling events ( december 2009 , february and april 2010 ) . 
 we sampled 2,018 dung beetles belonging to 39 species and distributed among 15 genera . 
 scarabaeinae -diversity and abundance were highest in december and equivalent between february and april , while -diversity among plots increased along the wet season . 
 the importance of nestedness and species turnover varies between pairs of sample periods as the main process of temporal -diversity . 
 most species collected in the middle and end of the wet season were found in greater abundance in early wet season . 
 thus , the dung beetle community becomes more homogeneous at the beginning of the wet season , and as the season advances , higher resource scarcity limits population size , which likely results in a smaller foraging range , increasing -diversity . 
 our results demonstrate high synchronism between the dung beetle life cycle and seasonality of environmental conditions throughout the wet season in a tdf , where the onset of rains determines adult emergence for most species . 
Material and Methods
Study Area
Dung Beetle Sampling
Data Analysis
Results
Discussion
Conclusions