Abstract
Landscape changes in tropical environments result in long-lasting and complex changes in biodiversity that involve several biological responses (e.g., loss of species diversity and functional diversity). Both taxonomic and functional diversity might respond differently to land-use change, and this response might also vary depending on several factors, such as the taxonomic group or landscape context. Even though each level of diversity expresses different properties of the community structure, studies characterizing the species community in human-dominated landscapes have often only focused on patterns involving taxonomic diversity. Here, we evaluated different descriptors of taxonomic (i.e., richness, diversity, and dominance) and functional entropy (i.e., richness, diversity, and redundancy) and the taxonomic and functional composition of ants in a forest cover gradient (%) in 16 highly fragmented tropical humid forest landscapes in Mexico. We found that all descriptors of taxonomic diversity decreased along a gradient of forest loss. Furthermore, functional redundancy was the only component of functional diversity that was positively associated with forest cover (%). These findings suggest an ecological backup of functions provided by species in landscapes with higher forest cover, protecting these landscapes against habitat disturbance or species loss. We also observed that landscapes with larger forest cover were inhabited by ant species with larger interocular distances and smaller femurs, which could allow predator ants the exploitation of ground cracks and higher mobility in leaf-litter microhabitats. Our results highlight the importance of the primary forest as a reservoir of the taxonomic and functional diversity of ants in highly fragmented tropical rainforest landscapes.
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References
Ahuatzin DA, Corro EJ, Jaimes AA, González JEV, Feitosa RM, Ribeiro MC, López-Acosta JC, Coates R, Dáttilo W (2019) Forest cover drives leaf litter ant diversity in primary rainforest remnants within human-modified tropical landscapes. Biodivers Conserv 28:1091–1107
Ahuatzin DA, González-Tokman D, Valenzuela-González JE, Escobar F, Ribeiro MC, Acosta JCL, Dáttilo W (2022) Sampling bias in multiscale ant diversity responses to landscape composition in a human-disturbed rainforest. Insectes Sociaux 69(1):47–58
Arnan X, Cerdá X, Retana J (2014) Ant functional responses along environmental gradients. J Anim Ecol 83:1398–1408
Asner GP, Anderson CB, Martin RE, Knapp DE, Tupayachi R, Sinca F, Malhi Y (2014) Landscape-scale changes in forest structure and functional traits along an Andes-to-Amazon elevation gradient. Biogeosciences 11:843–856
Bestelmeyer BT, Agosti D, Alonso LE, Brandão CRF, Brown WL Jr, Delabie JHC, Silvestre R (2000) Field techniques for the study of ground-dwelling ants: an overview, description and evaluation. In: Donat A, Majer JD, Alonso LET, Schultz TR (eds) Measuring and monitoring biological: standard methods for ground-living ants. Smithsonian Institute, Washington, pp 122–144
Biggs CR et al (2020) Does functional redundancy affect ecological stability and resilience? A review and meta-analysis. Ecosphere 11:e03184
Binh JH, Gebauer G, Brandl R (2010) Loss of functional diversity of ant assemblages in secondary tropical forests. Ecology 91:782–792
Borgelt A, New TR (2005) Pitfall trapping for ants (Hymenoptera, Formicidae) in Mesic Australia: the influence of trap diameter. J Insect Conserv 9:219–221
Botta-Dukát Z (2005) Rao’s quadratic entropy as a measure of functional diversity based on multiple traits. J Veg Sci 16:533–540
