Surrogatos para Avaliacoes Taxonomicas e Funcionais de Formigas em Serrapilheira

Ecological Indicators 122 2021 107305 Available online 30 December 2020 1470160X 2020 The Authors Published by Elsevier Ltd This is an open access article under the CC BY license httpcreativecommonsorglicensesby40 Seeking surrogates for taxonomic and functional evaluations of leaflitter ant faunas Elmo BA Koch a Ivan Cardoso Nascimento b Jonathan D Majer cd Jacques HC Delabie ae a Laboratorio de Mirmecologia Comissao Executiva do Plano da Lavoura Cacaueira Ilheus Bahia Brazil b Departamento de Ciˆencias Biologicas Universidade Estadual do Sudoeste da Bahia Jequie Bahia Brazil c School of Biological Sciences University of Western Australia Perth Western Australia Australia d School of Molecular and Life Sciences Curtin University Perth Western Australia Australia e Departamento de Ciˆencias Agrarias e Ambientais Universidade Estadual de Santa Cruz Ilheus Bahia Brazil A R T I C L E I N F O Keywords Biodiversity Taxonomic sufficiency Formicidae Atlantic rainforest Functional groups Economic assessment A B S T R A C T Comprehensive biodiversity inventories are expensive and timeconsuming to achieve especially for groups of megadiverse organisms One approach to resolve such situations is to utilize biological substitutes referred to as surrogates A surrogate should provide meaningful information at a lower cost andor effort than the original level of resolution Studies have shown that species richness is often not the best or most appropriate component or predictor of biodiversity Functional diversity can be used as a measurement of the ecological differentiation between habitats or between biological functions We evaluated the use of several taxonomic metrics as potential surrogates for leaflitter ant assemblages distributed in 65 Atlantic rainforest sites Our goal was to find reliable and economic substitutes for both taxonomic and functional leaflitter ant diversity and composition We tested four potential surrogate approaches for taxonomic metrics and three for functional group metrics Additionally we also evaluated the time and costs involved We used a large leaflitter ant database that comprises 364 ant species respectively classified into 13 or 26 ant functional groups based on either a general and specific reso lution Subfamily was found to be an unacceptable surrogate for both taxonomic and functional group metrics Mixedlevel and indicator taxa metrics were rated as excellent taxonomic surrogates Mixedlevel and genus metrics were rated as excellent or acceptable functional group surrogates when considering the most general functional resolution while mixedlevel and genus were considered as excellent surrogates when considering the more specific resolution The monetary and time costs to identify ants to genus level were lower than those using indicator taxa and mixedlevel metrics The use of a certain higher taxon functional and taxonomic sur rogates allows a reduction of survey and analysis costs while still enabling the analysis of biological diversity from the taxonomic and functional point of view 1 Introduction Exploring patterns of diversity have been one of the main challenges in community ecology Pianka 1966 Hawkins 2001 Agrawal et al 2007 while conserving diversity is the main goal of conservation biology Myers et al 2000 Wallington et al 2005 Moore et al 2009 However comprehensive biodiversity inventories are expensive time consuming and almost impossible to conclude satisfactorily Whit taker et al 2005 This is particularly so for groups of megadiverse organisms and those for which taxonomic knowledge is still lacking The choice of biological groups used in diversity studies and environmental assessments has particularly been influenced by taxonomic impediments and by the diminishing number of salaried taxonomists who are able to describe and assist in identification of species Basset et al 2004 For terrestrial invertebrates this deficiency has been a factor that has hin dered the inclusion of these groups in conservation and bioindication research Kallimanis et al 2012 Because of this there has been an increasing interest in finding more rapid and efficient biodiversity monitoring techniques Groc et al 2010 Mandelik et al 2010 Kessler et al 2011 One approach that is increasingly being used to circumvent this problem is the use of biological substitutes or surrogates of biological diversity A surrogate can be a subset of species that is indicative of the presence of all species Gaston 1996 It can be a higher taxonomic Corresponding author at Laboratory of Myrmecology CEPECCEPLAC Km 22 highway IlheusItabuna BR415 Ilheus Bahia Brazil Email address elmoborgesgmailcom EBA Koch Contents lists available at ScienceDirect Ecological Indicators journal homepage wwwelseviercomlocateecolind httpsdoiorg101016jecolind2020107305 Received 7 July 2020 Received in revised form 12 December 2020 Accepted 21 December 2020 Ecological Indicators 122 2021 107305 2 level such as family or genus Ellis 1985 Williams and Gaston 1994 de Oliveira et al 2020 the use of morphospecies as an alternative to the use of species to describe community structure Oliver and Beattie 1996a 1996b Pik et al 1999 or groups of species that are capable of representing responses to environmental conditions by other taxa Sar kar and Margules 2002 Landeiro et al 2012 The ideal surrogate should provide meaningful information about the environment in which it occurs at a lower cost or effort than would be required to sort and identify fauna at the species level Ellis 1985 ideally it should also require less taxonomic expertise Morrison et al 2012 Obtaining a good surrogate allows practitioners to analyze biological diversity while at the same time minimizing the costs and time associated with accurate