Introduction
The Atlantic Forest is the most biodiverse phytogeographic domain in Brazil, supporting > 17,000 catalogued species (Mittermeier et al., Reference Mittermeier, Hoffmann, Pilgrim, Brooks, Lamoreux, Mittermeier, Gil and da Fonseca2004; Brazil Flora Group, 2022). Annonaceae is a diverse family of flowering plants including Xylopia, one of the genera that occur in Brazil (Lobão et al., Reference Lobão, Lopes, Erkens, Mendes-Silva, Pontes Pires and Silva2020). Xylopia comprises several tree or shrub species, many of which are known as pindáiwa by the Indigenous peoples, meaning plants used as fishing nets (Dias, Reference Dias1988; Lopes & Mello-Silva, Reference Lopes and Mello-Silva2014).
Xylopia decorticans D.M. Johnson & Lobão (Plate 1), described in 2007, has a restricted distribution and is endemic to the highlands in central Espírito Santo State (Lobão & Johnson, Reference Lobão and Johnson2007). It is recognized by the reddish-brown bark on its branches (Plate 1a–b), its fleshy flowers that develop from the base of the stem to the branches (Plate 1d–f), and its pink or reddish fruits with arillate seeds (Lobão & Johnson, Reference Lobão and Johnson2007; Plate 1g–h). In addition, this zoochorous species provides resources for wildlife in different forest strata because of its characteristic cauliflory. The species was originally categorized as Least Concern because it occurs in at least two protected areas of the Atlantic Forest in Espírito Santo State, the Reserva Biológica Augusto Ruschi and the Estação Biológica Santa Lúcia (Lobão & Johnson, Reference Lobão and Johnson2007). The description was based on specimens from eight localities, six of which were in private areas. Since 2007, the species has been found in four new localities, also in private areas. Despite this increase in the number of recorded localities, as a result of the progressive conversion of the forest for other land use and the damage caused by logging and wood harvesting in the region (Mendes & Padovan, Reference Mendes and Padovan2000; Thomaz, Reference Thomaz2010; CNCFlora, 2018), it is now categorized as Endangered on the Brazilian Red List of Threatened Species (Brazil, 2022) and on the IUCN Red List (Fernandez et al., Reference Fernandez, Verdi, León, Martinelli and Lopes2021). Recently, advances in our knowledge of the flora of Espírito Santo State have led to the identification of a new subpopulation in a small private protected area. This study built on that discovery by carrying out an assessment of the abundance of X. decorticans locally, with a view to enhancing our understanding of its biology and distribution.
Plate 1 Identifying features of Xylopia decorticans in the Reserva Particular do Patrimônio Natural Macaco Barbado, Santa Maria do Jetibá, Espírito Santo, Brazil: (a) branch and leaves; (b) details of a branch emphasizing the reddish-brown bark; (c) cauliflory tubers; (d–e) flower buds; (f) flower at anthesis; (g) immature fruit; (h) mature and open fruit. Photos: (a–c, e) M.I.A. Horst; (d) L.S.B. Calazans; (f, h) L.O. Bezerra; (g) D.O. Sabbagh.
Ecologically, studies on rare and threatened species are important because population data are often scarce, resulting in significant knowledge gaps that hinder effective conservation actions and predictions of future population change (Hortal et al., Reference Hortal, De Bello, Diniz-Filho, Lewinsohn, Lobo and Ladle2015; Collen et al., Reference Collen, Dulvy, Gaston, Gardenfors, Keith and Punt2016; CNCFlora, 2018). Recognizing the critical need for such information (as highlighted by the Brazilian Red List; CNCFlora, 2018; Brazil, 2022), this study investigated the population structure of X. decorticans to contribute to its long-term conservation in the face of ongoing declines in habitat quality and extent, whilst providing crucial data for future management and restoration efforts for threatened flora in the region.
Study area
We conducted our study within the Reserva Particular do Patrimônio Natural Macaco Barbado, a private protected area located in the state of Espírito Santo, south-eastern Brazil (Fig. 1). The reserve encompasses < 50 ha of well-preserved dense ombrophilous forest, lies within the Centro Norte Serrano Ecological Corridor (Espírito Santo, 2010) close to several other protected areas (see Silva et al., Reference Silva, Calazans, Valadares and Dutra2020), and is designated as an Outpost of the Atlantic Forest Biosphere Reserve (IA-RBMA, 2023). Situated in the municipality of Santa Maria de Jetibá, the Reserve spans elevations of 750–900 m. According to Köppen’s climate classification, the region exhibits a warm temperate climate, fully humid with no dry season and a warm summer (Cfb: Alvares et al., Reference Alvares, Stape, Sentelhas, Gonçalves and Sparovek2014). The mean daily temperature is typically below 22 °C in the warmest month and below 18 °C in the coldest month, and mean annual precipitation is 1,259 mm (Incaper, 2023).
