Community Structure of Coleoptera Families and Staphylinidae Species as Potential Bioindicators in Atlantic Rain ForestAbstract
Beetles (Coleoptera) are structurally and functionally important in tropical forest ecosystems. The present research aimed to characterize Coleoptera families and Staphylinidae species in areas of native forest and pastures undergoing restoration with nucleation techniques in the Serra do Itajaí National Park. The collections were carried out from pitfall traps, from April/2017 to December/2018. A total of 2619 individuals of Coleoptera were collected, distributed in 30 families, and 637 individuals of Staphylinidae, distributed in 46 species. The abundance, richness, and composition of Coleoptera families and Staphylinidae species varied significantly between native forest and pasture with the inclusion of nucleation techniques for restoration. Microclimate had a significant influence on the ecological parameters analyzed. We identified families and species characteristic of forests and pastures. Less specific taxonomic identification levels showed significant differences, enabling its application as a potential bioindicator of restoration. Our results suggest that pasture areas still support an impoverished leaf litter beetle community.
Keywords Leaf litter insect fauna; nucleation techniques; taxonomy sufficiency
1. INTRODUCTION
Historically, the Atlantic Forest biome has suffered from intense processes of exploitation of natural resources, which range from the exploitation of timber and non-timber species, suppression of native vegetation for agricultural activities, urbanization, mining, among others ( Joly et al., 2014 ). Consequently, these changes impact the structure and functionality of biological communities ( Joly et al., 2014 ). Due to the high degree of threat, its high biodiversity, levels of endemism, and a high degree of threat, the Atlantic Forest is considered a biodiversity hotspot ( Myers et al., 2000 ).
The ecological restoration of degraded areas in this biome is an important strategy to mitigate and reverse the effects of environmental degradation, provide greater adaptability to climate change and sustainable development ( Rezende et al., 2018 ). The importance of restoration is evidenced by the United Nations (UN) definition of the period 2021-2030 as the Decade of Ecosystem Restoration as a way of encouraging a global effort to restore ecosystems and reduce degraded areas ( UN, 2019 ). In this scenario, the monitoring of different bioindicator groups is important both to assess the effects of degradation resulting from human activities and also to define more efficient strategies and in the monitoring of restoration ( Cole et al., 2016 ).
Restoration strategies and evaluation and monitoring indicators are geared towards the plant community ( Corbin and Holl, 2012 ; Suganuma and Durigan, 2015 ; Martins, 2018 ; Massi et al., 2021 ). However, with advances in restoration and ecology research, the importance of also considering the fauna and its interactions in this process has become increasingly evident ( McAlpine et al., 2016 ). This applies both to defining the techniques that can be implemented, to achieve effective results, and also as bioindicators in monitoring ( McAlpine et al., 2016 ; Cole et al., 2016 ).
The suppression of native plants causes significant changes in the environment, such as changes in the structure and functionality of native plant cover ( Maçaneiro et al., 2017 ). Which affect microclimatic variables, the dynamics of nutrient cycling, ecological interactions, among other changes ( Ottermanns et al., 2011 ). In the insect community (Hexapoda: Insecta), the effects of these changes are particularly important due to their representativeness, ecological importance, and ecosystem services provided ( Jeffery et al., 2010 ; Bouchard et al., 2017 ; Ramos et al., 2020 ). Of this group, beetles of the order Coleoptera have high species richness and functional importance, useful characteristics for obtaining information regarding variations in community structure, and as bioindicators of environmental quality ( Hopp et al., 2010 ; Jeffery et al., 2010 ; Wardhaugh et al., 2012 ; Leach et al., 2013 ; Bouchard et al., 2017 ; Noriega et al., 2021 ).