taxonomic analysis Grimbacher et al 2008 According to Williams and Gaston 1994 achieving this taxonomic independence could contribute to reducing the large load of identification by taxonomists thus allowing more investment in systematic studies and the allocation of more resources for temporal or spatial replications of studies Grim bacher et al 2008 Species taxonomic units or groups of species that can be used to measure some characteristic of the environment are regarded as bio logical indicators generally referred to as bioindicators McGeogh 1998 These taxa can act as a bioindicator when respondingrepre senting the biotic or abiotic state of an environment andor they can indicate the diversity of a set of species or a biological group As such they can represent the impact of environmental conditions or pollution in a habitat McGeoch 2007 Among terrestrial invertebrates ants Formicidae are a globally dominant group that are frequently used in environmental monitoring and evaluation studies Andersen and Majer 2004 Underwood and Fisher 2006 Delabie et al 2009 Guzman Mendoza et al 2016 This is mainly due to their ecological dominance Holldobler and Wilson 1990 their intimate relationship with the environment Kaspari and Majer 2000 their influence on the diversity of other groups Izzo and Vasconcelos 2005 Philpott and Armbrecht 2006 their predictable response to environmental disturbances Andersen and Majer 2004 Agosti and Alonso 2000 Delabie et al 2009 Andersen 2019 their role in important ecological functions Folgarait 1998 Hoffmann and Andersen 2003 Crist 2009 Bihn et al 2010 and the fact that this diverse group can be easily sampled by methods that are easy to reproduce Folgarait 1998 Delabie et al 2021 In recent years a considerable and growing number of studies have investigated suitable surrogates for the richness and composition of ant assemblages Andersen 1995 Leal et al 2010 Groc et al 2010 Gutierrez et al 2017 Souza et al 2016 Initially these studies focused on the use of higher taxonomic levels such as subfamily and genus see Andersen 1995 Andersen et al 2002 levels that are generally well defined and which can be identified through widely available identifi cation keys Some studies have also shown that the use of morphospe cies which can be identified in less time and with minimal training in taxonomy Oliver and Beattie 1993 1997 Beattie and Oliver 1994 is an adequate substitute for specieslevel identifications Oliver and Beattie 1996a 1996b Pik et al 1999 Recently other metrics that allow nonspecialists in the taxonomic groups concerned to incorporate these organisms in their own studies Souza et al 2016 have been developed These include the use of indicator taxa species from genera that meet certain preestablished criteria generally that are widespread diverse and identifiable and are considered representative of the entire assemblage details in Lawton et al 1998 McGeogh 1998 Linden mayer and Likens 2011 as well as the use of mixedlevel surrogates a nonhierarchical metric that considers the most specific level of identi fication possible for species of indicator genera with the rest of the ant assemblage of the genera that do not meet the indicator taxa criteria only being considered up to the level of genus details in Groc et al 2010 However all these studies have as a common objective of eval uating possible surrogates of ant taxonomic metrics ignoring the func tional approach Studies have shown that species richness is often not the best or most appropriate component or predictor of biodiversity Cadotte et al 2011 HainesYoung 2013 since the loss of species or changes in the composition does not necessarily result in the loss of ecosystem func tions and processes Hooper et al 2005 Nowadays fewer studies assess the role of species richness alone Dalerum et al 2012 and increasingly functional aspects are incorporated in order to complement the traditional taxonomic indicators Moretti et al 2009 Gerisch et al 2012 Functional diversity is considered to be one of the fundamental components of biological diversity Tilman 2001 and can be used as a measurement of the ecological differentiation between habits or be tween biological functions De Bello et al 2010 Thompson et al 2010 As a tool functional diversity evaluates the various ways in which organisms respond to environmental variability Gerisch et al 2012 and may reflect relevant components associated with patterns in the community De Bello et al 2010 Functional diversity is generally measured to determine how different species affect the functioning of the ecosystem through the time and space Petchey and Gaston 2006 Using species characteristics it is possible to infer about the functional role of these species in the community Díaz et al 2013 These char acteristics functional attributestraits can be classified as a response when they respond to certain environmental changes or they can be classified as an effect when they are related to ecosystem characteristics Chapin et al 2000 Lavorel and Garnier 2002 Díaz et al 2013 Traits at the individual level are generally used to evaluate effect while morphological or behavioral traits in response to abiotic or biotic factors are more used to assess response Chapin et al 2000 Lavorel and Garnier 2002 The use of these functional attributes allows practi tioners to evaluate fundamental dimensions of biodiversity in a simpli fied comprehensive and usefully predictive way Podgaiski et al 2011 Studies have shown a clear association between morphology ecol ogy and taxonomy Price 1991 Douglas and Matthews 1992 Silva and Brandao 2010 The morphology of an organism can reflect its habitat and its function within an environment Sosiak and Barden 2020 The use of functional groups reveals sets of sympatric species occupying niches or similar ecological