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Effects of habitat heterogeneity on epiedaphic Collembola (Arthropoda: Hexapoda) in a semiarid ecosystem in Northeast Brazil

ABSTRACT

The spatial distribution of abiotic resources and environmental conditions can vary at small scales within terrestrial ecosystems, influencing the composition of soil fauna. Epiedaphic springtails (Collembola) of a semiarid Caatinga ecosystem were studied to determine if factors related to vegetation structure, such as species richness, aerial biomass, litterfall, and soil characteristics (pH, granulometry and soil organic matter), influence species richness and abundance of this group. A total of 5,513 individuals were collected of 15 species distributed in 13 genera and 9 families. The most abundant species were Temeritas sp., with 2,086 (38% of the total abundance) individuals, and Neotropiella meridionalis (Arlé, 1939), with 1,911 (35% of the total abundance) individuals. None of the variables in the regression model were significantly related to Collembola species richness, but abundance was significantly related to plant species richness, aerial biomass and soil pH. Thus, even at a small spatial scale, habitat heterogeneity influences the epiedaphic Collembola in the Caatinga ecosystem, especially their abundance.

KEY WORDS:
Caatinga; diversity; soil dynamics; soil mesofauna; Neotropical Region

INTRODUCTION

Habitat spatial heterogeneity plays a key role in species diversity, allowing populations to persist through the exploitation of a variety of resources and refuges (Cam et al. 2002Cam E, Nichols JD, Hines JE, Sauer JR, Alpizar-Jara R, Flather CH (2002) Disentangling sampling and ecological explanations underlying species-area relationships. Ecology 83: 1118-1130., Tscharntke et al. 2002Tscharntke T, Stevan-Dewenter I, Kruess A, Thies C (2002) Contribution of small habitat fragments to conservation of insect communities of grassland-cropland landscapes. Ecological Applications 12: 354-363., Benton et al. 2003Benton TG, Vickery JA, Wilson JD (2003) Farmland biodiversity: is habitat heterogeneity the key? Trends in Ecology and Evolution 18: 182-188. https://doi.org/10.1016/S0169-5347(03)00011-9
https://doi.org/10.1016/S0169-5347(03)00...
, Vanbergen et al. 2007Vanbergen AJ, Watt AD, Mitchell R, Truscott AM, Palmer SCF, Ivits E, Eggleton P, Jones TH, Sousa JP (2007) Scale-specific correlations between habitat heterogeneity and soil fauna diversity along a landscape structure gradient. Oecologia 153: 713-725. https://doi.org/10.1007/s00442-007-0766-3
https://doi.org/10.1007/s00442-007-0766-...
). Although habitat heterogeneity is predictive of invertebrate population dynamics, more than 60% of the published articles on this topic focus on vertebrates, resulting in a scarcity of data on invertebrates, especially insects (Tews et al. 2004Tews J, Brose U, Grimm V, Tielborger K, Wichmann Mc, Schwager M, Jeltsch F (2004) Animal species diversity driven by habitat heterogeneity diversity: the importance of keystone structures. Journal of Biogeography 31: 79-92. https://doi.org/10.1046/j.0305-0270.2003.00994.x
https://doi.org/10.1046/j.0305-0270.2003...
, Price et al. 2011Price PW, Denno RF, Eubanks MD, Finke DL, Kaplan I (2011) Insect Ecology. Behavior, Populations and Communities. Cambridge, Cambridge University Press, 829 pp.).