Staphylinidae (Insecta: Coleoptera) is a megadiverse family ( Bouchard et al., 2017 ) and stands out for its representativeness, heterogeneity, ecological importance, and sensitivity to environmental changes ( Bohac, 1999 ; Hopp et al., 2010 ; Irmler et al., 2018 ). In the Brazilian Atlantic Forest, rove beetles are often the most representative ( Marinoni and Ganho, 2003 ; Uehara-Prado et al., 2009 ; Hopp et al., 2010 ). At the soil-litter interface, they have different habits, such as predators, detritivores, fungivores, and phytophages ( Bohac, 1999 ; Irmler et al., 2018 ). Rove beatles have the potential to be considered bioindicators (see Méndez-Rojas et al., 2021 ), however, there is insufficient knowledge regarding the structural and functional parameters of this group. Little is known about this group, and despite their potential, they are rarely considered in restoration projects. Many factors influence the structural and functional parameters of staphylinids, such as successional stage, microclimate, soil type, amount of litter ( Hopp et al., 2010 ; Hoffmann et al., 2017 ), among others. Surveys of this group in the Atlantic Forest are important to characterize the biodiversity of Coleoptera and Staphylinidae, to better support conservation and restoration actions.
The high diversity of insects, the need for consultation with specialists, many species still unknown in tropical ecosystems, and their small size are some of the limiting factors in the application of these organisms as bioindicators ( Grimbacher et al., 2007 ; Hopp et al., 2010 ). In this context, the use of less specific identification levels (family) becomes an alternative ( e.g ., Nakamura et al., 2007 ; Uehara-Prado et al., 2009 ; Paiva et al., 2020 ). However, this does not seem to be a consensus ( Grimbacher et al., 2007 ). More research is needed to understand and validate this practice.
Considering the potential and importance of the order Coleoptera and the family Staphylinidae, the present research aimed to compare areas of native forest of the Atlantic Forest with areas of pastures undergoing ecological restoration techniques as nucleation.
2. MATERIAL AND METHODS
2.1. Study region
The study area is located in the Serra do Itajaí National Park (SINP) (27°00’ and 27°17’S, 49°01’ and 49°21’W, the altitude ranges from 600 to 700m), Santa Catarina state, South Brazil. The vegetation of the region is classified as Ombrophilous Dense Montana forest, Atlantic forest Biome ( IBGE, 2012 ). According to the Köppen classification, the climate of the region is Cfa ( Alvares et al., 2013 ). The average annual temperature between 16-18°C, with an average rainfall between 1,500 and 1,600 mm, with well-distributed rainfall throughout the year and with a relative humidity of approximately 82-84% ( Pandolfo et al., 2002 ).
2.2. Site characteristics and experimental design
Four areas were selected for study, divided into two treatments, namely:
1) Native forest (FOR): inserted in the Atlantic Forest Biome, in the phytophysiognomy Ombrophilous Dense Forest ( IBGE, 2012 ), classified in advanced and intermediate stages of succession, with a high richness of herbaceous, shrub and arboreal species and; 2) Nucleation techniques (NUC): pastures in the process of restoration from the techniques of planting seedlings and transposition of litter. For the planting of seedlings, the selection of species was based on the floristic-forestry inventory carried out in the SINP areas and the proportions of each species were determined based on the structure of forest remnants. The seedlings were distributed in cores adapted from Anderson (1953) according to Meneghetti & Vitorino ( 2018 ). The litter cores have dimensions of 1.0 x 1.0 meters and were deposited in the area to be restored in an open square on the ground with dimensions of 1.5 by 1.5 meters, distributed randomly, totaling 60 cores per hectare. Litter transposition consisted of transposing the litter layer from an area in an advanced stage of succession to the area to be restored ( Reis et al., 2003 ).
For each treatment, six sampling points (replications) were installed. Sampling was performed by installing pitfall traps (height: 18.5 cm; upper diameter: 21.5 cm, bottom diameter: 17 cm), 10 meters apart, containing water, 70% alcohol, and biodegradable detergent. The traps remained in the field for a period of three nights, installed bimonthly from April/2017 to December/2018, totaling 11 collections.
