Site description

The study was carried out in the Guapi-Macacu Basin in the state of Rio de Janeiro, located east of Guanabara Bay. The predominant climate in the region is Af tropical wet according to the Köppen classification. The average precipitation varies between 1,300 and 2,200 mm and the temperature between 14 and 27°C, presenting an average of 21.1°C [48]. The vegetation of the region is Dense Ombrophilous Lowland Forest included in the Atlantic Forest (sensu stricto) [49]. The forest cover of the basin occupies 42.4% of the territory and is divided into larger and continuous fragments in areas of higher elevation, while hills and hillocks are located in the lowlands with smaller and more dispersed forests in the landscape [48].

The study was developed in 14 forest fragments dispersed in the Basin, with an environment predominantly consisting of agriculture and livestock. The fragments were selected in four size ranges: 4 small fragments (< 15 ha), 4 medium fragments (> 19 < 30 ha), 3 large fragments (> 90 < 200 ha) and 3 segments of continuous forests (> 40,000 ha) belonging to the Parque Estadual dos Três Picos forest. Continuous forest segments were used to control fragmentation effects. The Atlantic Forest fragments selected for this study have been fragmented for at least 18 years, and their selection followed some criteria such as the native vegetation structure (given by stratification, tree size and life forms), management and usage history. There has been a great effort in identifying fragments of similar structure and with similar dynamics of use in their surroundings in the last ten years.

The fragments are surrounded by different soil uses, predominantly pastures and crops (43.6% and 4.8% of the territory, respectively) (Fig 1). Agriculture herein will be treated as intensive crop, with high use of agricultural inputs and soil tillage, and pastures.

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Fig 1. Location of the studied fragments and land use classes in the Guapi-Macacu River Basin, Rio de Janeiro, Brazil.

https://doi.org/10.1371/journal.pone.0212725.g001

All the forest fragments used in this research work were located in private properties. All the owners were contacted and gave permission for the researchers involved in this work to enter and to collect data prior to the field collections. No specific permits from local authorities were necessary because there was no need for tree cutting or intervention to any endangered or protected species.

Intensive use areas are characterized by annual corn (Zea mays) rotations with manioc cultivation (Manihot esculenta), with high frequency of soil rotation through plowing followed by harvesting and use of fertilizers and lime. An average of 2000 kg.ha^-1 lime and 60 kg^-1 of 4-14-8 NPK fertilizer are added for the corn cultivation. Some proprietors use organic compost (manure) applied as cover as a complement to chemical fertilization. Agrochemicals are also frequently used to control pests such as caterpillars (Spodoptera frugiperda). After this, new plowing and harrowing is carried out for planting the manioc roots, without new chemical fertilization. Management activities are almost non-existent in pasture areas (Brachiaria brizantha), with only general grazing occurring. The maximum stocking density of cattle is on average 1 head.ha^-1.

The criteria described by Laurance et al. (2002) [50] were adopted as references to evaluate the effect of the soil use on the native vegetation areas. These authors establish that the anthropic area of the environment must have a minimum size of 100 m in length and the same area of width in contact with the fragment edge.

Sampling design

Six fragments were evaluated for an adequate evaluation of the established questions, with an agricultural percentage in their perimeter being zero, and 5 fragments and 3 areas of continuous forest (part of the Parque Estadual dos Três Picos) with a variable percentage in their perimeter surrounded by agriculture covering all size classes of the selected fragments. All the matrices classified as intensive crops have a continuous usage history for at least 10 years.

The selected forest fragments are characterized by a sloping hillside relief, typically uphill from the edge of the forest toward the interior, and thus three different strata were established for sampling, with the sole objective of sampling the differences in slope and distances from the edge of the fragment to the production areas. The fragments were stratified as follows: i) 1^st third—area closer to the agroecosystem, which has greater anthropic influence; ii) 2^nd third–the area next to the 1^st third, generally with great slope; iii) Final third—top hill region, with lower slopes. Three plots of 50 x 5 m (250 m²) were allocated in each third, which totals an area of 2,250 m² per fragment. The plots were systematically delimited in each stratum, parallel to the agroecosystem, with 10 meters of distance between them in the horizontal direction (parallel to the edge) and 10 meters in the vertical direction (perpendicular to the edge and towards the inside). Three plots were also allocated in the surrounding agricultural areas for soil sampling, following the same methodology for allocating the plots within the fragments.