In terrestrial ecosystems, studies on grasshoppers (Davidowitz and Rosenzweig 1998Davidowitz G, Rosenzweig ML (1998) The latitudinal gradient of species diversity among North American grasshoppers within a single habitat: a test of the spatial heterogeneity hypothesis. Journal of Biogeography 25: 553-560. https://doi.org/10.1046/j.1365-2699.1998.2530553.x
https://doi.org/10.1046/j.1365-2699.1998...
), beetles (Romero-Alcaraz and Ávila 2000Romero-Alcaraz E, Ávila JM (2000) Landscape heterogeneity in relation to variation in epigaeic beetle diversity of a Mediterranean ecosystem. Implications for conservation. Biodiversity and Conservation 9: 985-1005. https://doi.org/10.1023/A:1008958720008
https://doi.org/10.1023/A:1008958720008...
), flies (Tanabe et al. 2001Tanabe SI, Masanori JT, Vinokurova AV (2001) Tree shape, forest structure and diversity of drosophilid community: comparison between boreal and temperate birch forests. Ecological Research 16: 369-385. https://doi.org/10.1046/j.1440-1703.2001.00402.x.
https://doi.org/10.1046/j.1440-1703.2001...
), and birds (Poulsen 2002Poulsen BO (2002) Avian richness and abundance in temperate Danish forests: tree variables important to birds and their conservation. Biodiversity and Conservation 11: 1551-1566. https://doi.org/10.1023/A:1016839518172
https://doi.org/10.1023/A:1016839518172...
) have shown that vegetation gradients influence the assemblages of these animals by affecting the physical structure of habitats and their potential for occupation. However, the relationship between species richness and habitat heterogeneity depends on the specificity of each taxonomic group and the spatial scale at which they are studied (Tews et al. 2004Tews J, Brose U, Grimm V, Tielborger K, Wichmann Mc, Schwager M, Jeltsch F (2004) Animal species diversity driven by habitat heterogeneity diversity: the importance of keystone structures. Journal of Biogeography 31: 79-92. https://doi.org/10.1046/j.0305-0270.2003.00994.x
https://doi.org/10.1046/j.0305-0270.2003...
).