Beetle sampled were counted, and identified at the family and species level. The Coleoptera families were identified at the Laboratory for Monitoring and Forest Protection (LAMPF) of the Regional University of Blumenau (FURB). Staphylinidae species were identified by Edilson Caron, from the Federal University of Paraná (UFPR).
2.3. Microclimatic parameters
Mean temperature (ºC) and air humidity (%) data were collected during the period when the pitfalls remained in the field. The equipment used for data collection was the Lascar Eletronics data logger, model EL-USB-2, installed 30 cm above ground level near the pitfall located in the center of the transect. Two data logger was installed per treatment area, recording the data every 15 minutes.
2.4. Statistical analyses
To verify if there are significant differences between the abundance and richness of species and families, the Shapiro-Wilk normality test, analysis of variance (ANOVA) (p < 0.05) was applied. To verify significant differences at the family level, those with a relative frequency > 2% were selected and the Shapiro-Wilk normality test and, later, to the Kruskal-Wallis test (p < 0.05) for nonparametric data and an analysis of variance (ANOVA) (p < 0.05) for parametric data. At the species level, the Individual Indicator Value (IndVal) was determined with the aim of identifying indicator species ( Dufrêne and Legendre, 1997 ). The significance value of IndVal for each species was determined by the Monte Carlo test, with 4,999 permutations.
To test whether the composition of Coleoptera families and Staphylinidae species were different between areas, Non-Metric Multidimensional Scaling (NMDS) ( Borcard et al., 2011 ) based on Bray-Curtis dissimilarity was applied. To test the significance of likely differences in composition between areas, PERMANOVA (Permutational multivariate analysis of variance) was performed at a 5% significance level ( Anderson, 2011 ). The similarity between the sample areas was evaluated by applying the Jaccard similarity index ( Magurran, 2011 ).
Generalized Linear Models (GLM) were used to detect the effects of independent variables (medium humidity, medium temperature and variation temperature) on dependent variables (family/species richness and abundance of order Coleoptera and Staphylinidae species). The models were constructed for the distribution of Poisson errors with logarithmic link function. All analyzes were performed using the program R (version 4.1).
3. RESULTS
3.1. Coleoptera
A total of 2619 individuals were collected, distributed in 30 families ( Table 1 ). The most representative families were Ptiliidae (39.87%), Staphylinidae (35.75%), Leiodidae (6.59%), and Nitidulidae (6.07%) ( Table 1 ). Family abundance and richness were statistically higher in native forest areas ( Figure 1 A and B). Of the total number of families, 12 were registered exclusively in native forest and three in areas with nucleation techniques ( Table 1 ). The Jaccard index indicated similarity of 46.66%. The families composition differed significantly according to PERMANOVA and NMDS (F 1,10 = 42.53; p = 0.0019; stress = 0.09) ( Figure 2 A).
Abundance of Coleoptera families (A), richness of Coleoptera families (B), abundance of Staphylinidae species (C), and richness of Staphylinidae species (D). * F: values followed by the same latter are not statiscally different according variance analysis (ANOVA) (p < 0.05).
Nonmetric multidimensional scaling plots of families Coleoptera composition (A) and Staphylinidae species (B) in the two areas. Bray-Curtis was used as a similarity measure.
The families that showed significantly higher abundance in the native forest were Ptiliidae (F 1,10 = 102.4; p = < 0.0001), Staphylinidae (F 1,10 = 43.3; p = < 0.0001), Leiodidae (F 1,10 = 48.81; p = < 0.0001), Curculionidae (F 1,10 = 12.48; p = 0.005) and Scarabaeidae (K = 8.50; p = 0.003) ( Table 1 ). In the areas with the nucleation techniques, the families that showed the highest abundance were Chrysomelidae (F 1,10 = 7.56; p = 0.020) and Monotomidae (F 1,10 = 12.16; p = 0.005) ( Table 1 ).