Bregman TP, Lees AC, MacGregor HE, Darski B, de Moura NG, Aleixo A, Barlow J, Tobias JA (2016) Using avian functional traits to assess the impact of land-cover change on ecosystem processes linked to resilience in tropical forests. Proc R Soc Lond 283:20161289
Bu W, Zang R, Ding Y (2014) Functional diversity increases with species diversity along successional gradient in a secondary tropical lowland rainforest. Trop Ecol 55:393–401
Cadotte MW, Carscadden K, Mirotchnick N (2011) Beyond species: functional diversity and the maintenance of ecological processes and services. J Appl Ecol 48:079–1087
Cardinale BJ, Duffy JE, Gonzalez A, Hooper DU, Perrings C, Venail P, Narwani A, Mace GM, Tilman D, Wardle DA, Kinzig AP, Daily GC, Loreau M, Grace JB, Larigauderie A, Srivastava DS, Naeem S (2012) Biodiversity loss and its impact on humanity. Nature 486:59–67
Carmona CP, de Bello F, Mason NW, Lepš J (2016) Traits without borders: integrating functional diversity across scales. Trends Ecol Evol 31:382–394
Carmona CP, de Bello F, Mason NW, Lepš J (2019) Trait probability density (TPD): measuring functional diversity across scales based on TPD with R. Ecology 100:e02876
Chao A, Jost L (2012) Coverage-based rarefaction and extrapolation: standardizing samples by completeness rather than size. Ecology 93:2533–2547
Chao A, Gotelli NJ, Hsieh TC, Sander EL, Ma KH, Colwell RK, Ellison AM (2014) Rarefaction and extrapolation with Hill numbers: a framework for sampling and estimation in species diversity studies. Ecol Monogr 84:45–67
Christianson DS, Kaufman CG (2016) Effects of sample design and landscape features on a measure of environmental heterogeneity. Methods Ecol Evol 7:770–782
Corro EJ, Ahuatzin DA, Aguirre A, Favila ME, Ribeiro MC, López-Acosta JC, Dáttilo W (2019) Forest cover and landscape heterogeneity shape ant–plant co-occurrence networks in human-dominated tropical rainforests. Landsc Ecol 34:93–104
Dáttilo W, Dyer L (2014) Canopy openness enhances diversity of ant–plant interactions in the Brazilian Amazon rain forest. Biotropica 46:712–719
Dáttilo W et al (2020) MEXICO ANTS: incidence and abundance along the Nearctic-Neotropical interface. Ecology. https://doi.org/10.1002/ecy.2944
Dauber J, Hirsch M, Simmering D, Waldhardt R, Otte A, Wolters V (2003) Landscape structure as an indicator of biodiversity: matrix effects on species richness. Agric Ecosyst Environ 98:321–329
Davidson DW, Cook SC, Snelling RR (2004) Liquid-feeding performances of ants (Formicidae): ecological and evolutionary implications. Oecologia 139:255–266
De la Mora A, Murnen CJ, Philpott SM (2013) Local and landscape drivers of biodiversity of four groups of ants in coffee landscapes. Biodivers Conserv 22:871–888
Debuse VJ, King J, House AP (2007) Effect of fragmentation, habitat loss and within-patch habitat characteristics on ant assemblages in semi-arid woodlands of eastern Australia. Landsc Ecol 22:731–745
Fernandes TT, Dáttilo W, Silva RR, Luna P, Oliveira CM, Morini MSDC (2019) Ant occupation of twigs in the leaf litter of the Atlantic Forest: influence of the environment and external twig structure. Tropical Conserv Sci 12:1940082919852943
Di Giulio M, Edwards PJ, Meister E (2001) Enhancing insect diversity in agricultural grasslands: the roles of management and landscape structure. J Appl Ecol 38:310–319
Edie SM, Jablonski D, Valentine JW (2018) Contrasting responses of functional diversity to major losses in taxonomic diversity. Proc Natl Acad Sci USA 115:732–737
Eisner T (1957) A comparative morphological study of the proventriculus of ants (Hymenoptera: Formicidae). Bull Mus Comp Zool 116:441–490