Collembola assemblages appear to be positively influenced by heterogeneity, habitat size, and resource availability (Sousa et al. 2006Sousa JP, Bolger T, Gama MM, Lukkari T, Ponge JF, Simon C, Traser G, Vanbergen AJ, Brennan A, Dubs F, Ivitis E, Keating A, Stofer S, Watt AD (2006) Changes in Collembola richness and diversity along a gradient of land-use intensity: a pan European study. Pedobiologia 50: 147-156. https://doi.org/10.1016/j.pedobi.2005.10.005
https://doi.org/10.1016/j.pedobi.2005.10...
, Vanbergen et al. 2007Vanbergen AJ, Watt AD, Mitchell R, Truscott AM, Palmer SCF, Ivits E, Eggleton P, Jones TH, Sousa JP (2007) Scale-specific correlations between habitat heterogeneity and soil fauna diversity along a landscape structure gradient. Oecologia 153: 713-725. https://doi.org/10.1007/s00442-007-0766-3
https://doi.org/10.1007/s00442-007-0766-...
, Salmon et al. 2014Salmon S, Ponge JF, Gachet S, Deharveng L, Lefebvre N, Delabrosse F (2014) Linking species, traits and habitat characteristics of Collembola at European scale. Soil Biology and Biochemistry 75: 73-85. https://doi.org/10.1016/j.soilbio.2014.04.002
https://doi.org/10.1016/j.soilbio.2014.0...
). These animals are among the most diverse and representative groups of soil fauna (Deharveng 1996Deharveng L (1996) Soil Collembola diversity, endemism, and reforestation: a case study in the Pyrenees (France). Conservation Biology 10: 74-84. https://doi.org/10.1046/j.1523-1739.1996.10010074.x
https://doi.org/10.1046/j.1523-1739.1996...
, Cassagne et al. 2003Cassagne N, Gers C, Gauquelin T (2003) Relationships between Collembola, soil chemistry and humus types in forest stands (France). Biology and Fertility of Soils 37: 355-361. https://doi.org/10.1007/s00374-003-0610-9
https://doi.org/10.1007/s00374-003-0610-...
) and play a critical role in nutrient cycling and organic matter decomposition dynamics (Hopkins 1997Hopkin SP (1997) Biology of the Springtails (Insecta: Collembola). New York, Oxford University Press., Zeppelini and Bellini 2004Zeppelini DF, Bellini BC (2004) Introdução ao estudo dos Collembola. João Pessoa, Editora Universitária, Universidade Federal da Paraíba, 82 pp.). Despite their importance, most studies on springtails from Neotropical ecosystems employ solely a systematic or taxonomic approach (Abrantes et al. 2010Abrantes EA, Bellini BC, Bernardo AN, Fernandes LH, Mendonça MC, Oliveira EP, Queiroz GC, Sautter KD, Silveira TC, Zeppelini D (2010) Synthesis of Collembola: an update to the species list. Zootaxa 2388: 1-22., 2012Abrantes EA, Bellini BC, Bernardo AN, Fernandes LH, Mendonça MC, Oliveira EP, Queiroz GC, Sautter KD, Silveira TC, Zeppelini D (2012) Errata Corrigenda and update for the “Synthesis of Brazilian Collembola: an update to the species list.” Abrantes et al. (2010), Zootaxa 2388: 1-22., Bellini and Godeiro 2012Bellini BC, Godeiro NN (2012) A new species of Tyrannoseira (Collembola: Entomobryidae: Seirini) from the Brazilian coastal region. Zoologia 29: 81-84. https://doi.org/10.1590/S1984-46702012000100010
https://doi.org/10.1590/S1984-4670201200...
, Bellini and Zeppelini 2008Bellini BC, Zeppelini D (2008) A new species of Seira (Collembola: Entomobryidae) from northeastern Brazil. Revista Brasileira de Zoologia 25(4): 724-727. https://doi.org/10.1590/S0101-81752008000400018
https://doi.org/10.1590/S0101-8175200800...
, 2011Bellini BC, Zeppelini D (2011) New genus and species of Seirini (Collembola, Entomobryidae) from Caatinga Biome, Northeastern Brazil. Zoosystema 33: 545-555. https://doi.org/10.5252/z2011n4a6
https://doi.org/10.5252/z2011n4a6...
, Culik and Zeppelini 2003Culik MP, Zeppelini D (2003) Diversity and distribution of Collembola (Arthropoda: Hexapoda) of Brazil. Biodiversity and Conservation 12: 1119-1143. https://doi.org/10.1023/A:1023069912619
https://doi.org/10.1023/A:1023069912619...
, Santos-Rocha et al. 2011Santos-Rocha IM, Andreazze R, Bellini BC (2011) Registros de Collembola (Arthropoda, Hexapoda) no estado do Rio Grande do Norte, Brasil. Biota Neotropica 11: 167-170. https://doi.org/10.1590/S1676-06032011000300013
https://doi.org/10.1590/S1676-0603201100...
, Zeppelini and Bellini 2004Zeppelini DF, Bellini BC (2004) Introdução ao estudo dos Collembola. João Pessoa, Editora Universitária, Universidade Federal da Paraíba, 82 pp., Zeppelini and Lima 2012Zeppelini D, Lima ECA (2012) A new species of Tyrannoseira (Collembola, Entomobryidae, Seirini) from Paraiba, Northeastern Brazil. Zootaxa 3423: 36-44.), yielding little information on variations in species richness and abundance of individuals in space and time (Vasconcellos et al. 2010Vasconcellos A, Andreazze R, Almeida AM, Araujo HFP, Oliveira ES, Oliveira U (2010) Seasonality of insects in the semi-arid Caatinga of northeastern Brazil. Revista Brasileira de Entomologia 54: 471-476. https://doi.org/10.1590/S0085-56262010000300019
https://doi.org/10.1590/S0085-5626201000...
, Ferreira et al. 2013Ferreira AS, Bellini BC, Vasconcellos A (2013) Temporal variations of Collembola (Arthropoda: Hexapoda) in the semiarid Caatinga in northeastern Brazil. Zoologia 30: 639-644. https://doi.org/10.1590/S1984-46702013005000009
https://doi.org/10.1590/S1984-4670201300...
).