Fig. 1 The study site in Reserva Particular do Patrimônio Natural Macaco Barbado, Santa Maria do Jetibá, Espírito Santo, Brazil, showing the distribution and size (DBH, diameter at breast height) of the Xylopia decorticans trees recorded.
We collected some data outside the original boundaries of the Reserve in recently procured forest areas bordering the protected area. Access to the remainder of the forest fragment was limited as we did not have permission to enter other private areas contiguous with the Reserve.
Methods
We identified a subpopulation based on its degree of isolation in an extremely fragmented landscape subject to continuous anthropogenic disturbance (IUCN, 2019). We searched for X. decorticans in the Reserve during October 2023–August 2024, following the census protocol defined by Bullock (Reference Bullock and Sutherland)1996) and the guidelines for threatened tree conservation surveys outlined by the Global Trees Campaign (Brewer, Reference Brewer2013). We utilized existing trails as well as making incursions into the forest interior to carry out our search. The species occurs in well-preserved primary forest (Saiter et al., Reference Saiter, Oza and Freitas2024), so we did not survey forest areas undergoing regeneration.
We recorded all individuals ≥ 1.30 m tall, a sufficient height to measure other parameters (Moro & Martins, Reference Moro, Martins, Felfili, Eisenlohr, Melo, Andrade and Meira-Neto2011), and georeferenced coordinates in the Universal Transverse Mercator system using a GPS (Fig. 1). We also recorded life stage, diameter at breast height (DBH) and tree height (estimated by eye). We calculated height and diameter at breast height using the Spiegel formula (Felfili & Rezende, Reference Felfili and Rezende2003). We classified any individuals with cauliflory tubers present (Plate 1c) as adults, others as juveniles.
For our population census analysis, we plotted occurrence points in QGIS 3.32.0 (QGIS Development Team, 2016) to delineate minimum convex polygons for X. decorticans in the area. The sum of the area of the polygons represents the total area occupied by the subpopulation. We calculated population density by dividing the total number of individuals found by the total area occupied by the subpopulation.
We analysed qualitative indicators provided by the Brazilian Law for the Protection of Native Vegetation (Brazil, 2012) to assess the degree of habitat preservation in the survey area. We assessed the occurrence and condition of individual X. decorticans found near the edge of the forest fragment in a 10 m strip extending from the edge to the interior. We defined this limit based on qualitative indicators typically associated with edge effects, such as fallen trees, herbaceous strata dominated by heliophylous bamboos, discontinuous leaf litter, and high light intensity or luminosity (e.g. Murcia, Reference Murcia1995; Rodrigues & Nascimento, Reference Rodrigues and Nascimento2006; Laurance et al., Reference Laurance, Nascimento and Laurance2007). We assessed the vitality of individuals based on the condition of the crown and leaves, and the presence of any disease or damage indicators such as cavities in the trunk or fungal growths (Gill & Daltry, Reference Gill and Daltry2013).
Results
Our habitat assessment showed that X. decorticans thrives in minimally disturbed forest remnants or areas of advanced regeneration/successional stages. We identified the following indicators of suitable habitat: thick, continuous leaf litter; the presence of woody vines; a high density of epiphytes; palm indicator species such as Euterpe edulis Mart., Attalea dubia (Mart.) Burret, Syagrus insignis (Devansaye) Becc., Bactris timbuiensis H.Q.B.Fern. and Geonoma schottiana Mart.; an average canopy height of 25 m, including emergent specimens; and a high floristic richness with diverse life forms.
We located and measured 121 specimens of X. decorticans within the study area, occupying 4.08 ha, and comprising 38 juveniles and 83 adults with diameter at breast height ≥ 0.9 cm (Supplementary Table 1). We grouped our sample into two height classes (0–9.25 m and 9.26–18.50 m) and two DBH classes (0.95–12.95 cm and 12.96–25.9 cm). The majority of individuals (91.7%) were 2–9 m tall, and nearly all had a DBH of 0.95–10.5 cm. We calculated X. decorticans density as 29.65 individuals/ha.
We identified five dead or desiccated individuals in the edge strip of the study area. They were located in sections exposed to the prevailing north-east winds following conversion of adjoining areas to monoculture plantations of eucalyptus trees Eucalyptus spp. Although our sample is small, our observations are supported by the increase in luminosity, strong development of a heliophyte Chusquea spp. (Poaceae) community, discontinuity in the accumulation of leaf litter and the presence of large fallen trees. It is of note that we also recorded up to three fallen trees of X. decorticans with large stems (DBH ≥ 10 cm) in the edge strip. Overall, the species exhibited a strong preference for forest patches not exposed to edge effects.
