The study was carried out in the Catimbau National Park, a protected area covering about 62,000 ha of the Caatinga dry forest (Fig. 1). The climate is tropical semi-arid, with an average annual temperature of 23 °C and average annual rainfall ranging from 486 mm to 975 mm. The rainy season usually takes place between March and June, when the herbs grow and spread throughout the park, but some zones also receive rainfall earlier (January and February). Although the Catimbau National Park has been created in 2002 through a Federal Decree (without number) signed by president Fernando Henrique Cardoso in December 13 of that year, there are dozens of small landholdings within its borders, particularly small farms devoted to subsistence agriculture and livestock production (mostly goats) (Specht et al., 2019). Farmers depend on forest resources for food, energy and water security, such as firewood, fodder, and timber (Arnan et al., 2018; Specht et al., 2019). Consequently, this region has been converted into a vegetation mosaic consisting of old- and second-growth stands (i.e., regenerating forest stands), crops, and pastures (Souza et al., 2019). Goats, sheep, and other cattle roam freely across the park, feeding on the remaining vegetation (Alves et al., 2020). The woody stratum is dominated by Fabaceae, Euphorbiaceae, and Cactaceae families (Rito et al., 2017b) and cover a gradient of plant density and aboveground biomass (Souza et al., 2019). The herbaceous stratum is poorly known (Andrade et al., 2020; Menezes et al., 2021).

Fig. 1.

Location of the study area in the Catimbau National Park, Pernambuco State, northeast Brazil. Circles indicate 20 × 50 m plots where herb communities were sampled. The size of the circle is proportional to its level of chronic anthropogenic disturbance. Pixel color indicates the annual rainfall.

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We surveyed herb species in 19 0.1-ha permanent plots (20 m × 50 m) that were established ≥ 2 km from each other across the environmental gradients. These permanent plots were devoted to the study of the woody flora on previous studies (see Rito et al., 2017b for further details). In each plot we systematically established one subplot every 10 m along the imaginary line that split the plot longitudinally into two symmetric parts, totaling five subplots per plot and 95 subplots in the entire study. Because herb communities are transitory in the Caatinga, we conducted the surveys in three consecutive seasons – July 2015, January 2016 and April 2016 – to ensure high levels of sample completeness (0.92–1.00; see Appendix S1 for details). In each subplot, we counted all herbaceous plants (i.e. no sign of woody tissue) and collected for further species identification. Plants were identified at species level using analytical keys, specialized literature, consulting specialists, based on our own field experience (Queiroz et al., 2015; Andrade et al., 2020; Menezes et al., 2021), and through comparisons with material previously identified in master and PhD projects of our team. For the purposes of the analyses, we summed up the data from the three seasons and the five subplots into a single replicate and extracted key community descriptors at the plot level, such as herb density, species richness, and species composition. These metrics were used to describe the taxonomic responses of communities to the environmental gradients.

To identify the phylogenetic responses of herb communities to the environmental gradients, we took into account components of phylogenetic richness, divergence and structure of the communities (sensuTucker et al., 2017). After constructing a time-calibrated molecular phylogenetic tree (Fig. S1; see details of phylogeny construction in Appendix S2 and Table S1), we used the comstruct function of Phylocom 4.2 (Webb et al., 2011) to calculate complementary phylogenetic metrics based on abundance and presence/absence: mean phylogenetic distance (MPD), mean nearest taxon distance (MNTD), net relatedness index (NRI) and nearest taxon index (NTI). MPD estimates the mean distance between all pairs of species or individuals (if weighted by abundance) while MNTD estimates the average distance to the nearest relative of all species or individuals (Webb et al., 2011). Both are measures of phylogenetic divergence and are expressed here in millions of years (Tucker et al., 2017). NRI and NTI are standardized measures of MPD and MNTD, respectively, based on 999 random communities. Positive values of NRI and NTI indicate that taxa are more related to each other than expected by chance (i.e. phylogenetic clustering), while negative values indicate the opposite (i.e. phylogenetic dispersion). We also calculated three metrics of phylogenetic richness and divergence based on Hill's numbers, °D(T), 1D(T) and 2D(T), which express the mean effective number of lineages for rare, common and dominant taxa (Chao et al., 2010; see details in Appendix S3).