Caatinga is a seasonally dry tropical forest that covers approximately 970,000 km2 of a semiarid region almost entirely restricted to the Northeast Region of Brazil (Brasil 2007Brasil (2007) Ministério do Meio Ambiente. Caatinga. http://www.mma.gov.br/biomas/caatinga [Accessed: 09/08/2017]
http://www.mma.gov.br/biomas/caatinga...
). It hosts a surprisingly large diversity of environments in the form of a mosaic of vegetation types, including dry forests and open formations (Tabarelli and Silva 2003Tabarelli M, Silva JMC (2003) Áreas e ações prioritárias para a conservação da biodiversidade da Caatinga. In: Leal IR, Tabarelli M, Silva JMC (Eds) Ecologia e Conservação da Caatinga. Universidade Federal de Pernambuco, Recife, 777-796.). Caatinga soils are generally rich in minerals, but at the same time they are also stony, shallow, and well drained (Alves et al. 2009Alves JJA, Araújo MA, Nascimento SS (2009) Degradação da Caatinga: uma investigação ecogeográfica. Revista Caatinga 22: 126-135.).

Currently, Caatinga is one of the South American phytogeographic domains most affected by anthropogenic disturbance, including desertification (Leal et al. 2003Leal IR, Tabarelli M, Silva JMC (2003) Ecologia e Conservação da Caatinga. Recife: UFPE, 804p., MMA 2005MMA (2005) Análise das variações da biodiversidade do bioma Caatinga. Suporte a estratégias regionais de conservação. Brasília, Ministério do Meio Ambiente, 466 pp.), but there have been few studies on biodiversity and ecological processes of this region, especially on structure of its soil fauna. In this context, this study aims to identify which parameters of a selected set related to vegetation structure, such as species richness, aerial biomass, litterfall, and soil characteristics, such as pH, granulometry and soil organic matter, are related to and can predict the epiedaphic Collembola species richness and abundance in Caatinga, Northeast Brazil.

MATERIAL AND METHODS

Springtails were collected in Caatinga from Cauaçu Farm (05°32’15”S, 35°49’11”W), located at municipality of João Câmara, state of Rio Grande do Norte, Brazil. The study area covers 700 ha of a continuum of habitats composed of secondary forests with distinct disturbance histories and distinct levels of vegetation recovery, and has a strong decidual character, losing practically all leaves during the dry season. The climate of the region is semiarid with an average annual rainfall of 648.6 mm and a short rainy season from March to June. The average annual temperature is 24.7 °C with a minimum temperature of 21 °C and a maximum of 32 °C.

A grid of 2000 × 500 m that has been undisturbed for more than 50 years was delimited and, within this area, 30 plots (20 ×20 m) were randomly selected for sampling springtails and quantifying habitat variables. Two samplings were performed, one during the rainy season (July 2011) and another during the dry period (November 2011), using five pitfall traps in each plot, disposed in a cross-shaped design and distant 1m from each other. Traps were 20 cm high and 10 cm in diameter and each one contained 300 ml of 70% ethanol; they were left exposed for 48 hours in each plot.

All sampled specimens were counted under a stereomicroscope and posteriorly mounted on glass slides in Hoyer’s medium, following the methodology described by Arlé and Mendonça (1982Arlé R, Mendonça C (1982) Estudo preliminar das espécies de Dicranocentrus Schött, 1893, ocorrentes no Parque Nacional da Tijuca, Rio de Janeiro. Revista Brasileira de Biologia 42: 41-49.). Taxonomic identifications were performed under an optical microscope with specialized identification keys (Christiansen and Bellinger 1980Christiansen K, Bellinger PF (1980) The Collembola of North America north of Rio Grande, a taxonomic analysis. Grinnel College, Iowa, 1322 pp., Zeppelini and Bellini 2004Zeppelini DF, Bellini BC (2004) Introdução ao estudo dos Collembola. João Pessoa, Editora Universitária, Universidade Federal da Paraíba, 82 pp., Bellinger and Christiansen 1996-2017Bellinger PF, Christiansen KA, Janssens F (1996-2017) Checklist of the Collembola of the world. http://www.collembola.org [Accessed: 08/31/2017]
http://www.collembola.org...
).

