Introduction

Pinus species are cultivated in roughly 2 million hectares in Brazil (Sistema Nacional de Informaçōes Florestais [SNIF], 2019), 288 thousand in the state of Rio Grande do Sul (Associação Gaúcha De Empresas Florestais [AGEFLOR], 2020). Pine forests are often mentioned as ‘green deserts’, because they form microclimates, modify soil properties, inhibit the development of other plant species, homogenize the litter with needles and produce allelopathic substances (Pompeo et al., 2016; Spiazzi et al., 2017). Needles have poor nutritional quality, high content of tannins, terpenes, and other secondary metabolites that make difficult consumption by many soil organisms, favoring groups that can digest them (Kleinpaul, Schumacher, Brun, Brun, & Kleinpaul, 2005; Zhang, Wang, & Liu, 2018). In addition, substances are released from needles during decomposition, such as monoterpenes, which is harmful to many soil organisms and plants (Schlyter & Birgersson, 1999). Environmental homogenization in pine forests results in low diversity of food and reduces species richness of soil fauna (Mboukou-Kimbatsa & Bernhard-Reversat, 2001; Silva, Lima, Andrade, & Brown, 2019).

Springtails (Collembola) are organisms of the soil mesofauna responsible for ecosystem services, such as biological control, dispersion of microorganisms, nutrient mineralization, production of humic substances, and others (Čuchta, Kaňa, & Pouska, 2019; Potapov et al., 2020). In forest soils, springtail density can reach up to 40,000 organisms per square meter (Orgiazzi et al., 2016). Furthermore, they are excellent bioindicators of soil quality due to their sensitivity to environmental factors. Marx (2008) demonstrated that sites with intermediate soil moisture harbor higher abundances, followed by wet and dry areas. In native forests from southern Brazil, the abundance of springtails of the order Entomobryomorpha are directly related to rainfall during the soil sampling period (Rieff, Luz, Sousa, & Sá, 2014).

Soil moisture is also a decisive factor for the life cycle and distribution of Crustacea. These organisms habitually live in marine environments, although some species are adapted to terrestrial environments, especially forest soils (Sousa & Dangremond, 2011). Members of the family Gammaridae, superfamily Talitridae, live on the soil/litter interface (Friend & Richardson, 1986), associated with humid environments where they find shelter from dehydration. Some species of the family Talitridae were co-introduced with species of the exotic flora, and were associated with disturbed areas and areas of Eucalyptus spp. afforestation (Kotze & Lawes, 2008).

Knowledge regarding the fauna of Collembola and crustacean in Brazilian P. elliottii forests is very limited (Troian, Baldissera, & Hartz, 2009; Bugs, Araujo, Mendonça Júnior, & Ott, 2014; Buckup & Bond-Buckup, 1999), therefore, the environmental conditions in a 52-year-old pine forest are very conducive to studying groups of organisms adapted to these adverse conditions. Thus, the goal of this study was (1) to evaluate the abundance and richness of springtails in soil of a 52-year-old pine afforestation with different soil moisture contents; and (2) to identify the landhopper sampled unintentionally.

Material and methods

Site description

Soil fauna was sampled in an afforestation of P. elliottii of 6.2 hectares and 2 x 2 meters spacing at the Universidade Federal de Santa Maria, Santa Maria, state of Rio Grande do Sul, Brazil (29º43′20′′ S, 53º42′48′′ W, 95 m). The area was planted in 1966, and since then the pine trees were never pruned or cut. The soil is classified as Gray-Brown Argisol, and the climate is Cfa Subtropical humid, according to the Köppen classification (Moreno, 1961). The average temperature reaches 18.5ºC, and the rainfall is well distributed reaching 1,580 mm per year. Values of temperature and rainfall in the period close to and during the sampling are illustrated in Figure 1. Weather data was obtained from an official station, located 530 m from the study area (Instituto Nacional de Metereologia [INMET], 2017).

Soil fauna sampling

Collembola specimens were sampled in the spring, during four days (09 – 13 Oct. 2017). Pitfall traps (diameter 10 cm and depth 20 cm) protected from rainfall were added with 500 mL ethanol 70% (v v^-1), used as a preservative solution. Traps were set up at six points distant seven meters from each other. Three points were located in the high moisture area (Ug 0.35 g g^-1), at an approximate distance of 3 m from a stream. The other three points were located in the low moisture area (Ug 0.25 g g^-1), far 12 m from the same stream, and in a slightly more elevated area of the forest. At each point, three pitfall traps were set up, totaling 18 traps. After four days, traps were taken from the field and samples were processed at the laboratory. Specimens were carefully cleaned up with water, and kept in ethanol 70% (v v^-1). Springtails were classified into families and genera according to specialized keys (Cipola, Silva & Bellini, 2018; Bellinger, Christiansen, & Janssens, 1996-2022), once the identification into species was not possible due to the scarce number of records for the region (Bellinger et al., 1996-2022). The unique landhopper species sampled was identified according to Buckup and Bond-Buckup (1999).

