Abiotic and anthropic factors predicting bryophyte assemblages in a humid enclave in Chapada do Araripe, Northeastern Brazil

Abstract

The structure and water availability in the understory of the humid forest of Chapada do Araripe, Northeastern Brazil, are very heterogeneous. This environment is affected by the mono-dominance of babassu palms (Attalea speciosa) and other forms of anthropogenic disturbance. The objective of this work was to examine the use of bryophytes as indirect bioindicators of environmental quality in this forest. Epiphytic bryophytes were collected in localities with distinct levels of babassu dominance and springs/streams. Additionally, proxies for anthropogenic disturbances, humidity and light conditions were evaluated. Functional groups and the species composition were investigated. Our results demonstrated that the region has a high level of environmental heterogeneity. Anthropogenic disturbance was the main driver shaping species composition and abiotic conditions mediated the effects on species. Sites with higher levels of disturbance and greater abundance of babassu palms and canopy opening further limited the distribution of species that require high levels of humidity and shade specialists and favored sun specialists and generalists compared to environments with greater water availability. Therefore, abiotic and anthropic factors are important to understanding the relationships between bryophyte ecology and the environment, helping to predict changes in these assemblages driven by changes in the environment.

Keywords:
enclave of Tropical forest; functional groups; indirect bioindicator; liverworts; microclimate; mosses; multivariate analysis.

Introduction

The structure and composition of tropical forests have been highly modified by human interventions through fragmentation, resource exploitation and uncontrolled land use (Western, 2001; Laurance et al., 2002). As such, anthropogenic disturbances serve as modulating agents in biological communities, interfering with environmental integrity and provoking changes, or even losses, of biodiversity (Tabarelli et al., 2010; Brancalion et al., 2013). In this scenario, the use of bioindicator organisms is a useful and complementary tool for understanding the effects of alterations on ecological systems and for subsidizing preventive measures for biodiversity conservation (Dale & Beyeler, 2001).

Due to their poikilohydric nature (i.e., their dependence on high external humidity conditions), bryophytes can serve as indicator organisms of environmental conditions in both direct (e.g., bio-accumulation; see Holt & Miller, 2011; Barbosa & Carvalho, 2016) or indirect manners and indicate alterations in the structural parameters of communities (Frahm & Gradstein, 1991; Karger et al., 2012). Bryophyte assemblages have been widely utilized as indirect bioindicators of environmental conditions in tropical forests, e.g., humidity of the air, temperature, altitudinal gradients, vegetation types and forest integrity (Costa, 1999; Frahm & Gradstein, 1991; Gradstein et al., 2001; Acebey et al., 2003; Costa & Lima, 2005; Karger et al., 2012; Santos et al., 2014; Batke et al., 2015).

Bryophytes have the principal characteristics of good bioindicators, as they are easily measured, have short life cycles, are sensitive to environmental alterations and respond in predictable manners to those alterations (Dale & Beyeler, 2001; Burger, 2006; Holt & Miller, 2011). Although bioindicators demonstrate certain limitations in terms of capturing the structural complexity of the systems being analyzed, they are often efficient for evaluating the niche assembly, driven by environmental filtering (Burger, 2006; Heink & Kowarik, 2010). In the case of bryophytes, abiotic factors related to humidity and light conditions are key modulators of the composition of species and functional groups (Mandl et al., 2009; Glime, 2017). Life forms are functional groups that respond well to humidity and light conditions (Bates, 1998). In humid tropical forests, for example, the flabellate and pendant forms are typical of shady environments, as the understory, while forms that maximize water storage, such as tufts and cushions, predominate in edge environments or open vegetation, where light incidence is more intense (Costa, 1999; Glime, 2018; Souza et al., 2020). Functional groups of light tolerance also respond to abiotic and anthropic factors because disturbances such as habitat fragmentation and habitat loss modify the natural conditions of forest remnants, for example, increasing the exposure to sunlight and high temperatures and decreasing the humidity, negatively affecting shade specialists (Alvarenga et al., 2009; 2010). In turn, depending on the degree of disturbance, sun specialist species may become dominant in lower strata such as the understory (Acebey et al., 2003). Hernández-Hernández et al. (2019) found that anthropogenic disturbances altered the expected patterns for bryophytes along an altitudinal gradient (e.g. loss of liverworts and perennial species). In recent decades, many ecological studies with bryophytes have analyzed anthropic or abiotic factors in isolation and most of them reported negative effects for the assemblages (Acebey et al., 2003; Alvarenga et al., 2010; Tavares et al., 2014; Peñaloza-Bojacá et al., 2017; Hernández-Hernández et al., 2019; Souza et al., 2020). However, it is known that the combination of abiotic factors can minimize (e.g. precipitation) or maximize (e.g. fire) the effects of anthropogenic disturbances on plant species (Laurance & Williamson, 2001; Rito et al., 2017). Evaluating the combined effect of factors contributes to the understanding of assembly rules in bryophyte assemblages and helps explain the species diversity patterns (Araújo et al., 2021).