roles these being organisms that influence the environment together and in a similar way Wilson 1999 Philpott et al 2009 Over the years researchers on ants from the Neotropical region have proposed classifications of functional groups that consider morphology trophic characteristics microhabitat distribution vertical stratification of fauna biology and life styles Delabie et al 2000 Silva and Brandao 2010 Brandao et al 2012 Koch et al 2019 The use of such schemes simplifies the ecological complexity of the situation and allows comparative analyses Philpott et al 2009 In this study we evaluated and compared the use and performance of different metrics as potential surrogates of leaflitter ant diversity in the Atlantic rainforest throughout the Brazilian state of Bahia We tested four potential surrogates for ant assemblages by considering the composition and number of species as well as the composition and number of functional groups of ants at two functional group FG reso lutions Our goal was to find a reliable economic and effective substitute for the direct measurement of taxonomic and functional leaflitter ant diversities We hypothesized that i at the species level the best sub stitute may be genus ii at the FG level the best substitute may be a mixedlevel and iii genus will be the best substitute when considering time and monetary savings These results were expected since previous studies have shown that genus is an excellent substitute for species level determinations in different environments Pik et al 1999 Heino and Soininen 2007 Gallego et al 2012 Souza et al 2016 Gutierrez et al 2017 de Oliveira et al 2020 By contrast we expected that functional diversity could provide a different outcome than for taxonomic di versity since studies have shown a positive linear relationship between taxonomic and functional diversity Bihn et al 2010 RochaOrtega et al 2018 In addition the functional role of some of the species within any given genus may differ in their role within the ecosystem EBA Koch et al Ecological Indicators 122 2021 107305 3 Koch et al 2019 2 Materials and methods 21 Study region and ant sampling design We used the same large leaflitter ant database that was used for the study of Koch et al 2019 The ants were collected in 65 Atlantic rainforest sites in the southern region of the state of Bahia Brazil Fig 1 The region covers an area of 6500 km2 130 50 km of Atlantic rainforest This formation belongs to the tropical wet forest biome and is considered one of the most threatened tropical biomes on the world being one of the Worlds major hotspots of terrestrial biodi versity Mittermeier et al 1998 Myers 1988 Myers et al 2000 For the sampling of ants an adaptation of the ALL protocol was used Agosti and Alonso 2000 One transect of approximately 2500 m was established in each site along each transect 50 sampling points at in tervals of 50 m were marked out At each point the ants living in 1 m2 of leaf litter were extracted using Winkler traps Bestelmeyer et al 2000 Delabie et al 2021 A total of 50 leaf litter samples were sampled per site The samples remained in the Winkler extractors for 48 h Then the ants were separated from the other arthropods mounted and iden tified to the most specific level possible based on the Formicidae reference collection at the Myrmecology Laboratory of the Cocoa Research Center and by consulting the relevant literature eg Bolton et al 2007 22 Taxonomic surrogate metrics To evaluate the various metrics as possible surrogates for ant spe ciesmorphospecies hereafter referred to as species we reduced the taxonomic resolution by classifying ants to i the level of subfamily ii genus and iii a selected subset of genera that could be considered as indicator taxa details in Lawton et al 1998 Lindenmayer and Likens 2011 The latter were based on the presupposition that certain genera could be good substitutes of all ant species within certain environments Andersen 1995 We considered indicator taxa to be those genera that met the following criteria namely that a the indicator must have at least one species present in a minimum of 50 of 65 sampling sites b it must have at least seven species in all site data grouped and c it must be taxonomically well defined Of the 68 genera obtained in the data base those that meet the established criteria were Apterostigma Bra chymyrmex Cyphomyrmex Gnamptogenys Hypoponera Megalomyrmex Neoponera Nylanderia Pheidole Rogeria Solenopsis and Strumigenys see Table S1 in Supporting information Finally iv we tested the mixed level metric proposed by Groc et al 2010 This combines two different levels of identification with part of the assemblage identified to species level ie all members of the 12 indicator genera and the remaining part identified to genus level 23 Functional surrogates Ant functional group resolutions Except for the subfamily level the same potential surrogate levels were also tested as predictors of the number of FGs found per site We did not consider the subfamily level because the variation in ecological functions amongst taxa is too varied within a subfamily For functional surrogates the analyses were performed using two different FG resolu tions one more general and one more specific details below Because patterns between richness and number of FGs of leaflitter ants may vary according to the FG resolution used Koch et al 2019 we used two resolutions of ant FGs in this study the first being FCA in which we classified the ants according the commonly used scheme for Neotropical ants Delabie et al 2000 Silvestre et al 2003 Silva and Brandao 2010 Brandao et al 2012 Silva et al 2015 This approach groups ant species into up to 13 different functional groups considering trophic characteristics microhabitat distribution eye size body size and shape grouping of species according their