Escobar F, Halffter G, Solís Á, Halffter V, Navarrete D (2008) Temporal shifts in dung beetle community structure within a protected area of tropical wet forest: a 35-year study and its implications for long-term conservation. J Appl Ecol 45:1584–1592
Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol Syst 34:487–515
Fahrig L (2017) Ecological responses to habitat fragmentation per se. Annu Rev Ecol Evol Syst 48:1–23
Fahrig L, Baudry J, Brotons L, Burel FG, Crist TO, Fuller RJ, Sirami C, Siriwardena GM, Martin JL (2011) Functional landscape heterogeneity and animal biodiversity in agricultural landscapes. Ecol Lett 14:101–112
Falcão JC, Dáttilo W, Izzo TJ (2015) Efficiency of different planted forests in recovering biodiversity and ecological interactions in Brazilian Amazon. Forest Ecol Manag 339:105–111
Flynn DF, Gogol-Prokurat M, Nogeire T, Molinari N, Richers BT, Lin BB, DeClerck F (2009) Loss of functional diversity under land use intensification across multiple taxa. Ecol Lett 12:22–33
Fowler HG, Forti LC, Brandao CRF, Delabie JHC, Vasconcelos HL (1991) Ecologia nutricional de formigas. In: Panizzi AR, Parra JRP (eds) Ecologia nutricional de insetos. Editora Manule, Sao Paulo, Brazil, pp 131–223
García-Martínez MÁ, Escobar-Sarria F, López-Barrera F, Castaño-Meneses G, Valenzuela-González JE (2015) Value of riparian vegetation remnants for leaf-litter ants (Hymenoptera: Formicidae) in a human-dominated landscape in Central Veracruz, Mexico. Environ Entomol 44:1488–1497
García-Martínez MÁ, Valenzuela-González JE, Escobar-Sarria F, López-Barrera F, Castaño-Meneses G (2017) The surrounding landscape influences the diversity of leaf-litter ants in riparian cloud forest remnants. PLoS ONE 12:e0172464
García-Morales R, Moreno CE, Badano EI, Zuria I, Galindo-González J, Rojas-Martínez AE, Ávila-Gómez ES (2016) Deforestation impacts on bat functional diversity in tropical landscapes. PLoS ONE 11:e0166765
Gibb H, Parr CL (2013) Does structural complexity determine the morphology of assemblages? An experimental test on three continents. PLoS ONE 8:e64005
Gibson L, Lee TM, Koh LP, Brook BW, Gardner TA, Barlow J, Peres CA, Bradshaw CJA, Laurance WF, Lovejoy TE, Sodhi NS (2011) Primary forests are irreplaceable for sustaining tropical biodiversity. Nature 478:378–381
Gotelli NJ, Colwell RK (2001) Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol Lett 4:379–391
Gotelli NJ, Ellison AM, Dunn RR, Sanders NJ (2011) Counting ants (Hymenoptera: Formicidae): biodiversity sampling and statistical analysis for myrmecologists. Myrmecol News 15:13–19
Greenslade PJM (1973) Sampling ants with pitfall traps: digging-in effects. Insectes Soc 20:343–353
Guilherme DR, Souza JLP, Franklin E, Pequeno PACL, das Chagas AC, Baccaro FB (2019) Can environmental complexity predict functional trait composition of ground-dwelling ant assemblages? A test across the Amazon Basin. Acta Oecol 99:103434
Guisan A, Edwards TC Jr, Hastie T (2002) Generalized linear and generalized additive models in studies of species distributions: setting the scene. Ecol Model 157:89–100
Hahn DA, Wheeler DE (2002) Seasonal foraging activity and bait preferences of ants on Barro Colorado Island, Panama. Biotropica 34:348–356
Hamilton AJ (2005) Species diversity or biodiversity? J Environ Manag 75:89–92
Hernández-Ruedas MA, Arroyo-Rodríguez V, Morante-Filho JC, Meave JA, Martínez-Ramos M (2018) Fragmentation and matrix contrast favor understory plants through negative cascading effects on a strong competitor palm. Ecol Appl 28:1546–1553
Hevia V, Carmona CP, Azcárate FM, Torralba M, Alcorlo P, Ariño R, Lozano J, Castro-Cobo S, González JA (2016) Effects of land use on taxonomic and functional diversity: a cross-taxon analysis in a Mediterranean landscape. Oecologia 181:959–970