In this context, to take advantage of the bioindicator properties of bryophytes, we evaluated the influence of local abiotic and anthropic factors over these plants in an ecological refuge area. The humid forest of the Chapada do Araripe Mountains (CAM), located in the southern portion of Ceará State, Northeastern Brazil, is extremely important because it is home to endemic and endangered taxa of animals (Silva et al., 2011) and vascular plants, which depend on the environmental quality (especially water availability) of the forest to survive. Despite this, the CAM is affected by several anthropic disturbances that indirectly alter the local abiotic conditions, especially humidity (due to the exploitation of water resources, e.g. establishment of plumbing systems in springs) and luminosity [e.g. increase in babassu palms (Attalea speciosa Mart. ex Spreng), with the opening of clearings]. Although efforts have been undertaken to conserve the CAM forests, and their biotas are formally protected by law (Lima & Bezerra, 2004), habitat quality monitoring has been insufficient and proactive plans for regional conservation and the protection of threatened species are still very necessary (Silva et al., 2011). Within that context, environmental characterization and the use of bioindicator species could contribute to diagnoses of environmental quality (Dale & Beyeler, 2001).

Considering the context into which the humid forests of the Chapada do Araripe are inserted and the potential use of bryophytes as bioindicators, the present study sought to determine: (1) the degree of environmental heterogeneity of the humid forests of the Chapada do Araripe (considering moisture availability, luminosity, the abundance of babassu palms and anthropogenic disturbances); (2) if the bryophyte diversity will be affected by that environmental heterogeneity; and (3) if species or functional groups of bryophytes can be used as bioindicators of environmental quality. Assuming that poikilohydric plants can be bioindicators, we predicted that the absence of water resources, the high abundance of babassu palms and high degrees of anthropogenic disturbance would modulate the floristic composition and functional groups of bryophytes to life forms and light tolerance.

Materials and methods

Study area

The present study was undertaken in a remnant area of humid forest (7°13’ - 7°24’ S and 39°28’ - 39°09’ W, between 600 and 950 m a.s.l.) within a mosaic of dry and savanna forests (e.g., Caatinga, Cerrado and Carrasco) situated in the northeastern region of the Chapada do Araripe Mountains (Ceará State, northeastern Brazil). The study was performed in 12 localities throughout the forest. The elevation of the sampling areas varied between 684 and 950 m a.s.l. The regional climate is hot and humid, with Austral summer rains [classified as Aw (A- Equatorial w- equatorial savanna with dry winter) according to the Koeppen-Geiger classification, Alvares et al., 2013]. Rainfall is seasonal, with an annual mean of 1,033 mm, with 80% of the precipitation concentrated into four months of the year (January through April - which characterizes the rainy season) (Melo-Júnior et al., 1996). The regional vegetation is classified as Semi-Deciduous Seasonal Forest (Veloso et al., 1991), and despite the seasonal nature of rainfall there, approximately 80% of the vegetation cover is maintained by springs and creeks and the humidity they provide (Melo-Júnior et al., 1996; Loiola et al., 2015). The humid forest studied was located within two legally constituted conservation areas: the Chapada do Araripe Environmental Protection Area (EPA) and the Araripe National Forest (FLONA). However, large areas around the forests are urbanized and used for tourism, pasture, agriculture and unrestricted exploitation of timber and non-timber plant resources (Lima & Bezerra, 2004; Esmeraldo et al., 2011; Silva et al., 2011; Silva-Neto, 2013; Linhares & Silva, 2015; Albuquerque et al., 2017). Additionally, the degradation of springs by channeling all of their waters, as well as diverting streams and rivers, has degraded or eliminated those vital resources in many locations (Silva et al., 2011). Concurrent with that water resource degradation has been the increasing dominance of babassu palms (Attalea speciosa Mart. ex Spreng) in the last 40 years (Almeida et al., 2016). The literature suggests that successive fires and the abandonment of degraded areas have resulted in increasing densities of that palm species (Fearnside, 1990; May et al., 1985; Mitja & Ferraz, 2001), contributing to the modification of the CAM landscape (Almeida et al., 2016). The babassu palm is, however, one of the principal species exploited by regional human populations to produce charcoal, animal feed and craft works, and its fruits are harvested as a food resource (Campos, 2013; Campos et al., 2015; Almeida et al., 2016).