3.2. Staphylinidae
A total of 637 individuals distributed in eight subfamilies, 28 genera, and 46 species were collected ( Table 2 ). The most representative species were Aleocharinae sp. 1, (13.81%), Lomechusini sp. 1 (6.44%), Anotylus sp. 1 (4.55%), and Hoplandriini sp. 1 (4.24%) ( Table 2 ). Species abundance and richness were statistically higher in the native forest ( Figure 1 C and D). Of the total number of species, 21 occurred exclusively in the native forest and 11 species exclusively in areas with nucleation techniques ( Table 2 ). The Jaccard index indicated 15.38% of similarity between the sample areas. Species composition varied significantly between sample areas according to PERMANOVA (F 1,10 = 6.32; p = 0.0018; stress = 0.13) ( Figure 2 B).
From IndVal, five indicator species were identified, with the highest number of indicator species from the native forest (n = 5) ( Table 3 ). All indicator species of the native forest have high indication values (> 75%), especially the species Aleocharinae sp. 1, Anotylus sp. 1, and Lomechusini sp. 1 ( Table 3 ). For areas with nucleation techniques, Falagriini sp. 1 showed 83.33% of indication ( Table 3 ).
Abundance and species composition of Staphylinidae (Insecta: Coleoptera) in native forest (FOR) and nucleation techniques (NUC).
3.3. Microclimatic variables
The temperature and relative humidity of the air presented the same dynamics for all the sampled areas ( Figure 3 A and B). In the native forest, the lowest values of temperature and the highest values of relative humidity were observed. An inverse pattern was observed in the pasture areas with the nucleation techniques ( Figure 3 A and B).
A) Medium temperature (ºC) and B) medium relative humidity air in native forest and nucleation techniques.
All analyzed microclimatic variables significantly influenced the abundance and richness of Coleoptera families and Staphylinidae species ( Table 4 ). The temperature variation had a negative influence on the beetle fauna parameters. The average air temperature and relative humidity positively influenced the richness of Coleoptera families, except for the relative humidity, which negatively influenced if ( Table 4 ).
Results of generalized linear models (GLM) demonstrating the effect of microclimate variables on abundance and richness. *significant effect (p<0,05).
4. DISCUSSION
In forest ecosystems, the suppression of native vegetation for the establishment of pastures causes significant biotic and abiotic changes in the place. Our data show that these changes affect Coleoptera families and Staphylinidae species. Pasture areas with nucleation techniques support an impoverished leaf litter beetle community when compared to native forests. The significant difference in composition, reduction in abundance, and the number of families and species in pasture areas with nucleation techniques indicate that the environment is still unsuitable for leaf litter beetles. This pattern corroborates with comparative surveys between Atlantic Forest environments and anthropized environments ( Salomão et al., 2018 ) and tropical forests with different successional stages ( Hopp et al., 2010 ).
The composition at the family level of the Coleoptera order and Staphylinidae species varied significantly between the sample areas. We believe that this difference may be related to the influence, direct and indirect, of the vegetation structure, through the deposition of litter, diversity of materials constituting the litter, and microclimate, resulting from the shading of the crowns. Through the analysis of the abundances of the families ( Table 2 ) and IndVal ( Table 3 ) for the species, a greater number of taxa associated with the native forest environment was observed.
4.1. Coleoptera families
The Ptiliidae, Staphylinidae, Leiodidae, Nitidulidae, and Curculionidae families were the most representative in the number of individuals. This pattern corroborates surveys carried out in different phytophysiognomies of the Atlantic Forest ( e.g. , Marinoni and Ganho, 2003 ; Hopp et al., 2010 ; Brito-Silva et al., 2016 ).