Physical and chemical properties of soil

Soil samples were collected (0–20 depth) to analyze the physical and chemical properties of each of the six points. Samples were mixed into a composite sample for the areas of high and low soil moisture content. The properties analyzed were: clay content (densimeter), organic matter (Walkley-Black), pH (water 1:1), phosphorous (Mehlich-1), calcium (EDTA), magnesium (EDTA), sulfur (Ca₃(PO₄)₂), cation exchange capacity (CEC), potential acidity (H+Al) and base saturation (V%). The chemical properties from both high and low moisture soil areas in the afforestation are listed in Table 1.

For physical property analysis, two undeformed samples (0-5 cm depth and 5 -10 cm depth) from three points of each area were collected using steel cylinders, totaling 12 samples. Soil density (graduated cylinder method), total porosity (saturation by water), microporosity, and macroporosity (tension table) were determined, according to Teixeira, Donagemma, Fontana, and Teixeira (2017). The gravimetric moisture was determined after drying soil at 105°C. For each sampling point, three samples of litter were collected using a metallic frame (25 x 15 cm). Samples were dried in a forced air oven at 65°C to constant weight.

Data analysis

For the Collembola community, we calculated the diversity profile by the Renyi index (function renyiresult, ‘BiodiversityR’ package); the dissimilarity between areas was calculated by the Jaccard index. A permutational multivariate analysis of variance, using distance matrices (function ‘adonis’) based on the Jaccard index (function ‘vegdist’), was applied to evaluate the difference in springtail community between areas with low and high soil moisture. Medians of abundance of Collembola and Crustacea in the areas of low and high soil moisture were compared by the Mann-Whitney test. All statistical analyses were run using R version 3.6.0 (R Core Team, 2019).

Results

A total of 2,528 specimens of Collembola were sampled and identified in the P. elliottii afforestation, belonging to Desoria, Ceratophysella, Lepidocyrtus, Calvatomina, and Entomobrya (Table 2 and Figure 2). Specimens of Onychiuridae were not identified at the genus/species levels due to the lack of literature and records for the region. The low soil moisture area showed an abundance of springtails eight times fold higher than the high soil moisture area. Specimens of Onychiuridae largely dominated the low soil moisture area, representing 89% individuals sampled and being 45 times more abundant in this environment compared to the high moisture soil. In this sense, Desoria and Lepidocyrtus were more abundant in the low soil moisture. Nevertheless, Desoria was superior in the high soil moisture area, with 48% relative frequency of individuals. Cerathophysella was found in a greater number in the high moisture area. The abundance of Entomobrya and Calvatomina was very low in the pine afforestation soil. Unintentionally, 16 specimens of Talitroides sylvaticus Haswell belonging to the family Talitridae (Crustacea) were collected. Their abundance was superior in the high moisture area (Table 2).

The calculated Jaccard Index was 66.7%, indicating similarity in the composition of genera and families of Collembola between high and low soil moisture areas (p = 0.23928). The Renyi diversity profiles showed that the species richness of springtails was five (alpha = 0) in both areas (Figure 3). However, the Shannon index (alpha = 1) and the Simpson index (alpha = 2) were higher in the area with high soil moisture. Moreover, this area was more even (alpha =0) and the lower proportion of dominant groups contributed to higher diversity.

The two sampled areas showed differences regarding the soil chemical and physical properties (Table 1). The high soil moisture area stood out by the content of calcium and magnesium, respectively, 545% and 440% superior to the low soil moisture area. On the other hand, values of OM, P, S, CEC, H+Al were higher in the low moisture area. The litter, composed of needles of P. elliottii, showed a high amount of dry mass, especially in the low soil moisture area. The analysis of physical properties demonstrated that the high moisture area soil is less dense due to a higher total porosity, with a predominance of micropores.

Discussion

The P. elliottii afforestation showed a low abundance of Collembola, with an average of 31 and 249 springtails per pitfall trap, in the high and low soil moisture areas. In the same pine afforestation, in a soil fauna study, Pessotto et al. (2020) obtained a greater abundance of springtails per trap, although in a longer sampling period (seven days). Silva, Saidelles, Vasconcellos, Webber, and Manassero (2011) also reported a high average abundance (1736 per pitfall trap) of Collembola in a pine forest close to the study region. In addition to the sampling time and environmental conditions in the study local (moisture, structure of the understory, soil surface, litter availability, etc.), seasonality may also influence the springtail abundance. In native and Eucalyptus forests, Ortiz et al. (2019) found a superior number of springtails per pitfall trap in the summer compared to the winter.