Floristic and phytosociological survey

A forest inventory was carried out in March 2016 with assistance from a botanist. All individual trees with diameter at breast height (DBH) greater than or equal to 5 cm were measured and identified in all the plots. When possible, the identification was carried out in the field and, when necessary, botanical material collections were carried out for further identification. The taxonomic determinations were carried out by consulting the Herbariums of the Research Institute of the Botanical Garden of Rio de Janeiro and the Department of Botany (RBR) of UFRRJ (Federal Rural University of Rio de Janeiro), by bibliography, or by specialists. Part of the floristic survey had already been carried out in a previous study [29] using the same methodology. These data were also collected for conducting this work.

The species were classified into two functional groups according to Swaine and Whitmore [46]: pioneer or heliophilous species, which require direct light for seed germination, or those generally classified as pioneers and early secondary; and the group of non-pioneer/late successional or sciophilous species which can germinate and develop under the shade, being found under the canopy and also in open environments [51]. Studies for the state of Rio de Janeiro were used for these classifications in order to avoid variations in classifications [51–55]. Non-classified species (NC), did not fall into any of the categories due to lack of information.

The calculations of the community phytosociological parameters were performed according to Mueller-Dombois & Ellenberg [56] by calculating the absolute and relative parameters of species density, dominance and frequency in order to obtain the Importance Value (IV) of each species, which consists of the sum of the relative values mentioned above (S1 Table).

Soil fertility and granulometry

Simple soil (different amounts of soil taken at different points within the plot areas) samples were collected between February and March 2016 in order to analyze the relationship between abundance and richness of functional groups of tree species and the soil fertility characteristics of the forest fragments. Three soil samples were collected per plot at a depth of 0–5 cm with the aid of a metal probe. Samples were collected at the ends (0; 50 m) and center (25 m) of each plot, forming a sample composed of soil for each plot. Each composite sample was placed in a plastic bag and identified for transport to the laboratory, where each soil sample was air dried. After drying, they were sieved using an 8 mm sieve to remove coarse material. The samples were sent for chemical analysis in the Nutrient Cycle Laboratory of EMBRAPA Agrobiology, which follows the methods recommended by EMBRAPA [57]. The chemical characteristics analyzed were pH in water, calcium (cmolc.dm^-3), magnesium (cmolc.dm^-3), potassium (mg.L^-1), phosphorus (mg.L^-1), carbon (dag.Kg^-1) and nitrogen (dag.Kg^-1). The granulometric analysis of the samples was carried out at the Soil Physics Laboratory of the UFRRJ Soils Department, using the Pipette Method [57], quantifying the sand, silt and clay fractions expressed as percentage.

Canopy opening

Hemispheric photographs were taken for estimating the canopy cover of each fragment, from which it was possible to indirectly calculate the canopy cover and light input in the plots [58]. The photographs were taken at the ends (0; 50 m) and center (25 m) of each plot using a digital camera attached to a ‘fish eye’ lens positioned at a distance of 1.5 m from the ground using a tripod. The tripod was always positioned to the north with the help of a compass in order to maintain standardization of the photographs. Afterwards, each photo was analyzed with the purpose to quantify white (the points related to the open sky) and black (referring to the vegetation) pixels, which was performed using the Gap Light Analyzer (GLA), Version 2.0 program [59]. Analysis of the photographs enabled an estimation for each plot for the canopy opening, direct light input and diffuse light. Direct light input was used as a measure of canopy opening for the statistical analysis of the present study due to the high correlation of these parameters.

Slope

The central point in each plot (25 m) was measured with the aid of a digital clinometer for evaluating the terrain slope.

Obtaining and evaluating landscape indexes

In order to understand the relationships between the structural variables of the landscape and the tree community composition in the fragments, landscape metrics were used according to the procedures used in Uzêda et al. [29]. The following measures were used: area, which refers to the fragment size; perimeter/area ratio (PARA), which is an indicator of the fragment shape, and therefore related to the amount of existing border; and Euclidean distance of the nearest neighbor (ENN), which is an indicator of fragment isolation. The agricultural border percentage (agri) was also obtained, which is an indicator of the border perimeter percentage of the forest fragment which is directly in contact with the agricultural area. All types of land use along the fragment perimeter that made direct contact with its border which were delimited in the map and coverage used were considered for this calculation.