The Ptiliidae, Leiodidae, Curculionidae, and Scarabaeidae families were significantly more abundant in the native forest ( Table 1 ). This pattern can be explained by the fact that the tree cover of the forest provides adequate resources and conditions for these organisms. The Ptiliidae family and some species of Leiodidae have fungivorous habits ( Chandler and Peck, 1992 ; Darby and Chaboo, 2015 ) and, therefore, there is evidence that litter deposition and the presence of woody material provide more food resources for these organisms ( Chandler and Peck, 1992 ). The tree cover promotes greater litter deposition, greater humidity, and less light, favoring the proliferation of fungi ( Marinoni and Ganho, 2003 ). The family Curculionidae is composed of phytophagous beetles, many generalists, feeding on a wide variety of plant species ( Audino et al., 2007 ). As it is in an intermediate to an advanced stage of succession, the native forest provides a greater variety of food resources to be exploited by the weevils, when compared to pastures.
For Scarabaeidae, the significantly higher abundance in the native forest and the near absence in the areas of pasture with nucleation techniques ( Table 1 ) indicate the sensitivity of the family to tolerate changes in the environment. Removing canopy cover for alternative land uses, particularly pasture, results in biodiversity loss ( Arellano et al. 2023 ). The family Scarabaeidae are mostly scavengers ( Bouchard et al., 2017 ). In areas with nucleation techniques, the cover is predominant by exotic grasses and leaf litter is practically absent. The data corroborate those of Niero and Hernández ( 2017 ) when comparing pasture areas with native forest (Ombrophilous Dense) in Scarabaeinae (Coleoptera: Scarabaeidae) assemblages.
The lack of significance in the abundance of Nitidulidae indicates the adaptability of individuals to environments with different resources and conditions. This is because it is a family composed of individuals of different types of habits (detritivores, phytophagous, fungivorous, predators, among others) ( Audino et al., 2007 ), allowing its establishment in different environments. Our data corroborate those of Salomão et al. ( 2018 ) who observed that nitidulids are resistant to sugarcane matrices and with Fagundes et al. ( 2011 ) in exotic plantations ( Pinus elliottii and Eucalyptus saligna ).
Families Chrysomelidae and Monotomidae were more abundant in pasture areas with nucleation techniques ( Table 1 ). These families have different habits. Chrysomelidae has a phytophagous ( Bouchard et al., 2017 ). Monotomidae have diversified habits and can be found in decomposing materials, predators, and mycophages ( Bouchard et al. 2017 ). The pattern of abundance distribution among the sampled areas indicates the greater tolerance of families to environmental changes.
4.2. Staphylinidae species
The abundance and richness of species were statistically higher in the native forest ( Figure 2 C and D; Table 2 ), indicating the preference of rove beetles for forest environments, in a better state of conservation. The data corroborate the meta-analysis performed by Méndez-Rojas et al. ( 2021 ) and López-Bedoya et al. ( 2021 ), which indicates that species density and richness respond negatively to changes in land use, including pastures and forest plantation of exotic species. Hopp et al. ( 2010 ) observed the increase in Staphylinidae density during the advance of Atlantic Forest regeneration. Caballero et al. ( 2009 ) observed that open environments are not suitable for the main species of Staphylinidae.
Species composition varied significantly between sample areas ( Figure 2 – B). The Staphylininae subfamily, for example, occurred almost exclusively in the native forest ( Table 2 ). In pasture areas with nucleation techniques, only Aleocharinae spp. presented a greater number of individuals (n = 62). The other species showed an abundance equal to or less than six ( Table 2 ). Rove beetles are, for the most part, non-specific predators ( Bohac, 1999 ). According to other surveys carried out in Faxinal do Bepe, there is a reduction in springtail abundance and significant differences in insect composition between areas of native forest and pastures with different nucleation techniques ( Cristo et al., 2019 ; Arenhardt et al., 2020 ). Thus, changes in the structural parameters of staphylinid communities may be a consequence of the effects of habitat alteration on interspecific interactions.