Hijmans RJ et al (2021) Package “raster”. R Package Version 3.4-13. https://CRAN.R-project.org/package=raster
Hooper DU et al (2005) Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol Monogr 75:3–35
Houadria M, Menzel F (2017) What determines the importance of a species for ecosystem processes? Insights from tropical ant assemblages. Oecologia 184:885–899
Hsieh T, Ma K, Chao A (2016) Package “iNEXT: iNterpolation and EXTrapolation for species diversity”. R package version 2.0. 12. http://chao.stat.nthu.edu.tw/blog/software-download
Jost L (2006) Entropy and diversity. Oikos 113:363–375
Kaspari M (1993) Body size and microclimate use in Neotropical granivorous ants. Oecologia 96:500–507
Kaspari M, Weiser MD (1999) The size–grain hypothesis and interspecific scaling in ants. Funct Ecol 13:530–538
Kelatwang S, Garzuglia M (2006) Changes in forest area in Africa 19902005. Int for Rev 8:21–30
Kuznetsova A, Brockhoff PB, Christensen RH (2017) lmerTest package: tests in linear mixed effects models. J Stat Softw 82:1–26
Leal IR, Filgueiras BK, Gomes JP, Iannuzzi L, Andersen AN (2012) Effects of habitat fragmentation on ant richness and functional composition in Brazilian Atlantic forest. Biodivers Conserv 21:1687–1701
Legendre L, Legendre P (1998) Numerical ecology, Second English. Elsevier Science BV, Amsterdam
Longino JT, Branstetter MG, Valenzuela J (2017) Ants of Los Tuxtlas biological station, Veracruz, Mexico. ADMAC. https://sites.google.com/site/admacsite/reports/2016-mexico/ants-of-los-tuxtlas. Accessed 5 Feb 2017
Lopes CT, Vasconcelos HL (2008) Evaluation of three methods for sampling ground-dwelling ants in the Brazilian Cerrado. Neotrop Entomol 37:399–405
Martello F, De Bello F, de Castro Morini MS, Silva RR, de Souza-Campana DR, Ribeiro MC, Carmona CP (2018) Homogenization and impoverishment of taxonomic and functional diversity of ants in Eucalyptus plantations. Sci Rep 8:3266
Martensen AC, Ribeiro MC, Banks-Leite C, Prado PI, Metzger JP (2012) Associations of forest cover, fragment area, and connectivity with neotropical understory bird species richness and abundance. Conserv Biol 26:1100–1111
Mason NW, Mouillot D, Lee WG, Wilson JB (2005) Functional richness, functional evenness and functional divergence: the primary components of functional diversity. Oikos 111:112–118
Mason NW, de Bello F, Mouillot D, Pavoine S, Dray S (2013) A guide for using functional diversity indices to reveal changes in assembly processes along ecological gradients. J Veg Sci 24:794–806
Mendes ES, Fonseca C, Marques SF, Maia D, Pereira MJR (2017) Bat richness and activity in heterogeneous landscapes: guild-specific and scale-dependent? Landsc Ecol 32:295–311
Mendoza E, Fay J, Dirzo R (2005) A quantitative analysis of forest fragmentation in Los Tuxtlas, southeast Mexico: patterns and implications for conservation. Rev Chil His Nat 78:451–467
Menezes ASO, Schmidt FA (2020) Mechanisms of species coexistence and functional diversity of ant assemblages in forest and pasture habitats in southwestern Brazilian Amazon. Sociobiology 67:33–40
Montine PSM, Viana NF, Almeida FS, Dáttilo W, Santanna AS, Martins L, Vargas AB (2014) Seasonality of epigaeic ant communities in a Brazilian Atlantic rainforest. Sociobiology 61(2):178–183
Naeem S, Wright JP (2003) Disentangling biodiversity effects on ecosystem functioning: deriving solutions to a seemingly insurmountable problem. Ecol Lett 6:567–579
Naeem S (2002) Ecosystem consequences of biodiversity loss: the evolution of a paradigm. Ecology 83:1537–1552