Sampling

Based on previous visual observations of the structural heterogeneity of the forest concerning the occurrence of babassu palm trees and springs/streams that were perennial, redirected, or absent, it was possible to define the following environments (treatments): three localities with perennial water (presence of water - PW) and without babassu palms (absence babassu - AB); four with PW and the presence of babassu palms (PB); two without water (absence water - AW) and AB; three AW and PB. All of the sites were separated by at least 1.3 km. Three 10 × 10 m plots were established in each locality and between six and eight phorophytes within those plots were inventoried, totaling 20 phorophytes per locality (except the Valentim locality [PWAB], which demonstrated only a low occupation of bryophytes on tree trunks, so that only ten phorophytes were inventoried there). The plots were spatially close to the trails and springs/streams of water, when present. Also, all of the plots were separated by at least 100 m. Bryophytes were inventoried in the usual way, collecting small patches measuring approximately 5 x 5 cm along the whole phorophyte from the base up to a maximum of 2 m in height. It was done so that the diversity existing on the phorophyte could be captured. Each phorophyte was considered as a subsample to account for the occurrence (i.e. for bryophytes, the abundance) of the species in each plot.

To characterize the environments (Fig. 1), we measured the following abiotic factor proxies (indirect measures) in each plot: canopy opening (CO), as a proxy for light availability (using a digital camera with a fisheye lens and photographs captured between 07:00 and 08:00 in the morning); the proximity of springs/streams (note: the distance to water data was measured with the aid of a Garmin GPS, then was standardized (ranging) and applied to a formula: -1 to obtain the data in the opposite direction, that is, proximity to water. For the analyzes we used the data transformed into proximity to water - Prox_water) and elevation (Elevation), both as proxies of atmospheric humidity. Additionally, we measured proxies of anthropogenic disturbances related to the exploitation of natural resources, determining the distances from the center of each plot to the following nuclei of human activities: the nearest house (House); the nearest village (Village) (village = more than five houses included within a 200 m transect); nearest asphalt road (Road); and the closest city (City). Those proxies represent easily measurable variables, as direct measures are often not possible, and proxies have been successfully used to correlate anthropogenic disturbances with biodiversity alterations (Martorell & Peters, 2005; Ribeiro et al., 2015). That methodology considers that the greater the distance of any site from nuclei of human activities will result in lower levels of anthropic intervention in terms of the exploitation of natural resources (Hill et al., 2002; Laurance et al., 2002; Liley & Clarke, 2003; Martorell & Peters, 2005; Ribeiro-Neto et al., 2016). All proxies of anthropogenic disturbances were measured (in meters) using Land Sat 8 satellite images in the QGIS software version 2.14.16 (Quantum GIS Development Team, 2017). These distance measurements were then transformed to proximity to those nuclei. Additionally, the abundance of babassu palms (Babassu) per plot was also adopted as a proxy for disturbance, since degraded areas have a high density of this species and, consequently, they present more open canopy, which changes the microclimatic conditions of the understory (Mitja & Ferraz, 2001; Cintra et al., 2005; Almeida et al., 2016).

Fig. 1.
Environmental characterization of localities. Environmental data was transformed by ranging (0 - 1) and categorized for each study locality in terms of the following conditions: the absence of water and babassu palms (AWAB); the presence of water and the absence of babassu palms (PWAB); the presence of water and babassu palms (PWPB); the absence of water and the presence of babassu palms (AWPB). The symbols represent the treatment localities. In AWAB: Grota Flores -FL (triangle) and Grota Forquilha-FO (inverted triangle). In PWAB: Valentim-VA (circle), RPPN- Soldadinho do Araripe-RP (square) and Fonte São Joaquim-SJ (lozenge). In PWPB: Granjeiro-GR (circle), Levada da Preguiça-LP (square), Riacho do Meio-RI (triangle) and Santa Rita-ST (inverted triangle). In AWPB: Ladeira da Macaúba-LM (circle), Passárgada-PA (square) and Linha de Transmissão-LI (lozenge).