Of the total number of native forest indicator species, four (Aleocharinae sp. 1, Anotylus sp. 1, Lomechusini sp. 1. and Hoplandriini sp. 1) belong to the Aleocharinae subfamily (Tables 2 and 3). This result evidences the preference of these species for more structured environments, with the presence of native tree cover. The Falagriini sp. 1 (Aleocharinae subfamily) seems to have benefited from the change in vegetation cover since it was an indicator of the pasture area with nucleation techniques ( Table 3 ). Aleocharinae is the largest subfamily of Staphylinidae and among the different habits, there are myrmecophilous individuals (Parker, 2016 ). Faxinal do Bepe has an expressive diversity of Formicidae (Hymenoptera) that inhabit the soil-litter interface, with significantly different compositions between native forest and pastures undergoing restoration ( Arenhardt et al., 2020 ) which in part may explain the pattern of distribution of Aleocharinae in the sample areas. However, specific experiments associating these two groups are necessary.
4.3. Microclimatic variables
In forest ecosystems, canopy structure is one of the main components that affect the microclimate ( Jennings et al., 1999 ), dampening the effect of extreme temperatures ( Ottermanns et al., 2011 ). In open landscapes, microclimatic conditions are more stressful due to greater exposure to wind, frost, extreme temperatures, and greater variation in temperature ( Tougeron et al., 2016 ). In our study areas, the native forest canopy cover provided an increase in relative humidity and a reduction in mean temperature and fluctuations throughout the day ( Figure 3 A and B), which significantly influenced the beetles’ fauna at the level of family and species ( Table 3 ). In this context, the canopy closure level has significant effects on litter re-colonization by these organisms, due to its effect on microclimatic conditions. This pattern corroborates Ottermanns et al. ( 2011 ). This result demonstrates that microclimate variabe is an important variable to be considered in the definition of strategies aimed at the recolonization by these organisms in areas undergoing restoration.
4.4. Taxonomy sufficiency
The data analysis used with the two levels of taxonomic identification (family and species) differentiated the areas of native forest from the areas of pastures with nucleation techniques. The use of less specific taxonomic levels has the limitation of obscuring significant responses, since species and families within the same order may respond differently to environmental changes ( Nakamura et al., 2009 ). However, considering the significant differences in the abundance, the richness of families ( Figure 1 A and B), and composition of Coleoptera ( Figure 2 A), and the differences in the abundance of some families ( Table 1 ), our results suggest the possibility of applying of less specific taxonomic levels (family). More robust conclusions can be obtained from the abundance of families such as, for example, Ptiliidae, Staphylinidae, Curculionidae, and Leiodidae, which were statistically superior in the native forest. The taxonomy and ecology of several Coleoptera species are still unknown in the Atlantic Forest. The bioindicator analysis at the family level proves to be a promoting alternative in this scenario.
5. CONCLUSION
- The abundance, richness, and composition of families of the Coleoptera order and species of the Staphylinidae differed significantly between areas of native forest and pastures with nucleation techniques.
- Families and species with bioindicator potential were identified, being the families Ptiliidae, Staphylinidae, Curculionidae, Leiodidae, and Scarabaeidae and the species Aleocharinae spp., Aleocharinae sp. 1, Anotylus sp. 1, Lomechusini sp. 1, and Hoplandriini sp. 1 as indicators of native forest. The families Chrysomelidae and Monotomidae and the species Falagriini sp. 1 as indicators of pasture with nucleation techniques.
- The microclimatic variables significantly influenced the leaf litter beetles fauna, being an important variable to be considered in the definition of strategies aimed at the recolonization by these organisms in areas undergoing restoration.
- From the less specific identification level (family) it was possible to differentiate the areas of native forest and pasture with nucleation techniques, allowing the application for bioindicator analyses.
- The Serra do Itajaí National Park (SINP) has a representative diversity of leaf litter beetles fauna that were previously unknown. The results show the importance of SINP conservation and restoration actions.
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