Narendra A, Alkaladi A, Raderschall CA, Robson SK, Ribi, WA (2013) Compound eye adaptations for diurnal and nocturnal lifestyle in the intertidal ant, Polyrhachis sokolova. PLoS ONE 8:e76015
Ness JH, Morin DF (2008) Forest edges and landscape history shape interactions between plants, seed-dispersing ants and seed predators. Biol Conserv 141:838–847
Nunes CA, Braga RF, Figueira JEC, Neves FDS, Fernandes GW (2016) Dung beetles along a tropical altitudinal gradient: environmental filtering on taxonomic and functional diversity. PLoS ONE 11:e0157442
Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2021) “vegan: Community Ecology Package”. R Package 2.5-7. https://CRAN.R-project.org/package=vegan
Parr CL (2008) Dominant ants can control assemblage species richness in a South African savanna. J Anim Ecol 77:1191–1198
Pavoine S, Bonsall MB (2011) Measuring biodiversity to explain community assembly: a unified approach. Biol Rev 86:792–812
Pinheiro J, Bates D, DebRoy S, Sarkar D, Heisterkamp S, Van Willigen B, Maintainer R (2021) Package ‘nlme’. Linear and nonlinear mixed effects models. R package version 3.1-152. https://cran.r-project.org/web/packages/nlme/nlme.pdf
Quétier F, Thébault A, Lavorel S (2007) Plant traits in a state and transition framework as markers of ecosystem response to land-use change. Ecol Monogr 77:33–52
R Core Team (2021) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Rabello AM, Parr CL, Queiroz AC, Braga DL, Santiago GS, Ribas CR (2021) Taxonomic and functional approaches reveal different responses of ant assemblages to land-use changes. Basic Appl Ecol 54:39–49
Reynolds C, Fletcher RJ et al (2017) Inconsistent effects of landscape heterogeneity and land-use on animal diversity in an agricultural mosaic: a multi-scale and multi-taxon investigation. Landsc Ecol 33:241–255
Sarty M, Abbott K, Lester P (2006) Habitat complexity facilitates coexistence in a tropical ant community. Oecologia 149:465–473
Schofield SF, Bishop TR, Parr CL (2016) Morphological characteristics of ant assemblages (Hymenoptera: Formicidae) differ among contrasting biomes. Myrmecol News 23:129–137
Silva RR, Brandão CRF (2014) Ecosystem-wide morphological structure of leaf-litter ant communities along a tropical latitudinal gradient. PLoS ONE 9:e93049
Silva FHO, Delabie JHC, dos Santos GB, Meurer E, Marques MI (2013) Mini-Winkler extractor and pitfall trap as complementary methods to sample Formicidae. Neotrop Entomol 42:351–358
Silva LF, Souza RM, Solar RR, de Siqueira NF (2017) Ant diversity in Brazilian tropical dry forests across multiple vegetation domains. Environ Res Lett 12:035002
Siqueira EL, Silva RR (2021) Taxonomic and morphological diversity of the ground-dwelling ant fauna in Eastern Amazonian grasslands. Acta Oecol 110:103693
Sobrinho TG, Schoereder JH, Sperber CF, Madureira MS (2003) Does fragmentation alter species composition in ant communities (Hymenoptera: Formicidae)? Sociobiology 42:329–342
Solar RR, Barlow J, Andersen AN, Schoereder JH, Berenguer E, Ferreira JN, Gardner TA (2016) Biodiversity consequences of land-use change and forest disturbance in the Amazon: a multi-scale assessment using ant communities. Biol Conserv 197:98–107
Soto M (2006) El Clima. In: Los Tuxtlas: El paisaje de la sierra. Guevara SS, Laborde DJ, Sánchez-Ríos G (eds) Instituto de Ecología, A. C. y Unión Europea, Mexico, pp 195–200
Stevens RD, Cox SB, Strauss RE, Willig MR (2003) Patterns of functional diversity across an extensive environmental gradient: vertebrate consumers, hidden treatments and latitudinal trends. Ecol Lett 6:1099–1108
Tilman D (2001) Functional diversity. Encyclopedia Biodivers 3:109–120
Tista M, Fiedler K (2011) How to evaluate and reduce sampling effort for ants. J Insect Conserv 15:547–559