Species richness, density, and aerial biomass of the vegetation were obtained through a phytosociological study using the plots method (Mueller-Dombois and Ellenberg 1974Mueller-Dombois D, Ellenberg H (1974) Aims and methods of vegetation ecology. New York, John Willey & Sons, 547 pp.); all living individual plants with a root collar diameter (RCD) equal to or greater than 3 cm and with a total height equal to or greater than 1m were sampled (Rodal 1992Rodal MJN (1992) Fitossociologia da vegetação arbustivo-arbórea em quatro áreas de caatinga em Pernambuco. PhD Thesis, Universidade Estadual de Campinas, Campinas, São Paulo, 198 pp. http://repositorio.unicamp.br/jspui/handle/REPOSIP/314972
http://repositorio.unicamp.br/jspui/hand...
). The phytosociological evaluation was performed in a 10 × 10 m area at the centers of each plot. A general equation for Caatinga plants was used to estimate the aerial biomass of each plot (Sampaio and Silva 2005Sampaio EVSB, Silva GC (2005) Biomass equations for Brazilian semiarid Caatinga. Acta Botanica Brasilica 19: 935-943. https://doi.org/10.1590/S0102-33062005000400028
https://doi.org/10.1590/S0102-3306200500...
).

Litterfall was collected each month from November 2010 to October 2011 in a 1m × 1m collector net composed of a galvanized steel frame suspending a nylon mesh (1.0 mm) approximately 20 cm above the ground at the center of each plot. The nylon mesh enabled the falling litter to be collected without accumulating water (and thus avoided decomposition during the rainy season) (Costa et al. 2007Costa CCA, Dantas IM, Camacho RGV, Souza AM, Silva NF (2007) Produção de serapilheira na Caatinga da Floresta Nacional do Açú-RN. Revista Brasileira de Biociências 5(Supl. 1): 246-248.). After 12 months, the litterfall dry mass was calculated for each of the 30 plots. Soil analyses to assess pH, organic matter content, and grain size were performed at the EMPARN (Empresa de Pesquisa Agropecuária do Rio Grande do Norte), using soil methods analysis described by Embrapa (1997EMBRAPA (1997) Manual de métodos de análise de solo. Embrapa, Centro Nacional de Pesquisa de Solos, Rio de Janeiro, 212 pp.).

To evaluate which of the studied habitat parameters best explain the species richness and abundance of epiedaphic Collembola in Caatinga, a multiple linear regression was performed between the assemblage and habitat parameters (plant species richness, plant density (ind./100 m²), aerial biomass of the vegetation (kg) and litterfall, as well as the pH, organic matter (g.dm-3) and sand (g.kg-1)). Regression analyzes were also performed for the most abundant species. The parameters included in this model vary spatially and can create habitat heterogeneity on a local scale (Tscharntke et al. 2002Tscharntke T, Stevan-Dewenter I, Kruess A, Thies C (2002) Contribution of small habitat fragments to conservation of insect communities of grassland-cropland landscapes. Ecological Applications 12: 354-363., Vinatier et al. 2011Vinatier F, Tixier P, Duyck PF, Lescourret F (2011) Factors and mechanisms explaining spatial heterogeneity: a review of methods for insect populations. Methods in Ecology and Evolution 2: 11-22. https://doi.org/10.1111/j.2041-210X.2010.00059.x
https://doi.org/10.1111/j.2041-210X.2010...
). All analyses were performed in R (R core Team 2015R Core Team (2015) R: A language and environment for statistical computing. Vienna, R Foundation for Statistical Computing. https://www.R-project.org [Accessed: 07/25/2015]
https://www.R-project.org...
).

RESULTS

A total of 5,513 springtails were collected, distributed in 15 species, 13 genera and 9 families (Table 1). Entomobryidae was the richest family with five species, three of them from Seira Lubbock, 1870. The most abundant species were Temeritas sp., with 2,086 individuals (38% of the total abundance) and Neotropiella meridionalis (Arlé, 1939), with 1,911 individuals (35% of the total abundance). The least abundant species was Hemisotoma thermophila (Axelson, 1900), with only one specimen collected.