The land use and coverage map of the Guapi-Macacu and Caceribu river basins on a scale of 1:50.000 [60] was used to identify the areas under natural vegetation cover in the study area. This map was elaborated based on the image classification of the TM-Landsat 5 sensor, from June to August 2007, with a resolution of 30 meters. The original map was recorded to the boundary of the Guapi-Macacu basin area, and the selected natural vegetation sites were extracted: forest in initial, middle and advanced stages of regeneration. The fragment data were spatialized in digital format (“raster”) with a resolution of 30 meters, and the Fragstats program was used [61] for calculating landscape metrics.

Next, the proportion of the fragment boundaries to be found in line with the different types of land use was calculated. As the studied fragments are only surrounded by pasture and agriculture, and therefore the percentages of these two edge types total 100, it was decided to only use the border percentage with agriculture, thus avoiding highly correlated variables [29].

Data analysis

In order to identify the similarity of the structure and composition of the tree community among the fragments, non-metric multidimensional scaling (NMDS) with the Bray-Curtis similarity index [62] was used to verify clustering trends. Therefore, a matrix with the Importance Value (IV) of the species of each fragment (S2 Table) was used. NMDS construction was performed in the statistical R program using the “vegan” packages, version 2.3.0, and “labdsv” version 1.7.0 [63].

Generalized linear models (GLMs) were constructed and tested to identify the variables that best explain the functional groups’ abundance and richness pattern in the fragments. Therefore, in order to construct these predictive models, the richness and abundance of the ecological groups (pioneer and shade-tolerant) were considered as dependent variables and the levels of carbon, nitrogen, phosphorus, potassium, calcium and magnesium (C, N, K, Ca and Mg, respectively), clay percentage in the soil (Arg), border percentage with agriculture (lagri), Euclidean distance of the nearest neighbor (ENN), fragment size in hectares (area), perimeter-area ratio (PARA), canopy opening (abos) and slope as independent variables (S3 and S4 Tables). We used abundance of each species in each ecological group and average data of the independent variables in each stratum of each fragment as inputs. Next, 19 possible models were tested for the abundance of heliophytes and 28 models for the abundance of sciophytes in total. Then, 33 models were tested for the richness of heliophilous species, and 27 models for the richness of the sciophilous species (S5 Table).

Using Gaussian data distribution, the models were tested and selected through the second order Akaike criteria (AICc) generating a rank from the best to the worst model [64]. Models with ΔAICc values smaller than two (ΔAICc < 2) and of higher AICc weight (AICcWi) were selected. AICcWi is the selection probability of a given model in the cases of re-sampling the available data. Verifying the likelihood of the parameters to the selected models was performed by a chi-squared test (χ²). The analyses of the models were carried out in the R statistical software program [63] using the packages “bbmle”, version 1.0.16, and “MuMIn”, version 1.15.1.

Impacts of intensive agriculture on functional groups

The predictive model results point to a clear and direct influence of the intensive farming environment on the tree community in the forest fragments. This can be observed by the influence that the greater direct border percentage with agriculture areas has on the abundance of the functional groups. According to the models, the forest fragments with greater border extension focused on intensive corn and manioc cultivation are associated with greater pioneer species abundance and the lowest abundance of sciophilous species. Furthermore, there seems to be possible indirect impacts caused by the soil eutrophication inside the fragments, possibly due to the aerial drift of fine particles of the soil which are eventually deposited inside these fragments. Thus, the direct edge of a forest fragment with an intensive agriculture area has potential impact on the abundance and richness of the functional groups due to differences in interaction between functional groups and fertility levels. As indicated by the models, the heliophytes are benefited by calcium levels and disadvantaged by magnesium levels, while the sciophilous species are benefited by magnesium and are disadvantaged by the higher phosphorus levels.

Among the potential impacts from surrounding agricultural areas on the interior of the fragments, changes in soil fertility with increased nutrient levels have been widely discussed in the literature [23,28,29,65]. A recent work [29] showed a trend of soil eutrophication in forest fragments located in the same study area, with significant increases in calcium, phosphorus and potassium, while another similar study [65] observed that the higher the fertilizer application intensity in agricultural areas, the higher the nutrient content in nearby forest fragments. The frequent practices of liming and fertilizer use in conventional agriculture fields combined with soil tilling result in drift and transport of fine soil particles by air, which are deposited in soil fragments [28,29,65]. The result is a significant increase in nutrient levels in the soils of nearby forest fragments such as nitrogen [30,65], phosphorus [28,29], calcium and magnesium [23,29].