potentially similar biology and life styles The second was FCB which in addition to the information from the previous classification also incorporated more detailed aspects of the ants biology such as natural history information Koch et al 2019 This classification groups ant species into up to 24 different functional groups Details of functional groups such as description and their functional significance are provided in Table S1 24 Assessment of time and money costs Although the sampling of ants is relatively easy to carry out the costs and time spent are a necessary consideration eg Majer et al 2007 Souza et al 2012 We therefore assessed the time and money costs involved in the four surrogate metrics These assessments were per formed according to Souza et al 2016 by which we calculated the time taken and monetary costs associated with each surrogate Costs were based on basic staff charges materials and ant sampling costs According to Gardner et al 2008 costs of accommodation buildings and laboratory equipment and for the field team are fixed costs for all procedures so we did not consider them All costs were estimated for each site with the rates being based on current 2020 Brazilian Federal Government costing tables available at httpswwwbcbgovbr estabilidadefinanceirahistoricocotacoes First we consider costs considering the value of the currency during the time that the material was processed and corrected for current inflation We converted the Brazilian currency Real R to US dollars using the conversion rate 1 US R 406 daily averages between the months of March 2019 to Fig 1 Positions of the 65 Atlantic rainforest ant sample sites in the state of Bahia Brazil EBA Koch et al Ecological Indicators 122 2021 107305 4 February 2020 source Brazilian Central Bank httpswwwbcbgov br For each forest site we calculated the time and monetary costs to obtain the number of registered species ie processing and identifica tion Then to obtain the value for each potential surrogate we divided the total money and time spent by the number of units of surrogate resolutions in a given site 25 Statistical analysis The surrogate was considered to be excellent if it predicted based on r or r2 values obtained 80 of variation found in the actual species level data good if it predicted 70 and 80 of variation acceptable if it predicted 60 and 70 of variation and not acceptable if it predicted 60 of variation These values were origi nally proposed by Leal et al 2010 for predictions of taxonomic di versity by substitutes although we adapted its use for our study and expanded it to functional diversity of ants 251 Surrogates for assemblage composition and functional group composition For each site and considering all 50 points a fullyresolved taxo nomic spreadsheet based on ant species and morphospecies was used to produce taxonomic spreadsheet at two levels genus and subfamily Additionally as already detailed we also organized the spreadsheet to consider the indicator taxa and mixedlevel resolutions Thus five pages of spreadsheets were constructed for each site Then we calculate a distance matrix for each different spreadsheet We used the Jaccard index Rohlf 1989 one of the similarity indices most used to assess the compositional similarity of species assemblages Manthey and Fridley 2009 We focused on beta diversity in this study Samplebytaxon matrices are recommended to compare measures of beta diversity among groups of samples Groc et al 2010 Beta di versity is often measured using indices of species overlapping between pairs of samples We used the Mantel test Mantel 1967 to correlate the speciesdistance matrix with that of each different surrogate evaluated subfamily genera indicator taxa and mixedlevel values considering each site The Mantel test calculates the similarity between two given distance matrices here using the Pearson correlation method The sta tistical significance of the Mantel tests was calculated using 5000 per mutations Subsequently we evaluated whether there is a difference in how much each matrix of the different surrogate taxa predicted the species matrix represented by Pearsons correlation coefficients using an analysis of variance ANOVA with repeated measures followed by the Tukey multiplerange test In this analysis the dependent variable was the Mantel correlation coefficient value and the independent vari able was the surrogate resolution type considering the site as a random factor We used repeated measures ANOVA to consider any possible residual autocorrelation within the sites The same analyses were performed considering the composition of functional groups We subsequently tested how much each matrix of the different metrics predicted the FG matrix using a twoway repeated measures ANOVA In this analysis the dependent variable was the Mantel correlation coefficient value and the independent variables were the surrogate resolution type and FG scheme considering the site as a random factor 252 Surrogates for species richness and functional group richness In order to evaluate whether the number of surrogate taxa is a good predictor of species richness we compared the number of ant species per site with the number of the surrogate taxa considering the different surrogate levels number of subfamilies genera indicator taxa and mixedlevel values per site using a series of linear regressions sepa rately for each possible surrogate level Additionally we compared the number of ant FGs with the number of the surrogate taxa considering the different surrogate levels genera indicator taxa and mixedlevel values also using linear regressions separately for each possible surrogate level For these analyses we considered each of the 65 forests sampled sites as the units of analysis 253 Assessment of time and monetary costs We evaluated differences in the