Table 1
Epiedaphic Collembola taxa recorded from João Câmara, Rio Grande do Norte, Brazil, in July 2011 (rainy period) and November 2011 (dry period) and their respective abundances.

Species richness and abundance were not correlated (r = 0.42) and, therefore, both were separately treated as dependent variables in the models. A correlogram between the environmental variables also showed a weak relation between them (r < 0.5); therefore, both were inserted in the regression model. The environmental variables included in the model did not significantly explain the epiedaphic Collembola species richness (R2 = 29%, R2 adj = 1.7%, P-value > 0.5), but the regression model explained approximately 59% (R2 = 59%, R2 adj = 43%, P-value < 0.01) of the variation in epiedaphic Collembola abundance (Table 2). From all the variables analyzed, plant richness, aerial biomass, and soil pH were significantly related to the epiedaphic Collembola abundance; aerial biomass was the only one negatively correlated (Table 2).

Table 2
Results of multiple regressions between epiedaphic Collembola abundance (R2: 59%, R2 adj: 43%, P-value: 0.011) and richness (R2: 29%, R2 adj: 1.7%, P-value: 0.424) and environmental variables recorded in João Câmara, Rio Grande do Norte, Brazil, in 2011. SOM: soil organic matter.

Based on the regressions among environmental variables and abundance of each species, only two of the sampled habitat variables significantly affected the number of individuals: Seira sp. 2 (R² = 0.47, R²adj = 0.17, P-value < 0.05) was positively correlated with litter production and Sphaeridia sp. (R2 = 0.48, R²adj = 0.27, P-value < 0.05) was positively correlated with both plant density (P-value < 0.01) and litter production (P-value < 0.05).

DISCUSSION

Collembola species richness recorded in this study is in accordance with other studies performed in Caatinga, which range from 2 to 15 species (Santos-Rocha et al. 2011Santos-Rocha IM, Andreazze R, Bellini BC (2011) Registros de Collembola (Arthropoda, Hexapoda) no estado do Rio Grande do Norte, Brasil. Biota Neotropica 11: 167-170. https://doi.org/10.1590/S1676-06032011000300013
https://doi.org/10.1590/S1676-0603201100...
, Ferreira et al. 2013Ferreira AS, Bellini BC, Vasconcellos A (2013) Temporal variations of Collembola (Arthropoda: Hexapoda) in the semiarid Caatinga in northeastern Brazil. Zoologia 30: 639-644. https://doi.org/10.1590/S1984-46702013005000009
https://doi.org/10.1590/S1984-4670201300...
), and with Seira being dominant in terms of number of species. This genus is the most taxonomically rich in Brazil, with approximately 30 species, of which 17 have been recorded from Caatinga (Bellini and Zeppelini 2009Zeppelini D, Bellini BC, Creão-Duarte AJ, Hernández MIM (2009) Collembola as bioindicators of restoration in mined sand dunes of Northeastern Brazil. Biodiversity and Conservation 18: 1161-1170. https://doi.org/10.1007/s10531-008-9505-2
https://doi.org/10.1007/s10531-008-9505-...
, Santos-Rocha et al. 2011Santos-Rocha IM, Andreazze R, Bellini BC (2011) Registros de Collembola (Arthropoda, Hexapoda) no estado do Rio Grande do Norte, Brasil. Biota Neotropica 11: 167-170. https://doi.org/10.1590/S1676-06032011000300013
https://doi.org/10.1590/S1676-0603201100...
, Abrantes et al. 2010Abrantes EA, Bellini BC, Bernardo AN, Fernandes LH, Mendonça MC, Oliveira EP, Queiroz GC, Sautter KD, Silveira TC, Zeppelini D (2010) Synthesis of Collembola: an update to the species list. Zootaxa 2388: 1-22., 2012Abrantes EA, Bellini BC, Bernardo AN, Fernandes LH, Mendonça MC, Oliveira EP, Queiroz GC, Sautter KD, Silveira TC, Zeppelini D (2012) Errata Corrigenda and update for the “Synthesis of Brazilian Collembola: an update to the species list.” Abrantes et al. (2010), Zootaxa 2388: 1-22., Zeppelini et al. 2017Zeppelini D, Queiroz GC, Bellini BC (2017) Collembola in Catálogo Taxonômico da Fauna do Brasil. PNUD. http://fauna.jbrj.gov.br/fauna/faunadobrasil/8735 [Accessed: 07/10/2017]
http://fauna.jbrj.gov.br/fauna/faunadobr...
). As suggested by Bellini and Zeppelini (2009Bellini BC, Zeppelini D (2009) A new species of Seira Lubbock (Collembola, Entomobryidae), with a key to the species of Paraíba, Brazil. Revista Brasileira de Entomologia 53(2): 266-271.https://doi.org/10.1590/S0085-56262009000200008
https://doi.org/10.1590/S0085-5626200900...
), the Northeast Region of Brazil is possibly one of the areas with the highest Seira species richness in the world.