The relationship between the abundance and richness of early and late successional species and the increase in calcium, magnesium and phosphorus nutrient contents found in this study demonstrate that the enrichment of nutrients in the soils of these fragments by the practices implemented in their surroundings is a source of important impact in the tree community and which is still little recognized. This was observed in some studies that identified changes in the floristic composition of herbaceous leaves at the edges of fragments, possibly due to the large input of liming particles for soil acidity correction and the use of nitrogenous fertilizers, causing a dominance of common species in less acidic soils or of nitrophilous species [23,66–69].

Pioneer tree richness is clearly benefited by increased calcium content, while late successional species are negatively impacted by increased phosphorus content. These nutrients tend to increase in forest fragments near agriculture areas [23,29,65] due to the common practice of liming and use of phosphate fertilizers. In addition, phosphorus has low mobility in the soil, which can cause accumulation, and consequently lead to eutrophication of the system over time [29]. Although magnesium content has a positive relationship with the richness of sciophytes, the previous results found in this same study area [29] did not indicate significant increases of this nutrient in the fragments, which is the opposite of that found for calcium and phosphorus, as previously mentioned.

Thus, continuous additions of nutrients over long periods may have significant impacts on species composition of the forest community of forest fragments [37] close to conventional agricultural crops, altering the composition and structure of the functional groups of the tree community. Natural ecosystem plants are adapted to conditions with limited availability of nutrients, maintaining a certain balance of adjustment to local fertility characteristics [36,37]. Thus, soil fertility conditions in tropical forests limit plant growth and establishment, therefore constituting an important determinant of functional diversity on a local, landscape and regional scale [30,32,37].

Some recent long-term studies have investigated the primary productivity response of tropical rainforest trees to adding nutrients to the soil [37–41], demonstrating that even in soils relatively rich in exchangeable bases (K⁺, Ca²⁺, Mg²⁺ and Na⁺) and in nitrogen and phosphorus, some species and functional groups respond strongly to the addition of these elements and potassium. However, the impact in regions with lower fertility such as in the areas of this study may be more intense, since these regions tend to have more specialized flora when compared to regions with higher fertility, which have a greater number of fast-growing and more generalist tree species [32,37]. The literature demonstrates that fast-growing species are generally more abundant in naturally nutrient-poor soils [33,43]. This is because the availability of nutrients is not a limiting factor for pioneering and fast growing plants as their wood is low density, which does not require a high investment in nutrients [35,43]. Therefore, pioneer species seedlings are more efficient in nutrient consumption, being able to out-compete shade tolerant species in competitive environments [70].

Thus, constant deposition of nutrients in the forest fragment soils of this study may be creating a conducive environment for the proliferation of pioneer tree species. The fragments within the pasture environment showed the highest IV values for the sciophilous species (S1 Table), which helps to explain the observed grouping of these fragments in the ordering analysis. Thus, it is possible to observe that the pioneer or secondary heliophilous species may be benefiting in the fragments within an intensive agriculture environment, where the effects of nutrient drift are greater. When analyzing the two functional groups (heliophilous and sciophilous), it is possible to observe that fast growing pioneer species generally present higher rates of primary production in response to nutrient increase [4,70,71].

However, despite the influence of changes in soil fertility demonstrated in the results of our study, this variable does not solely explain the composition of the functional diversity in the fragments. The environment can affect the composition of the species in two ways: firstly by edge effects, which are more intense when the environmental matrix is agricultural, changing the chemical characteristics of the soil and creating direct impacts on the microclimate; and second, by factors that hinder the recruitment of late successional species by reducing propagule flow [4,14,72–74].

Agriculture areas may also impact shade tolerant species by influencing the connectivity between the fragments, as they may be a more hostile environment for the movement of pollinators and dispersers [14,75], reducing seed flows [74]. Changes in the number of individuals of some species due to decreased seed dispersal can cause local extinctions over time [74], making it difficult to maintain viable populations. In addition, more intensive use in agricultural areas may create unfavorable microclimatic conditions to the floristic community [76], and may contribute to the impact on the abundance of some shade tolerant species.