The soil moisture in the pine afforestation changed the population dynamics of Collembola, and the response relied on the genera and families, despite having the greater total abundance of individuals in the low moisture soil. Water excess in the soil may have reduced the availability of oxygen and impaired the population growth of some genera and families. Xu, Kuster, Goerg, Dobbertin, and Li (2012) indicate that springtails might be sensitive to excess of moisture in the environment and that specimens of some genera, such as Parisotoma, may be more abundant in low moisture areas. In our study, it should be considered that the low soil moisture area showed a higher amount of litter, higher organic matter content, phosphorous, and sulfur in the soil, which may have favored the grown of springtails (Eaton, 2006; Russell & Gercócs, 2019).

Specifically, specimens of Desoria, Lepidocyrtus, and the family Onychiuridae were more abundant in the low soil moisture area. Desoria acts in the decomposition of litter and their abundance is related to the amount of organic residues on the soil surface (Fujii, Saitoh, & Takeda, 2014). The organic matter content of the soil also influences the distribution of organisms of the family Isotomidae (including Desoria), and for this reason, they are considered indicators of changes in soil fertility (Salamon, Schaefer, Alphei, Schmid, & Scheu, 2004). Marx (2008) relates the presence of some organisms of this genus with low soil moisture. In contrast, in agriculture systems in southern Brazil, Sautter, Santos, and Ribeiro Júnior (1999) found individuals of the family Entomobryidae in no-till areas with high moisture and accumulation of organic matter.

In the area with low soil moisture, it was observed only one individual of Entomobrya. Chang, Wang, Liu, Callaham Jr. and Ge (2017) observed organisms of this genus in pine forests of different ages in China (from 26 to 260 years old), and its abundance did not vary significantly between forests. However, Fujii and Takeda (2012) report that the abundance of individuals of this genus is related to soil litter, which corroborates our results, in which Entomobrya was found in the area with the highest litter accumulation. Individuals of the family Onychiuridae largely dominated the area with low soil moisture. The high abundance of individuals of this family have been reported in a pine forest of around 80 years and justified by the high amount of litter in the soil (Chang et al., 2017). This condition also favors the development of fungi colonies, which are part of the diet of fungivorous springtails of this family (Potapov, Semenina, Korotkevich, Kuznetsova, & Tiunov, 2016; Samain, Baldy, Lecareux, Fernandez, & Santonja, 2019).

Some hygrobiont species of the Ceratophysella genus have been associated with high moisture and low pH of pine forest soils (Sławska, Bruckner, & Sławski, 2017), corroborating the observations of the present study. Organisms of the genus Calvatomina, belonging to the family Dicyrtomidae, might be sensible to drought environments and were also sampled in subtropical forests of high humid in Australia (Greenslade & Slatyer, 2017). In South Africa, Liu, Janion, and Chown (2012) report the presence of organisms of this family, and their invasive potential related to the high moisture of the litter of Pinus radiate forests. The litter moisture may also contribute to the greater abundance of springtails (Fujii et al., 2014) since the growth of fungi is favored in these conditions, which increases the availability of food for fungivorous springtails (Nakamori & Suzuki, 2010; Anslan, Bahram, & Tedersoo, 2018).

The moisture and the high content of calcium in the soil of the pine afforestation may have contributed to the occurrence of Talitroides sylvaticus, found in the area of high soil moisture. Landhoppers of the family Talitridae live in terrestrial environments and have nocturnal habits (Friend & Richardson, 1986). On the surface of the pine afforestation, T. sylvaticus finds conditions to avoid direct contact to solar radiation and consequently exoskeleton dehydration (Mendes & Ulian, 1987). Studies have also reported the presence of this landhopper in soils with high calcium content, an element necessary to exoskeleton formation, as observed in the present study (Ohta, Niwa, Agetsuma, & Hiura, 2014). Talitroides sylvaticus is an invasive species and its origin is unknown, although its presence was reported in the south of the state of Rio Grande do Sul state as well in urban areas, playgrounds, and botanic yards from Europe, where it was probably introduced by human activities (Buckup & Bond-Buckup, 1999).

Conclusion

Soil moisture changes the abundance, the structure of the community, and the diversity of Collembola in a 52-year-old P. elliottii afforestation. The low soil moisture area harbors a higher abundance of individuals of Desoria, Lepidocyrtus, Entomobrya, and the family Onychiuridae, meanwhile the high soil moisture area has a greater abundance of Ceratophysella and Calvatomina, as well as the larger diversity of springtails. The landhopper Talitroides sylvaticus sampled unintentionally was more abundant in the area with the high moisture and calcium in the soil.

Acknowledgements

This work was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001. and the authors thank the partnership with the Universidade de Santa Cruz do Sul and the Universidade Federal do Rio Grande do Norte.

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Notas de autor

rodrigo@ufsm.br

IR