Epiedaphic Collembola abundance was explained by plant richness and aerial biomass, indicating that Caatinga plant assemblage influences habitat structure and, possibly, the availability of direct and indirect food resources for these hexapods. Although springtails are considered generalist consumers, intestinal content analysis has shown considerable amounts of plant organic matter in the digestive tracts of several Neotropical species (Castaño-Meneses et al. 2004Castaño-Meneses G, Palacios-Vargas JG, Cutz-Pool LQ (2004) Feeding habits of Collembola and their ecological niche. Anales del Instituto de Biologia, Universidad Nacional Autónoma de México, Serie Zoologia 75: 135-142.). Therefore, the vegetation can apparently influence the Collembola fauna through changes in the habitat and the availability of food resources.

Epiedaphic Collembola assemblage only responded positively to spatial heterogeneity of the environment via plant richness, which potentially contributes to production of a more biochemically diverse litterfall that serves as a direct and/or indirect resource for different populations. A relationship between the composition of Collembola assemblages and vegetation structure and habitat quality has been previously suggested (Davidowitz and Rosenzweig 1998Davidowitz G, Rosenzweig ML (1998) The latitudinal gradient of species diversity among North American grasshoppers within a single habitat: a test of the spatial heterogeneity hypothesis. Journal of Biogeography 25: 553-560. https://doi.org/10.1046/j.1365-2699.1998.2530553.x
https://doi.org/10.1046/j.1365-2699.1998...
, Vegter et al. 1988Vegter JJ, Joosse ENG, Ernsting G (1988) Community structure, distribution and population dynamics of Entomobryidae (Collembola). Journal of Animal Ecology 57(3): 971-981., Romero-Alcaraz and Ávila 2000Romero-Alcaraz E, Ávila JM (2000) Landscape heterogeneity in relation to variation in epigaeic beetle diversity of a Mediterranean ecosystem. Implications for conservation. Biodiversity and Conservation 9: 985-1005. https://doi.org/10.1023/A:1008958720008
https://doi.org/10.1023/A:1008958720008...
, Tanabe et al. 2001Tanabe SI, Masanori JT, Vinokurova AV (2001) Tree shape, forest structure and diversity of drosophilid community: comparison between boreal and temperate birch forests. Ecological Research 16: 369-385. https://doi.org/10.1046/j.1440-1703.2001.00402.x.
https://doi.org/10.1046/j.1440-1703.2001...
, Vanbergen et al. 2007Vanbergen AJ, Watt AD, Mitchell R, Truscott AM, Palmer SCF, Ivits E, Eggleton P, Jones TH, Sousa JP (2007) Scale-specific correlations between habitat heterogeneity and soil fauna diversity along a landscape structure gradient. Oecologia 153: 713-725. https://doi.org/10.1007/s00442-007-0766-3
https://doi.org/10.1007/s00442-007-0766-...
, Nunes et al. 2008Nunes LAPL, Araújo Filho JA, Menezes RIQ (2008) Recolonização da fauna edáfica em áreas de Caatinga submetidas a queimadas. Revista Caatinga 21(3): 214-220., Zeppelini et al. 2009Zeppelini D, Bellini BC, Creão-Duarte AJ, Hernández MIM (2009) Collembola as bioindicators of restoration in mined sand dunes of Northeastern Brazil. Biodiversity and Conservation 18: 1161-1170. https://doi.org/10.1007/s10531-008-9505-2
https://doi.org/10.1007/s10531-008-9505-...
), but our study indicated that the aerial biomass in the Caatinga was negatively related to epiedaphic Collembola abundance, suggesting that it is not favored by the high litterfall produced by a few large plant species. In other words, the environmental factors (i) plant species richness and (ii) aerial biomass were negatively related to each other in the study area. In this way, the model suggests that the epiedaphic Collembola has low species richness and abundance in sites where there is high litterfall produced by few plant species which hold abundant aerial biomass.