Other impacts on functional groups

The higher abundance of sciophilous species was dependent on the fragment size, being the only factor that positively influences the abundance of this group. On the other hand, the abundance of pioneer species is greater in smaller fragments, which is directly related to the fact that these smaller fragments are subject to greater intensity of edge effects [22,77]. The fragment size is not solely the main factor for tree species abundance. Its indirect effect is related to other associated factors such as edge effects, the characteristics of the landscape matrix and the isolation between the fragments [8,77,78].

The impact of abrupt edge creation by the fragmentation process for tree communities has been widely discussed, resulting in the elevation in mortality rates and changes in the recruitment dynamics of later successional trees at the edges of fragments [17,76,79], and even in the interior of small fragments [26], benefiting pioneer and generalist species [17,19].

Despite the significant effect on abundance, the species richness for the two functional groups was not affected by the fragment size. For richness, the soil characteristics (fertility levels and clay content), the canopy opening, the slope and isolation degree of the fragments are more important. Plant diversity is highly related to soil fertility and grain size characteristics [30,32,80], and these two factors are strongly correlated as previously discussed. A higher clay content in the soil allows more bonds, which provides greater nutrient availability [31,32]. Along these lines, flatter lands have a higher amount of clay coming from higher lands and deposited in these lower areas [31,32], which in turn also results in higher levels of soil fertility.

In addition to the influence on soil fertility, the slope of the terrain may make it difficult to maintain sciophilous species in two ways; firstly, because the recruitment of these species is difficult as they usually have large seeds which may present greater difficulties in establishment in very sloped areas; secondly, greater slope is associated with tree falling and mortality of large trees, since they present greater difficulty to remain fixed in these areas [32,43]. These situations explain the difficulty in maintaining the seedling recruitment of slow growing species, showing the positive influence of this factor on the abundance of pioneer species, and a negative relation with the abundance and also richness of sciophilous species.

The higher degree of isolation of the fragments did not influence the abundance of the species of the two ecological groups, but was one of the explanatory variables for the richness of late successional species, being more important than the fragment size [8,77]. As already discussed, this factor leads to reductions in seed flow, decreasing the chances of seed dispersal due to longer distances between fragments [4,72]. Initial successional species have an advantage in seed dispersion because they produce a greater quantity of seeds and generally their seeds are dispersed by wind or generalist animals [51]. On the other hand, late successional species generally produce larger seeds dispersed by specialist animals [15], making it harder for gene flows between more isolated fragments.

Finally, unlike what is expected, the larger canopy opening only had a negative influence on the richness of heliophilous species. This result differs from that expected, since greater abundance and diversity of light-loving species are expected for germination and growth in great clearings [34,81]. However, areas with larger canopy openings may have a lower species richness (even of heliophiles) due to different disturbances, regardless of soil fertility. This is also related to factors of the natural dynamics of succession in gaps, which may be totally different in small and large gaps. Even if there is a small opening created in the canopy from the falls of some trees or branches, regeneration will not necessarily be occupied by pioneer species [34].

The study sought to show the direct and indirect impacts of agriculture on the functional diversity of trees in forest fragments of the Atlantic Forest. In addition to the well-known edge effects, we tried to show that agricultural practices have an effect that has not yet been studied, such as changes in soil fertility of natural forest ecosystems and their implications on biodiversity. The use of an expressive number of forest fragments for comparing the intensive agriculture and pastures in the surroundings demonstrated that the conventional intensive agriculture can imply in a regression in the forest succession, either directly by the edge effects and alteration in soil fertility, and/or indirectly by the possible impact on the flows of dispersing and pollinating animals. However, as already shown, multiple factors negatively affect forest succession. In addition to the matrix effect, the fragmentation effects (size, isolation) and local variables (slope, canopy, clay content) cannot be ignored in this process [35].

Thus, forest fragments immersed in an agricultural matrix and exposed to conventional and intensive agriculture practices may be conditioned to a reduction in tree species diversity through the replacement of late successional species by pioneer species. Late successional species are responsible for most of the natural regeneration and the high diversity in mature tropical forests [19,36], and show a tendency to be restricted to areas with no edge effects reaching them, such as in interiors of large fragments and fragments with little isolation. Thus, the discussion of conservation in agricultural production landscapes should take into account that it is necessary to develop and encourage agricultural practices which are less impactful on biodiversity, in addition to the demand for maintaining large areas of natural remnants which is essential for some species. This is important to reduce the direct impacts caused by edge effects, such as the change in the fertility characteristics of the soils, and the impacts that the matrix quality can imply on the population flows between the fragments [22].