VanDerWal J, Falconi L, Januchowski S, Shoo L, Storlie C (2019) Package “SDMTools”. R Package Version 1.1-221.1. https://CRAN.R-project.org/package=SDMTools
Vandewalle M, De Bello F, Berg MP, Bolger T, Doledec S, Dubs F, Feld CK, Harrington R, Lavorel S, da Silva SL, Moretti M, Niemelä J, Santos P, Sattler T, Sousa JP, Sykes MT, Vanbergen AJ, Woodcock BA (2010) Functional traits as indicators of biodiversity response to land use changes across ecosystems and organisms. Biodivers Conserv 19:2921–2947
Villéger S, Mason NW, Mouillot D (2008) New multidimensional functional diversity indices for a multifaceted framework in functional ecology. Ecology 89:2290–2301
Violle C, Navas ML, Vile D, Kazakou E, Fortunel C, Hummel I, Garnier E (2007) Let the concept of trait be functional. Oikos 116:882–892
Von Thaden JJ, Laborde J, Guevara S, Venegas-Barrera CS (2018) Forest cover change in the Los Tuxtlas Biosphere Reserve and its future: the contribution of the 1998 protected natural area decree. Land Use Policy 72:443–550
Weiher E (2011) A primer of trait and functional diversity. In: Magurran AE, McGill BJ (eds) Biological diversity: frontiers in measurement and assessment. Oxford University Press, Oxford, pp 175–193
Weiser MD, Kaspari M (2006) Ecological morphospace of New World ants. Ecol Entomol 31:131–142
Weiss KC, Ray CA (2019) Unifying functional trait approaches to understand the assemblage of ecological communities: synthesizing taxonomic divides. Ecography 42:2012–2020
Wiescher PT, Pearce-Duvet JMC, Feener DH (2012) Assembling an ant community: species functional traits reflect environmental filtering. Oecologia 160:1063–1674
Wiezik M, Svitok M, Wieziková A, Dovčiak M (2015) Identifying shifts in leaf-litter ant assemblages (Hymenoptera: Formicidae) across ecosystem boundaries using multiple sampling methods. PLoS ONE 10:e0134502
Acknowledgements
The authors thank Praxedis Sinaca Colín and Karla Selene Andalco Cid for their help during fieldwork. We recognize Erick Corro for the help with obtaining the landscape parameters and data analysis. We express our sincere thanks to Pedro Luna and Roger Guevara for their advice on data analysis and Flavio Siqueira for sharing his knowledge about ant natural history. Our sincere gratitude goes out to Rosamond Coates and the staff of the Tropical Biology Station Los Tuxtlas for their support and hospitality. We thank the staff of the IEXA Entomological Collection, Dora L. Martínez Tlapa, Gibran Renoy Pérez Toledo and Delfino Hernández Lagunes, and Tae Tanaami for the identification of the entomological material. We extend our deep gratitude to the staff of the Museu Paraense Emílio Goeldi for the support and help during an academic internship. We also thank Armando Aguirre for financing part of the fieldwork, which was previously published in another study with a different research question.
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Scholarship from CONACyT to DAA (No. 584340). MCR thanks CNPq (312045/2013-1; 402765/2021-4; 313016/2021-6, 312292/2016-3, and 442147/2020-1), FAPESP (process 2013/50421-2; 2020/1779-5; 2021/08534-0, 2021/10195-0), and CAPES (Procad project 88881.068425/2014-0) for financial support.
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Ahuatzin, D.A., González-Tokman, D., Silva, R.R. et al. Forest cover modulates diversity and morphological traits of ants in highly fragmented tropical forest landscapes. Biodivers Conserv 31, 2097–2117 (2022). https://doi.org/10.1007/s10531-022-02428-3
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DOI: https://doi.org/10.1007/s10531-022-02428-3