Variation in Collembola abundance was also explained by variation in soil pH, reflecting the expected adaptation of some species to subneutral soil pH as previously presented in the literature (Van Straalen and Verhoef 1997Van Straalen NM, Verhoef HA (1997) The development of a bioindicator system for soil acidity based on Arthropod pH preferences. Journal of Applied Ecology 34(1): 217-232. https://doi.org/10.2307/2404860
https://doi.org/10.2307/2404860...
). Dynamics of soil pH is one of the most important edaphic biochemical factors, it differentially affects distribution and composition of Collembola soil assemblages, benefiting some taxa while eliminating more sensitive species (Pozo 1986Pozo J (1986) Ecological factors affecting Collembola populations. Ordination of communities. Revue d’Écologie et Biologie du Sol 23: 299-311., Cutz-Pool et al. 2003Cutz-Pool LQ, Palacios-Vargas JG, Vázquez MM (2003) Comparación de algunos aspectos ecológicos de Collembola em cuatro asociaciones vegetales de Noh-Bec, Quintana Roo, México. Folia Entomologica Mexicana 21: 91-101.).

The small-scale spatial variations affected the epiedaphic Collembola fauna in the studied semiarid ecosystem, especially the abundance of individuals, which was influenced by changes in some vegetation parameters such as plant species richness, aerial biomass, and soil pH. In contrast, the measured variables did not explain the variation in species richness, suggesting that other unmeasured variables, such as soil moisture and temperature, plant litter height, and predation pressure may be more closely related to variation in Collembola species richness. It is possible that temperature and humidity, isolated or in synergism, represent important environmental factors that affect Collembola activity in semiarid ecosystems. This fauna can be active only during periods of lower temperature and higher humidity, such as night, early morning, and sunset. In this way, active methods (soil core samples or entomological aspiration) or passive (pitfall traps) can reveal different species richness and abundance, biasing the results.

ACKNOWLEDGEMENTS

We thank Conselho Nacional de Desenvolvimento Científico e Tecnológico (Universal/CNPq, processes 441451/2014-4, PQ2015, 301498/2015-6) for funding this study and Uirandé Oliveira, Pedro Capistrano, Daniel Oliveira, Nicolas de Araújo, Heitor Bruno, and Thiago Felipe for their assistance in collecting the samples.

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Publication Notes

  • Available online:

    May 23, 2018
  • Zoobank Register:

    http://zoobank.org/6960ACAC-A5CB-4D76-B27E-54EC9E3EDF5B
  • Publisher:

    © 2018 Sociedade Brasileira de Zoologia. Published by Pensoft Publishers at https://zoologia.pensoft.net

Edited by

Editorial responsibility:

Gabriel L.F. Mejdalani

Data availability

Data citations

Bellinger PF, Christiansen KA, Janssens F (1996-2017) Checklist of the Collembola of the world. http://www.collembola.org [Accessed: 08/31/2017]

Publication Dates

  • Publication in this collection
    18 June 2018
  • Date of issue
    2018

History

  • Received
    12 May 2017
  • Reviewed
    09 Sept 2017
  • Accepted
    30 Oct 2017
  • Published
    23 May 2018
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