relative costs and time taken to obtain the final product according to the metric used considering that species level classification would be 100 To assess whether there is a difference in financial costs according to the levels of surrogates tested we used a repeated measures ANOVA followed by the Tukey multiple range test In this analysis the dependent variable was the financial cost to reach the taxonomic units evaluated for each site and the indepen dent variable was the surrogate resolution type considering the site as a random factor All analyses were performed using the software R v 361 R Development Core Team 2019 All assumptions of the tests per formed were tested and obeyed The packages ggplot2 Wickham 2016 and vegan Oksanen et al 2018 were used Finally we produced a table with a summary of the degree of per formance of the various surrogates evaluated For this we considered the prediction values already explained at the beginning of the data anal ysis section and costs We created an index ranging from 1 to 4 with 1 being the most desirable outcome and 4 the least We assigned the values 1 when the surrogate assessed was considered excellent or the best for a given metric tested 2 when it was considered the second best or most suitable and so on 3 Results The database in Table S1 comprises 10 ant subfamilies representing 68 genera and 364 species These were classified into 13 FGs under the FCA scheme and 26 FGs under FCB The number of taxonomic units identified as indicator taxa and as mixedlevel taxa ie the species of the 12 indicator genera plus the 56 remaining genera no indicator taxa was 195 and 251 respectively Table S2 31 Taxonomic diversity 311 Surrogates for assemblage composition The values of correlations between the species composition matrices and the surrogate composition matrices and pvalues for each of the 65 sites are shown in Table S3 All individual correlation coefficients were significant We found significant differences in the Mantel correlation co efficients between the surrogates that we evaluated F3192 1144 P 0001 Fig 2 with pairwise tests revealing significant differences be tween the surrogate resolutions Tukey P 0001 The highest Mantel correlations between assemblage composition with surrogate values were for mixedlevel taxa mean standard deviation 0939 SD 0034 followed by indicator taxa 0842 0067 both of which were therefore considered as excellent surrogates for ant assemblage composition The mean value for genus was lower 0648 0076 but still considered to be an acceptable surrogate for assemblage composi tion The lowest correlations were observed for subfamily 0329 0101 which did not reach the minimum value to be considered acceptable as an adequate predictor of assemblage composition For all comparisons the coefficients obtained for the subfamily level were lower than those obtained for genus Table S3 We observed nine in dividual cases where genus was better than indicator taxa Table S3 Only in two of the 65 Mantel correlations were the individual co efficients observed for genus higher than for indicator taxa but always smaller than for mixedlevel Only three Mantels correlation co efficients for indicator taxa were higher than those observed for the mixedlevel taxa Table S3 312 Surrogates for species richness The relationships between the number of taxa considering each of the four different surrogate levels and ant species richness are shown EBA Koch et al Ecological Indicators 122 2021 107305 5 graphically in Fig 3 The r2 values ranged from 0105 to 0973 The subfamily y 0019x 5702 r2 00105 P 0008 Fig 3a and genus y 01733x 19031 r2 0495 P 0001 Fig 3b metrics were considered to be not acceptable surrogates for species richness using the 60 cutoff mentioned in the methods The indicator taxa y 0632x 2931 r2 0908 P 0001 Fig 3c and mixedlevel y 0789x 5831 r2 0973 P 0001 Fig 3d metrics were rated as excellent surrogates 32 Functional group surrogates 321 Surrogates for functional group composition The values of Mantel correlation coefficients for each of the 65 sites for comparisons between matrices of functional ant composition with the various surrogate schemes are shown in Table S4 All but one of the individual correlation coefficients were significant P 005 We observed significant differences in the Mantel correlation Fig 2 Correlations between dissimilarity in species composition matrices and the dissimilarity in surrogate composition matrices means SD using the four surrogates The different letters above the SD bars indicate that all means are significantly different values are given in Table S3 Fig 3 Relationships between the number of ant species and the number of taxa for the four taxonomic surrogates at the 65 study sites a subfamily b genus c indicator taxa and d mixedlevel Fig 4 Correlations between dissimilarity in species composition matrices and the dissimilarity in surrogate composition matrices means SD using three surrogates of functional diversity comparing a more general resolution FCA and a more specific resolution FCB The different letters above the SD bars represent significant differences between surrogate whose values are available in Table S4 significance between the classifications used EBA Koch et al Ecological Indicators 122 2021 107305 6 coefficients for FGs versus the various surrogates F2128 5888 P 0001 Fig 4 In the pairwise Tukeys test we observed that indicator taxa showed lower average correlation coefficients when compared to genus and mixedlevel Tukey P 0001 Overall we found a signifi cant difference between the type of FG resolution used F1192 15 32 P 0001 However we also found a significant interaction between surrogate type and the FG resolution level used F2192 1398 P 0001 This was because this difference was dependent on surrogate used being significant only for indicator taxa