Data processing

The techniques used for the preservation of the botanical material followed Yano (1984). The identifications of the specimens were based principally on Buck (1998), Gradstein & Costa (2003), Gradstein & Ilkiu-Borges (2009) and Sharp et al. (1994). The community parameters adopted for comparing the treatments were: functional groups (life forms and groups according to their light tolerance) and species composition. The methodology described in Batista et al. (2018) was used to classify the functional groups of the species in terms of their life forms: turf (turf = dense colony), mat, weft and fan, according to Bates (1998), in addition to sparse turf colonies (when the individuals were sparse/spatially separated from the colony). According to Gimingham & Birse (1957), and considering Bates (1998), life-form responses to decreasing levels of humidity (desiccation), from the most tolerant to the most vulnerable, are turf, sparse turf, mat, weft and fan. The light tolerant groups were based on the classifications of Costa (1999), Gradstein (1992) and Richards (1954), considering them to be: shade species, sun species, or generalists. All collections were deposited in the bryophyte collection of the UFP herbarium (Tab. 1).

Data analysis

To identify the environmental heterogeneity of the study localities, all of the data in the environmental matrix was standardized (ranging) and analyzed using Principal Component Analysis (PCA) run on Fitopac 2.1 software (Shepherd, 2010). The species frequency in the phorophytes was used as a proxy for abundance in the ordination analysis. The floristic matrix contained data related to the abundance of the species (descriptors) in the different plots of each of the localities (samples). Rare species (with only one occurrence) were removed from the sample set of the matrix, totaling seven excluded taxa. The floristic matrix was first submitted to analysis of outliers, with a level 2.0 cut in the PCOrd 4.1 program (McCune & Mefford, 1999); a plot with a standard deviation >2.5 was excluded (Valentim = 2.66) as it contained only a single species. The floristic matrix was submitted to Detrended Correspondence Analysis - DCA (Hill & Gauch, 1980) using PCOrd software (McCune & Mefford, 1999). That analysis allowed the determination of the size of the gradient along the first axis and demonstrated that the floristic data was unimodal (gradient >2 standard deviation units, gradient size = 2.95). For that reason, Correspondence Analysis (CA) was used to visualize the variations in the floristic compositions of the plots about the treatments adopted.

We also tested the correlation between floristic dissimilarity and geographic distance, environmental dissimilarity (CO, Prox_water and Elevation) and anthropogenic disturbances (proxies: Babassu palms, House, Village, Road and City). Those matrices were correlated using the Mantel Test, with 999 permutations, using Fitopac 2.1 software (Shepherd, 2010). The null hypothesis was that there was no linear correlation between the two distance matrices (Legendre & Legendre, 1998). In the floristic matrix, the localities were considered samples and the occurrences of bryophytes in the plots were considered indicative of abundance. The floristic distance matrix was calculated using the Bray-Curtis dissimilarity index. The environmental and disturbance matrices were calculated using simple Euclidian distances and the geographic matrix was calculated using geographic distances. According to our working hypothesis, it was expected that species compositions would be correlated with environmental conditions (environmental matrix and disturbance matrix) and that geographic distances would not influence floristic composition.

Canonic Correspondence Analysis (CCA) was adopted to determine which environmental factors structured species composition, using Fitopac 2.1 software (Shepherd, 2010). For that analysis, the proxies of distance (proximity) to the nuclei of human activities were combined using Principal Components Analysis - PCA using Fitopac 2.1 software (Shepherd, 2010), to generate the index of anthropogenic disturbance; that is to say that however closer a nucleus of human activity was, the greater would be its disturbance. The value of the index for each plot corresponded to the values of the scores of the first PCA axis, following the methodologies described by Martorell & Peters (2005). Before using the CCA, the environmental matrix (which contained the disturbance index and the other environmental variables) was transformed (ranging). The variable "elevation" demonstrated a correlation of 0.77 with the disturbance index and was excluded from that analysis for that reason (i.e., the highest elevation plots were farther from the nuclei of human activities and would therefore be less disturbed). The Monte Carlo test, with 1000 permutations, was used to demonstrate the significance of the first two ordination axes.

Indicator Species Analysis - ISA (Dufrêne & Legendre, 1997) run on the PCOrd program (McCune & Mefford, 1999) was used to define environmental quality indicator species based on the treatments utilized (four groups). The species frequency in the phorophytes was used as a proxy for abundance. The significances of the indicator values (IndVal) of the species were tested using the Monte Carlo test, with 1000 permutations, examining the null hypothesis that the species would not have any indicator value. We considered indicator species with indicator values (IndVal) ≥ 50 (p ≤ 0.05). The raw data resulting from this work are available in Batista et al. (2024).

Results

What are the degrees of environmental heterogeneity in the areas?