To examine the functional responses of herb communities to the environmental gradients, we classified all herb species according to four key functional attributes: (1) life forms, following the Raunkiaer spectrum — chamaephytes, geophytes, and therophytes (Raunkiaer, 1934); (2) pollination syndrome — autophily, anemophily, melittophily, psychophily, phalaenophily, chiropterophily, and ornitophily (Quirino and Machado, 2014); (3) seed dispersal syndrome — autochory, anemochory and zoochory (Freitas et al., 2013; Gomes and Quirino, 2016); and (4) palatability — presence of secondary compounds, spines, or stinging hairs that protect against goats and other herbivores (obtained in the field and from the literature on toxic plants; Campos et al., 2016). We also classified the species in dicots and monocots. From each plot, we calculated the proportion of species or individuals in each trait category and modelled it against the explanatory variables.

Herb communities were assumed to result from three main forces: chronic anthropogenic disturbance, mean annual rainfall, and local density of woody plants. To estimate the chronic disturbance of each plot, we adopted direct (in the field) and indirect (interviews and geographic data) measurements of anthropogenic disturbances in forest stands, such as length of goat tracks, litter volume, number of tree stumps, number of residences and distance to the nearest road (see details in Arnan et al., 2018). We first checked for correlations between disturbance-related variables so we could select those that were not highly correlated (r < 0.7). We then integrated the selected variables using principal component analysis (PCA), with the significant PCA axes capturing most of the variability in the disturbance metrics. The mean was weighted by the variance explained by each PCA axis and varied between 0 (least disturbed) and 1 (most disturbed). The final values were multiplied by 100 and presented as percentages. Mean annual rainfall was obtained from the updated WorldClim global climate data repository (Hijmans et al., 2005), with 30-arc second resolution or about 1-km spatial resolution along the equator (www.worldclim.org), using the maptools package for R (Bivand and Lewin-Koh, 2015). Mean annual rainfall in the plots ranged from 510 to 940 mm. We used data on the density of woody plants from Rito et al. (2017b).

We used linear models to test the effect of annual rainfall, chronic disturbance, and density of woody plants on herb density, richness, and taxonomic, phylogenetic and functional metrics. Before constructing the models, we performed linear correlations between the explanatory variables to check for multicollinearity. None of the correlations were significant, with r ranging from 0.11 to 0.18. Herb density was log-transformed due to the substantial variation across the plots (54–2291 plants per 5 m2). Shapiro-Wilk tests were used to check whether model residuals were normally distributed. We used direct ordering to examine how species composition responded to the explanatory variables. Analyses were performed in the R 3.2.1 (R Core Team, 2020) and JMP 8.0 programs (Proust, 2009).

A total of 6787 individuals belonging to 57 species, 53 genera, and 24 families were recorded across the 19 forest stands (Table S2). Euphorbiaceae, Fabaceae, Malvaceae, Rubiaceae, and Poaceae were the most species-rich families (4–5 species each). The most abundant species were Eragrostis pilosa (24% of all herbs recorded), Mollugo verticillata (18%), Panicum sp., Urochloa mollis and Bulbostylis sp. (6% each), Diodela teres and Herissantia crispa (4% each). A small number of species were common and occurred in more than 60% of the plots (e.g. Commelina erecta, M. verticillata, U. mollis, Portulaca oleraceae and Tacinga inamoena). Most species occurred in five or less plots.

Species composition clearly varied across the environmental gradients. In the wettest and most conserved extremes of the gradient, the genera Ceratosanthes, Dalechampia, Jacquemontia and Dioscorea, all with climbing habit, plus Eragrostis, Herissantia, Antefora and Pavonia, dominated the communities (Fig. 2). In the driest stands, Rhaphiodon, Astraea, Merremia, Microtea, Richardia, Solanum, Tacinga and Neoglaziovia were more common, while in the most disturbed areas Borreria, Turnera, Solanum, Euphorbia and Tarenaya predominated (Fig. 2). This suggests that rainfall reduction and increased disturbance are driving communities towards different successional pathways. The genera Rhaphiodon, Astraea, Merremia, Richardia and Borreria, common in drier or disturbed areas, also dominated the plots with lower density of woody plots, along with Melocactus, Chamaecrista, Mimosa, Piriqueta, Blainvilea and Indigofera. Only Physostemom occurred exclusively in areas with higher density of woody plants.

Fig. 2.