F1129 3019 P 0003 Fig 4 The highest correlations with FGlevel resolutions were for genus mean 1000 SD 0000 for FCA and 1000 0000 for FC B followed by the mixedlevel approach 0988 0008 to FCA 0990 0007 to FCB these were both rated as excellent surrogates for FGs The corresponding correlation for indicator taxa 0684 0147 to FCA 0745 0064 to FCB indicated that this was considered as an acceptable surrogate for FG composition using FCA and good using FC B When considering the individual FGsurrogate Mantel correlations for individual sites Table S4 virtually all values were significant only in one case was the Mantel coefficient not significant site 11 for FCA and in five cases the values found for FCA were greater than FCB For mixedlevel only seven of the 65 Mantel coefficients for FCA presented higher values than FCB and in three cases the values found were the same For all comparisons the coefficients obtained for genus presented values were equal to 1000 and were higher than those obtained for the mixedlevel surrogate In one case there was no difference between genus and mixedlevel surrogates Table S4 322 Surrogates for functional group richness With the exception of the indicator taxa the other surrogates were able to predict the richness of ant FGs with the r2 ranging from 0608 to 0911 Fig 5 All r2 values were higher for FCB comparisons than for FCA We detected the lowest r2 values for the indicator taxa r2 0159 P 0001 for FCA and r2 0313 P 0001 for FCB Fig 5c and d respectively indicating that this was not an acceptable surrogate for either FG resolution Genus was rated as an acceptable surrogate when considering FCA y 0684x 2007 r2 0608 P 0001 Fig 5a Mixedlevel was rated as good surrogate when considering FCA y 0761x 1969 r2 0748 P 0001 Fig 5e Mixedlevel and genus were rated as excellent surrogates when considering FCB y 091x 1573 r2 0911 P 0001 and y 0827x 2078 r2 0818 P 0001 Fig 5f and b respectively 33 Assessment of time and monetary costs We found significant differences in the financial cost between the Fig 5 Relationship between the number of ant functional groups and the number of functional units for three levels of surrogates at the 65 study sites a genus c indicator taxa and e mixedlevel all using a more general resolution FCA b genus d indicator taxa and f mixedlevel all using a more specific resolution FCB EBA Koch et al Ecological Indicators 122 2021 107305 7 surrogates that we evaluated F4256 4471 P 0001 Fig 6 with pairwise tests revealing significant differences between the surrogate resolutions Tukey P 0001 The surrogate that required the most effort was mixedlevel accounting for an average 84 of the cost for specieslevel determinations The genus and indicator taxa metrics required averages of 42 and 65 and of the total costs respec tively As expected identifying ants only down to the subfamily level is the cheapest reducing total costs down to 25 of that of species determination Regarding the time to obtain the final product the pattern was similar to the monetary cost with relative values being mixedlevel determination reduced to 85 followed by indicator taxa 65 genus 43 and subfamily 20 Tables S5 and S6 34 Synthesis of results In summary our results indicate that the mixedlevel and indicator taxa presented the highest predictive values for both species richness and composition and were considered to be excellent indicators The genus predicted species composition at an acceptable level Subfamily was not considered to be an acceptable indicator of species richness or composition and nor was genus for species richness By contrast mixed level and genus surrogates were excellent indicators of FG composition and richness although the less sensitive FCA fared worse but never theless acceptably indicator taxa were acceptable indicators of FG composition but not of richness The trends in monetary and time costs were essentially the opposite to the trends in indicator values Table 1 If cost is not a factor mixedlevel surrogates perform the best overall while indicator taxa perform second best for species richnesscomposi tion and genus performs best for FG Surrogate relationships with the two sensitivity levels of FG did not differ appreciably although FCB tended to have a stronger correlation with surrogates than did FCA Table 1 4 Discussion The evaluation of species richness and composition patterns using surrogates has received increasing attention during terrestrial biodiversity investigations of various groups eg Baldi 2003 Cole optera Diptera and Acari Cardoso et al 2004 Araneae Souza et al 2016 Formicidae The use of a more accurate surrogates for inverte brate species represents a potentially significant advantage in the light of limited human and financial resources Williams and Gaston 1994 Oliver and Beattie 1996a Grimbacher et al 2008 allowing non specialists in the taxonomic groups concerned to incorporate these or ganisms in their own studies Souza et al 2016 However together with the increase in the number of studies investigating the use of sur rogates in recent decades Andersen 1995 Oliver and Beattie 1996b Pik et al 1999 Vasconcelos et al 2014 Souza et al 2016 2018 Gutierrez et al 2017 an increase in studies with varied and inconsis tent results has also become evident Lawler and White 2008 Neeson et al 2013 Oliveira and Tidon 2013 According to Andersen 1995 such idiosyncrasies in the results may be due to variation in the number of species within the genera being considered Other the factors that might influence the results include the type of study area Hess et al 2006 Stork et al 2014 Heino 2014 sample scale Sauberer et al 2004 sampling effort Vasconcelos et al 2014 and taxonomic group concerned Leal et al 2010 Landeiro et al 2012 Filgueiras et al 2019 Vasconcelos et al 2019 Nevertheless a recent cumulative meta