The PCA demonstrated an accumulated variance of 70.21% on the first two axes (Fig. 2). The first axis was strongly correlated with the distances from human activity, demonstrating a high correlation with the distances to villages (0.95), roads (0.93) and houses (0.89), as well as elevation (-0.85) and the abundance of babassu palms (-0.70). As such, the main environmental gradient in the study sites was anthropogenic disturbance. The localities with lower degrees of anthropogenic disturbances were located in the left-hand quadrants (principally the treatment AWAB and part of the treatment PWAB, i.e., areas without babassu palms), and on the right side, those in closer proximity to nuclei of human activities. The second axis of the PCA was positively correlated with the proximity of springs/streams (0.79) and positively negatively with canopy opening (-0.77), followed by babassu palms abundance (-0.38), including the localities of the treatments PWAB and PWPB, represented in the upper quadrant of the PCA. The PCA of the combined proximity proxies from the nuclei of human activity demonstrated an accumulated variance of 85% in the first two axes (see ^{Figure S1}). The anthropogenic disturbance index (AD), generated in the scores of axis 1, demonstrated that the localities of treatment AWAB were the least disturbed in terms of those factors, while the localities of treatment PWPB showed the highest values of that index.

Fig. 2.
Environmental heterogeneity of localities. Diagram of the ordination of the first two axes of the Principal Components Analysis (PCA). The colors denote the treatments: PWAB (red), AWAB (blue), PWPB (light green) and AWPB (dark green). The symbols represent the treatment localities. The variables adopted were: elevation (Elevation), proximity to streams/springs (Prox_water), canopy opening (CO) and abundance of babassu palms (Babassu palms). The proxies of disturbance were: proximity to a house (House), village (Village), road (Road), or city (City).

Are bryophytes affected by environmental heterogeneity?

A total of 41 epiphytic bryophyte taxa were encountered (Tab. 1) on the 230 phorophytes inventoried including liverworts (18 spp.) and mosses (23 spp. and one variety). In terms of life forms, all treatments demonstrated a predominance of life forms more tolerant to desiccation (turf, sparse turf) and intermediate conditions (mat and weft). The fan form (which is more vulnerable) was restricted to treatments without babassu palms (Fig. 3, for more details, see ^{Figure S2}). Concerning light tolerance, the generalist species and light tolerant species occurred in all localities, while shade species were generally located in localities without babassu palms, except for the PWPB treatment. It is important to note that shade-requiring species were not encountered in any treatments with babassu palms and without watercourses (AWPB), which present lower environmental quality (Fig. 3).

Fig. 3.
Localization of the humid forests in Chapada do Araripe, Ceará State, Brazil, and distribution of bryophytes. Colors denote the treatments: PWAB (red), AWAB (blue), AWPB (dark green) and PWPB (light green). The parameters observed in each locality and for each treatment were: effective species richness (Species richness); percentage relation to the light-tolerance groups: generalist species (Gen), typical of sunlight (Sun) and typical of shade (Shade); and the quantities of colonies of each life form: turf, sparse turf, mat, weft and fan.

Concerning floristic composition, the CA demonstrated an accumulated variance of 28.34% on the first two axes, without the formation of cohesive and isolated groups among the treatments (Fig. 4). A gradient of species composition was observed along the first axis (14.49%), where the localities without babassu palms (in blue and red) predominated in the left-hand quadrants, while those with palm trees appeared on the right-hand side. The shade species Fissidens pallidinervis Mitt. and Plagiochila raddiana Lindenb. appeared only in treatment AWAB (blue) together with various exclusive species (Tab.1).

Fig. 4.
Floristic composition of the epiphytic bryophytes. Biplot of the first two axes of the ordination diagram of Correspondence Analysis (CA). Colors denote the treatments: PWAB (red), AWAB (blue), AWPB (dark green) and PWPB (light green), and the symbols represent the treatment localities. To the full name of the species and their groups of tolerance to luminosity, see supplementary information.

Table 1.
Species recorded in rainforest localities (Localities) in the Chapada do Araripe. In the municipality of Crato: RPPN- Soldadinho da Araripe (RP); Levada da Preguiça (LP); Passárgada (PA); and Granjeiro (GR). In Barbalha: Ladeira da Macaúba (LM); Riacho do Meio (RI); Santa Rita (ST); Linha de Transmissão (LI); Fonte São Joaquim (SJ); Grota das Flores (FL); Grota Forquilha (FO). In Missão Velha: Valentim (VA). Light tolerant groups: generalist species (Gen), sun species (Sun), and shade species (Shade). * = species with rare distributions. Vouchers correspond to the accession number of the UFP collection.