Direct ordering of herb genera and their relative abundance as a function of the chronic anthropogenic disturbance, annual rainfall and density of woody plants across 19 stands of the Caatinga dry forest, northeast Brazil. Aec—Aechynomene; Ant—Anthephora; Ast—Astraea; Aye—Ayenia; Bla—Blainvillea; Bor—Borreria; Bul—Bulbostylis; Cer—Ceratosanthes; Cha—Chamaecrista; Cni—Cnidoscolus; Com—Commelina; Dal—Dalechampia; Dio-Diodella; Dios—Dioscorea; Era—Eragrostis; Eup-Euphorbia; Evol—Evolvulus; Fro—Froelichia; Gom—Gomphrena; Heri—Herissantia; Hyb—Hybanthus; Ind—Indigofera; Jac—Jacquemontia; Mar—Marsypianthes; Mel—Melocactus; Mer—Merremia; Mic—Microtea; Mim—Mimosa; Moll—Mollugo; Neo—Neoglaziovia; Oxa—Oxalis; Pan—Panicum; Pav—Pavonia; Phyl—Phyllanthus; Phy—Physostemon; Piri—Piriqueta; Por—Portulaca; Rha—Rhaphiodon; Rich—Richardia; Sch—Schwenckia; Set—Setaria; Sid—Sida; Sol—Solanum; Sta—Staelia; Taci—Tacinga; Tali—Talinum; Tar—Tarenaya; Trad—Tradescantia; Tur—Turnera; Uro—Urochloa; Zep—Zephiranthes; Zor—Zornia.

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Overall, forest stands supported relatively species-rich communities (5–26 species per 5 m2), with herb density varying from 54 to 2291 individuals per 5 m2. Herb density responded positively to rainfall as expected, but species richness did not (Fig. 3, Table S3). Chronic disturbance did not significantly affect herb density or species richness. Density of woody plants negatively affected species richness, but surprisingly did not influence herb density (Fig. 3, Table S3).

Fig. 3.

Relationships among chronic anthropogenic disturbance, annual rainfall and density of woody plants with species richness, herb density, and phylogenetic metrics of herb communities across 19 stands of the Caatinga dry forest, northeast Brazil. ab and pa refers to abundance-based and presence/absence metrics, respectively. Statistics are shown in Table S3.

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The level of relatedness close to the tips of the phylogeny (NTI) increased in the drier areas, but decreased in the more disturbed areas (Fig. 3, Table S3). Consistent with the taxonomic responses, these contrasting trends suggest that rainfall reduction and increased chronic disturbance are driving communities towards different phylogenetic profiles. Nonetheless, phylogenetic richness [0D(T)] and divergence [MPD, MNTD, 1D(T), 2D(T)] were not significantly affected by rainfall and disturbance (Fig. 3, Table S3).

The reduction in the density of woody plants increased the effective number of lineages [0D(T)], the level of relatedness close to tips (NTI) and across the entire phylogeny (NRI), and the phylogenetic divergence in the terminal branches (MNTD) (Fig. 3, Table S3). In summary, drier, less disturbed and less dense forest stands supported more phylogenetically clustered communities.

Herb communities were dominated by dicots (82.4% of species and 49.4% of individuals), therophytes (80.7% of species and 90.5% of individuals), species pollinated by bees (71.9% of species and 48.6% of individuals) and dispersed via autochory (61.4% of species and 47.9% of individuals). Grasses played a minor role in terms of number of species (8.8%), but were representative in terms of number of individuals (46.9%) (Table S4). The majority of species and individuals exhibited traits associated with high palatability to livestock (59.6% of species and 60.7% of individuals) (Table S4).

With the exception of life form and palatability, explanatory variables affected different functional attributes of herb communities (Table S5). Dicot abundance was positively related to chronic disturbance (Fig. 4, Table S5), while dicot species richness was negatively correlated with the density of woody plants (Fig. 4, Table S5). Chronic disturbance also affected positively the abundance of individuals pollinated by bees, while rainfall correlated negatively with the abundance of individuals pollinated by butterflies and birds, and positively with plants dispersed by wind (Fig. 4, Table S5).

Fig. 4.

Relationships among chronic anthropogenic disturbance, annual rainfall and density of woody plants with functional metrics of herb communities across 19 stands of the Caatinga dry forest, northeast Brazil. Statistics are shown in Table S5.

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