analysis review of higher taxon surrogate approaches from 2007 to 2017 demonstrated consistent success in using higher taxa as surrogates over the period of the review de Oliveira et al 2020 41 Taxonomic surrogates As with some of the abovementioned studies our results do not always agree with previous investigations into ant surrogates Earlier studies have sought to evaluate whether the genus level is a good sur rogate for ant species Andersen 1995 Oliver and Beattie 1996b More recent studies that have demonstrated that genus is an effective surro gate for detecting patterns with specieslevel data include Pik et al 1999 Heino and Soininen 2007 Gallego et al 2012 Souza et al 2016 Souza et al 2018 and Gutierrez et al 2017 However unlike in the current investigation some of these studies did not compare the performance of genus against other possible surrogates One exception is the study of Souza et al 2016 which demonstrated that the genus level was the best substitute for ant richness On the contrary our findings suggest that at although genus surrogates have some value mainly due Fig 6 Relationship between the monetary costs and the different metrics used in the study The different letters above the SD bars indicate that all means are significantly different values are given in Table S6 Table 1 Summary of degree of performance of the various surrogates with 1 being the most desirable outcome and 4 the least Performance level Subfamily Genus Indicator taxa Mixed level Correlation with species composition 4 3 2 1 not acceptable acceptable excellent excellent Correlation with ant species richness 4 3 2 1 not acceptable not acceptable excellent excellent Correlation with FG composition 1 3 2 not testable both FCs excellent FCB acceptable FCA good both FCs excellent Correlation with FG richness 2 3 1 not testable FCB excellent FC A acceptable both FCs not acceptable FCB excellent FCA good Time required 1 2 3 4 Cost involved 1 2 3 4 EBA Koch et al Ecological Indicators 122 2021 107305 8 to the reduction of effort expense and time there is a more effective surrogates available this being the mixedlevel resolution Our results agree with Groc et al 2010 whose study in French Guiana rainforest suggested that using mixedlevel and to a lesser extent indicator taxa surrogates result in a better prediction of species richness composition than does genus This outcome was different from what we originally hypothesized to be the best substitute for full species level determinations We believe that the discrepancy between our and pre vious studies results from the different patterns of litter ants of the Atlantic rainforest when compared to ants from other strata or envi ronments Previous studies showed that Neotropical leaflitter ant as semblages exhibit a relatively small number of species that are considered numerically dominant and a high number of habitatspecific species Longino et al 2002 Leponce et al 2004 Groc et al 2014 On the other hand in the Amazon although ant richness is locally high beta diversity is low and species richness tends not to be influenced by the difference between habitats Wilson 1987 Majer and Delabie 1994 Vasconcelos and Vilhena 2006 this fact is mainly attributable to the large number of Amazonian ants that are habitat generalists Wilson 1987 Majer and Delabie 1994 According to Oliveira and Tidon 2013 environmental conditions may also interfere in the development of surrogates for diversity In addition it is worth noting that even using similar scales and collection methods studies conducted in different environments may not be comparable since diversity may strongly vary for different reasons Favreau et al 2006 42 Functional surrogates Regarding functional diversity our results suggest that the indicator taxa surrogate is a poor surrogate for FG richness but marginally better for FG composition As we hypothesized the mixedlevel metric pro vides an excellent surrogate for both levels of FG sensitivity and of FCB richness and for FCA the outcome was still good Interestingly genus level was considered an excellent surrogate for FG composition at both sensitivities and an acceptable surrogate of FG richness for FCA and excellent one for FGB We believe the better performance of the genus surrogate for FG metrics than the taxonomic one is because species that are considered indicators do not exhibit great functional distinctions that is although they are representative of taxonomic diversity they are not of functional diversity This becomes evident when considering the relationship between the number of FGs in the original set of data and the indicator taxa species Fig 5C and D Studies have shown that taxonomic diversity can be a good surrogate for the functional diversity of ant assemblages Bihn et al 2010 Rocha Ortega et al 2018 This relationship is extremely important as its adoption would save time and resources needed to adequately quantify functional diversity RochaOrtega et al 2018 Although considerable variations in the number and composition of ant species between the study sites are observed details in Koch et al 2019 the composition of species and functional groups in the localities can generally be surpris ingly stable that is the same genera and most functional groups are found in the different locations studied this represents a considerable ecological redundancy and is evidenced mainly when we disregard rare species and consider FCA However when we consider FCB which seeks to use more specific information about all species we observe that although there is a substitution between species in the same genus they can represent other functional groups resulting in the composition of the genera being stable in different places while the composition of functional groups is highly variable a scenario of ecological complementarity