Species	Light tolerance groups	Localities in the Chapada do Araripe	Voucher
Marchantiophyta
Cheilolejeunea rigidula (Nees ex Mont.) R. M. Schust.	Gen	RP/LP/LM/LI	85032c
Cololejeunea camillii (Lehm.) A. Evans	Gen	RP/GR/FO	84851b
Cololejeunea contractiloba A. Evans	Gen	RP/LP/PA/RI/ST/VA	84901g
Cylindrocolea rhizantha (Mont.) R. M. Schust.*	Shade	SJ	85024d
Frullania dusenii Steph.	Sun	LP/FO	85040d
Frullania ericoides (Nees) Mont.	Sun	All	84916a
Frullania kunzei (Lehm. & Lindenb.) Lehm. & Lindenb.	Sun	FL/RI	85011b
Frullania platycalyx Herzog	Sun	LM/LI	84932
Lejeunea flava (Sw.) Nees*	Gen	FL	84999f
Lejeunea glaucescens Gottsche *	Gen	LP	85037c
Lejeunea phyllobola Nees & Mont.	Gen	RP/LP/PA/RI/SJ/FL/FO/VA	85042a
Microlejeunea bullata (Taylor) Steph.	Gen	RP/LP/PA/GR/LM/RI/ST/SJ/FO	85012c
Microlejeunea epiphylla Bischl.	Sun	RI/LI	85063c
Cololejeunea trachyphyllum Reimers*	Shade	FL	84995e
Myriocoleopsis minutissima (Sm) R.L.Zhu, Y.Yu & Pócs	Gen	RP/LP/ST	85032b
Plagiochila raddiana Lindenb.	Shade	RP/FO	84983c
Pycnolejeunea contigua (Nees) Grolle	Sun	RP/LP/GR/ST/FO	84909b
Schiffneriolejeunea polycarpa (Nees) Gradst.	Sun	LP/LI/SJ/FL/FO	84990b
Bryophyta
Calymperes afzelii Sw.	Gen	RP/FO	84973d
Brittonodoxa subpinnata (Brid.) W.R. Buck, P.E.A.S.Câmara & Carv.-Silva	Gen	RP/LP/PA/GR/FL/FO	84974b
Bryum capillare Hedw.	Gen	RI	84931g
Calymperes palisotii Schwägr.	Gen	SJ/PA	84885e
Donnellia commutata (Müll. Hal.) W. R. Buck	Gen	RI/PA	84928d
Entodontopsis leucostega (Brid.) W. R. Buck & Ireland	Gen	RP/LP/PA/GR/LM/ST/LI/SJ/VA	84898a
Erpodium coronatum (Hook. & Wilson.) Mitt.	Gen	LP/ST	84960c
Fabronia ciliaris (Brid.) Brid. subsp. ciliaris	Gen	RP/LP/PA/GR/LM/LI/SJ/VA	84909d
Fabronia ciliaris var. polycarpa (Hook.) W.R. Buck	Gen	PA/RI/ST/LI	84914b
Fabronia macroblepharis Schwägr.*	Sun	ST	87081a
Fissidens brevipes Besch.*	Gen	PA	84893c
Fissidens elegans Brid.	Gen	RP/PA/RI/SJ/FL/FO	84919a
Fissidens gardneri Mitt.*	Shade	GR	84919a
Fissidens pallidinervis Mitt.	Shade	FO	84981a
Fissidens radicans Mont.*	Gen	VA	85054c
Isopterygium tenerum (Sw.) Mitt.	Gen	RP	87084a
Jaegerina scariosa (Lorentz) Arzeni	Gen	FL/FO	84978d
Microcalpe subsimplex (Hedw.) W.R. Buck	Gen	RP/LP/GR/RI/ST/SJ/FL/FO	85034a
Ochrobryum gardneri (Müll. Hal.) Mitt.	Sun	FL/FO/SJ	84866c
Octoblepharum albidum Hedw.	Gen	All	84902b
Stereophyllum radiculosum (Hook.) Mitt.	Gen	PA/GR/SJ/FL/VA	85053
Syrrhopodon ligulatus Mont.*	Shade	FL	84992f
Syrrhopodon parasiticus (Brid.) Paris	Sun	FL	84999e
Vitalia galipensis (Müll. Hal.) P.E.A.S.Câmara, Carv.-Silva & W.R. Buck	Gen	LI/LM	85060a

The Mantel Test confirmed our working hypothesis, indicating a positive correlation between floristic dissimilarity and the levels of anthropogenic disturbance (rM= 0.79, p=0.003) and between environmental and floristic distances (rM= 0.46, p= 0.01). There were, however, no correlations between geographic and floristic distances (rM= 0.25 p= 0.07). CCA demonstrated a low accumulated variance in the first two axes (axis 1 = 19.13% of the total variance; and axis 2 = 4.45%). The Monte Carlo test was significant, however, for those axes (p < 0.01). In the ordination diagram, the treatments generally formed cohesive, although not well-isolated groups. The main environmental gradient that affected species composition was disturbance (AD), which demonstrated a 0.98 correlation with axis 1, followed by babassu palm abundance (0.55). The localities with the greatest levels of disturbance were also associated with the greatest abundances of babassu palms, those being positioned to the right of the CCA (Fig. 5). Axis 2 was correlated with the humidity gradient, associated with proximity to springs/streams (0.79), separating the localities with the higher disturbance index values and the presence of babassu palms in the lower right quadrant and the localities near springs/streams in the upper quadrants (Fig. 5).