Ants participate significantly in ecosystem structuring Holldobler and Wilson 1990 Hoffmann and Andersen 2003 Crist 2009 Bihn et al 2010 such as in seed dispersal Christianini and Oliveira 2009 Lengyel et al 2009 in regulating the populations of several other groups Izzo and Vasconcelos 2005 Philpott and Armbrecht 2006 and in promoting changes in the physical structure of the environment Folgarait 1998 Frouz and Jilkova 2008 Functional groups classify species on the basis of convergent morphological and life history char acteristics Brandao et al 2012 Some authors consider this a simpli fied way of inferring about functional diversity defending the use of functional traits In fact functional traits allow for quantification and greater prediction of functional diversity Tilman et al 1997 Cadotte et al 2011 However to obtain this information a longer time and the specific level of identification is required We believe that for ants the use of more specific information about the biology and natural history of genera in classifications of functional groups can allow to identify re lationships with ecological biogeographical and evolutionary processes driving community structure 43 Assessment of time and monetary costs Different studies have shown that the Formicidae is a group of great utility and importance for environmental assessment and monitoring Andersen and Majer 2004 Underwood and Fisher 2006 Delabie et al 2009 GuzmanMendoza et al 2016 Generally the obtaining of these data requires more time than for vertebrates thus increasing the total costs of projects Pik et al 1999 Moreno et al 2008 The process of separation of individuals and species identification of Formicidae is far from trivial In addition the taxonomic knowledge of ecologists is rarely sufficient due to among other factors inexperience in taxonomy diffi culty in following the taxonomic changes currently rather frequent in ant taxonomy and the large quantity of collected material Camarota and Pacheco 2015 Our suggested surrogates aim to assist in over coming these problems As demonstrated in other surrogate studies genus level is the metric with the lowest costs Souza et al 2016 2018 assuming that subfamily is removed as an option However in our study the most efficient sur rogate resolution was the mixedlevel one Clearly we have a tradeoff between reliabilityefficiency and economy since the most effective surrogate considering the different metrics and evaluated performances mixedlevel is also the one that requires the most time and monetary cost among the evaluated substitutes The economy of time and re sources generated by the use of an effective surrogate could allow a greater investment in other stages of the scientific study such as the inclusion of more sampling sites or additional replicates in sampled areas thus increasing study robustness quality to the statistical argu ments and better generalization of the results Costa and Magnusson 2010 The adoption of new approaches such as surrogates can save of time and money and does not necessarily exempt the researcher from seeking the correct identification of the study group The misidentifi cation of a taxonomic unit can generate an error cascade with impli cations not only in the understanding of biodiversity Khuroo et al 2007 but also in management and conservation outcomes Mcneely 2002 Bortolus 2008 As demonstrated in studies with different taxa the use of biodiversity substitutes such as those proposed here may provide quality information on the biotas response to management interventions in order to conserve biodiversity Lindenmayer et al 2002 Gonzalez et al 2013 Barton et al 2014 Westgate et al 2014 5 Conclusion This is the first study that compares the use of surrogates for For micidae from both the taxonomic and functional point of view In conclusion and differently from what was initially hypothesized we have demonstrated that when considering both species richness and FGs mixedlevel would be the most suitable surrogate for Atlantic rainforest ants However we observe the tradeoff between reliability efficiency and economy since the most effective surrogate was also the most expensive among those evaluated However this is still more economical in relation to time and monetary costs when compared to the speciesmorphospecies level Comprehensive and robust ant studies generally result in hundreds of species to be separated from the rest of EBA Koch et al Ecological Indicators 122 2021 107305 9 the invertebrate fauna then assembled and identified eg Souza et al 2012 Vasconcelos et al 2018 Santos et al 2017 Koch et al 2019 Our study lends support to this process by identifying suitable taxo nomic and functional surrogates that allow the analysis of biological diversity from both the taxonomic and functional point of view CRediT authorship contribution statement Elmo BA Koch Conceptualization Methodology Visualization Writing original draft Ivan Cardoso Nascimento Writing review editing Jonathan D Majer Writing review editing Jacques HC Delabie Writing review editing Project administration Resources Supervision Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper Acknowledgements We thank all the anonymous reviewers who helped improve this manuscript We wish to thank Jose RM dos Santos and Jose CS do Carmo in memoriam technicians from CEPLAC who were responsible for field data collection We are also grateful to the following funding agencies Coordenaçao de Aperfeiçoamento de Pessoal de Nível Superior Brazil CAPES and Fundaçao de Amparo a Pesquisa do Estado da Bahia FAPESB JHCD thanks the Conselho Nacional de Desenvolvi mento Científico e Tecnologico CNPq for his research grant Appendix A Supplementary data Supplementary data to this article can be found online at httpsdoi 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