Fig. 5.
Environmental filters determining species composition. Ordination diagram of the first two axes of the Canonic Correspondence Analysis (CCA). Colors denote the treatments: PWAB (red), AWAB (blue), AWPB (dark green), PWPB (light green), while symbols denote the localities of the treatments. The variables adopted were elevation (Elevation), proximity to streams/springs (Prox_water), canopy opening (CO), abundance of babassu palms (Babassu palms) and anthropogenic disturbance index (AD).

The analysis of indicator species showed that most of the species demonstrated low fidelity and specificity concerning the treatments. Only four species, Schiffneriolejeunea polycarpa Nees Gradst. (IndVal = 93.8), Brittonodoxa subpinnata (Brid.) W.R. Buck, P.E.A.S.Câmara & Carv.-Silva (77.0), Lejeunea phyllobola Nees & Mont. (72.9) and Jaegerina scariosa (Lorentz) Arzeni (66.7), had IndVal ≥ 50 and were indicators of the AWAB treatment (which represents the lowest degree of anthropogenic disturbance according to the PCA).

Discussion

What is the environmental heterogeneity of the area?

The treatments with babassu palms were associated with greater canopy opening and proximity to nuclei of human activities. In addition to the factors of anthropogenic disturbance associated with the use of babassu palms in the Chapada do Araripe (which results in greater direct human intervention in the forest), the abundance of that palm interferes with the microclimate of the sub-canopy. It has been widely demonstrated that palm trees contribute to greater light penetration into the sub-canopy due to the innate structures of those plants (Cintra et al., 2005; Raupp, 2010). In addition to greater light penetration, it was observed that the babassu palms in the study region had negative impacts on the sub-canopy due to the shedding of their large leaves, contributing to the alterations of the micro-environments available for bryophyte colonization. It is important to note that babassu palms are associated with localities that have suffered anthropogenic disturbances, such as abandoned pastures and burned areas (Gehring et al., 2011; Campos et al., 2015). As such, localities with babassu palms and the presence of water are common near urban areas, principally because of the extraction of those two resources.

The localities without water and babassu palms (AWAB) are less disturbed. Additionally, those localities are found on the plateau area of the CAM within the FLONA-Araripe environmental protection area and at higher elevations - which makes access by human populations more difficult; those localities are also subject to environmental monitoring. Despite the absence of streams and other sources of running water in those localities, their greater elevation acts to supply them with more atmospheric humidity (Körner, 2007) - a difficult variable to measure, but extremely important for poikilohydric plants. As such, it was confirmed that the environmental heterogeneity encountered in the humid forest, with localities apt for the maintenance of bryophyte diversity, was also subject to anthropogenic disturbances.

Are bryophytes affected by environmental heterogeneity?

In general, the analyzed aspects of the bryophyte assemblage demonstrate that sites distant from springs/streams, with a high abundance of babassu palms, greater canopy opening and greater proximity to nuclei of human activities affect the distribution of species. These factors can lead to an increasing generalist bryoflora concerning light tolerance and life forms (e.g. mat), particularly affecting shade-specialist species which have higher requirements regarding humidity. This is especially so in places where babassu palms are present because these trees are associated with altered light conditions inside the forest (greater canopy opening and, consequently, greater evaporation of water in the air). However, the effects of a monodominant forest of babassu palms can be minimized through the provision of water, which is confirmed by the occurrence of shade species in such conditions (PWPB). In terms of floristic composition, many bryophyte species were found to be shared between the treatments and the localities (a fact emphasized by the low number of indicator species). According to Batista et al. (2018), most bryophyte species found in the Chapada do Araripe show wide distributions in Brazilian phytogeographical domains, that is, they are generalists as to habitat conditions. Nonetheless, the AWAB localities (FL and FO) on the Chapada do Araripe plateau are more floristically distinct and harbor indicator species and species with restricted distributions (e.g. Micropterygium trachyphyllum Reimers). It is important to note that the species classified as indicators in the present work have wide distributions in tropical forests and savannas in Brazil (Batista et al., 2018). Nonetheless, it was evident that these species preferred areas with lower levels of human intervention in the Chapada do Araripe, as well as higher elevations (a proxy for atmospheric humidity). Such localities provided the best conditions for the survival of bryophyte species, resulting in greater richness of species, including exclusive ones, also greater functional group diversity (fan and weft type colonies) including species shade requirements (see Supplementary material).

Despite not being a cohesive group, the localities without water resources and with babassu palms (i.e., with low environmental quality) had similar floristic compositions, with representatives of sun tolerant (Frullania platycalyx Herzog and Microlejeunea epiphylla Bischl) and generalist species (Cheilolejeunea rigidula Nees ex Mont.) R. M. Schust). These liverworts have oil bodies (= volatile terpenoids contained within a membrane) within their cells that represent functional adaptations for tolerating high solar radiation levels and desiccation (Gradstein, 1978), suggesting resistance to stress conditions. Another important characteristic of species from this environment is the presence of specialized structures for water storage, such as lobules (i.e. water-accumulating leaf folds) in liverworts and wing cells in mosses (e.g., in the species Vitalia galipensis (Müll. Hal.) P.E.A.S.Câmara, Carv.-Silva & W.R. Buck).

Although most species are shared between the treatments, the geographic distances between localities were not found to be a determinant factor of their floristic compositions, but rather the similarities of their environmental conditions, especially the degree of anthropogenic disturbance. It is known that the floristic composition of bryophyte assemblages is associated with environmental determinism, whether at small scales, along vertical gradients (Costa, 1999; Oliveira & Steege, 2015), or at larger scales such as along altitudinal or horizontal gradients (Frahm & Gradstein, 1991; Santos et al., 2014; Amorim et al., 2017; Araújo et al., 2021). In the present study, we found that anthropogenic disturbances are the main driver of variation in species composition at the local level. It is also worth noting that the combination with other abiotic factors can minimize or intensify anthropic effects (Rito et al., 2017). Thus, even if the sites are subjected to similar levels of anthropogenic disturbance, water availability appears to minimize such effects. In turn, greater canopy opening combined with the abundance of babassu palms appears to intensify the effects on bryophyte species. Therefore, it is important to consider anthropic and abiotic factors in the ecology of bryophyte assemblages. Investigations of the effects of acute and chronic anthropogenic disturbances on bryophytes have confirmed their negative effects on the diversity of species and functional groups (e.g. loss of shade specialists), change in species composition principally due to the loss of environmental integrity (Costa, 1999; Zartman, 2003; Alvarenga & Pôrto, 2007; Tavares et al., 2014; Peñaloza-Bojacá et al., 2017). Therefore, the findings suggest that bryophytes can be used as environmental indicators at the local level, as the parameters of the assemblages analyzed here vary according to environmental heterogeneity. Changes that trigger biotic homogenization can compromise the conservation of biodiversity and the role that these species play in the environment. Future investigations should take into account the various types of anthropogenic disturbances and abiotic conditions that can act synergistically on plant species composition. In addition to the species composition, it is still worth exploring the functional composition of these species and the ecological strategies they adopt in the face of a changing world.

Acknowledgments

The present study represents part of the Master’s Degree dissertation of the first author, which was undertaken within the Programa de Pós-Graduação em Biologia Vegetal of Universidade Federal de Pernambuco, Brazil

. The authors thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brazil (CAPES) - Finance Code 001 for the grant awarded to the first author; also the nongovernmental organization IdeaWild (EUA) for donating field equipment and representatives of the Associação de Pesquisa e Conservação dos Ecossistemas Aquáticos (Aquasis) for their invaluable support during the field excursions, especially the team working on the conservation project of the threatened bird Araripe manakin.

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• Data availability
  All the data supporting the results of this study have been made available on SciELO Data and can be accessed at DOI: https://doi.org/10.48331/scielodata.XITNUZ.

Supplementary material

Figure S1. Ordination graph of the Principal Components Analysis (PCA) with anthropogenic disturbance variables. The variation in the first axis reflects the anthropogenic disturbance index values. Figure S2. Richness and percentage of species and functional groups of bryophytes by locality.

Edited by

• Editor Chef:
  Thais Almeida

• Associate Editor:
  Alexandre Salino

Data availability

All the data supporting the results of this study have been made available on SciELO Data and can be accessed at DOI: https://doi.org/10.48331/scielodata.XITNUZ.

Publication Dates

• Publication in this collection
  20 Dec 2024
• Date of issue
  2024

History

• Received
  29 Jan 2024
• Accepted
  10 Sept 2024