Discussion
This study provides the first ecological data on X. decorticans, building on information gathered in earlier studies of the tree community in the highlands of Espírito Santo (e.g. Saiter et al., Reference Saiter, Oza and Freitas2024) and establishing initial parameters for more targeted conservation efforts. One of the targets set by the Global Strategy for Plant Conservation (BGCI, 2024) is that at least 20% of threatened species should be included in restoration and recovery programmes. However, the ecological characteristics of X. decorticans suggest that it should be recognized as a climax species and planted in the more advanced stages of regeneration, known in Brazil as forest enrichment. In Brazil, it is common to plant ombrophilous species such as X. decorticans in regenerating areas where forest strata are diagnosable but low in richness. We recommend that reintroduction efforts in areas undergoing regeneration within the study area should be limited to enrichment in forest patches at advanced successional stages.
In addition to our data providing the location of future collection matrices for ex situ propagation, they also contribute to our knowledge of the ecology, distribution and abundance of X. decorticans (Cardoso et al., Reference Cardoso, Erwin, Borges and New2011; Hortal et al., Reference Hortal, De Bello, Diniz-Filho, Lewinsohn, Lobo and Ladle2015). However, there is a continuing need for dispersion and ex situ conservation studies that can provide insights into germination and development, and protocols for in situ planting.
The predominance of individuals with a DBH of < 10 cm suggests that the legal inclusion criterion currently employed to assess forest vegetation within the Centro-Norte Serrano Corridor (Brazil, 2012) does not accurately reflect the population size of X. decorticans. For example, in the case of environmental permits for major infrastructure works, only trees with a DBH above this threshold are included in the species list presented to the inspection agency, which means that smaller X. decorticans would be omitted. The species list is directly related to future environmental mitigation actions, which could include germplasm rescue of declining species (Brazil, 2012).
Monitoring programmes are included as one of the mitigating actions specified in Brazilian legislation (Brazil, 2012). Based on our findings, population monitoring programmes for X. decorticans should use a DBH threshold of 5 cm, so that both young and adult individuals are included. Although we recorded some individuals high up in the canopy (c. 18 m at average canopy height), this species demonstrates a reproductive strategy closely linked to the understory. The prevalence of small trees in our study area aligns with patterns observed in understory species in tropical forests generally (Bohlman, Reference Bohlman2015), including other Annonaceae (Gomes-Westphalen et al., Reference Gomes-Westphalen, Lins-e-Silva and Araújo2012). Thus, our findings suggest that X. decorticans is a specialist species adapted to specific ecological conditions with a variety of trophic niches and more intricate ecological networks (Losapio et al., Reference Losapio, Montesinos-Navarro and Saiz2019). Collectively, our results indicate that the species is an understory component of more advanced successional forest stages, where community structure is more complex and thus conducive to species that are sensitive to desiccation in more exposed habitats.
Cauliflory increases the supply of flowers and fruits to seed dispersers and can occur from the base of the stem to the thinnest branches of the crown (Onstein et al., Reference Onstein, Kissling, Chatrou, Couvreur, Morlon and Sauquet2019). Plants in the genus Xylopia are associated with diplochory, in which vertebrates (mainly birds) and invertebrates are involved in seed dispersal (Christianini & Oliveira, Reference Christianini and Oliveira2010; Cabral et al., Reference Cabral, Bender, Couvreur, Faurby, Hagen and Hensen2025). Xylopia decorticans exhibits cauliflory and is important for threatened seed-eating birds throughout its range. We believe it may support both terrestrial birds (Galliformes) and species that feed in the tree canopy, including the following Endangered (EN) and Critically Endangered (CR) species (status according to Espírito Santo, 2022): Odontophorus capueira (EN), Asthenes moreirae (CR), Grallaria varia imperator (EN), Turdus fumigatus fumigatus (EN), Crypturellus noctivagus (CR) and Tinamus solitarius (EN). Therefore, conservation of X. decorticans will be of benefit to a wide variety of other wildlife.
We categorized the individuals present in the Reserva Particular do Patrimônio Natural Macaco Barbado as a distinct subpopulation of X. decorticans because of the low genetic flow between the forest fragments that characterize the highlands in the central region of Espírito Santo, particularly within the Centro-Norte Serrano Ecological Corridor. More diverse populations would exhibit greater genetic variation, enhancing their resilience to inbreeding and other genetic bottlenecks (Ridley, Reference Ridley2009; DeWood et al., Reference DeWoody, Harder, Mathur and Willoughby2021). An understanding of the population structure of endemic species such as X. decorticans is crucial for guiding conservation efforts aimed at reconnecting fragmented forest patches and maintaining ecological function in the landscape.
Population studies are essential for robust analyses of threatened species because there are large gaps in our knowledge of the distribution, evolution, ecology and physiology of even well-studied taxa such as Annonaceae (Hortal et al., Reference Hortal, De Bello, Diniz-Filho, Lewinsohn, Lobo and Ladle2015; Erkens et al., Reference Erkens, Blanpain, Jara, Runge, Verspagen, Cosiaux and Couvreur2023). Based on our findings, we recommend that X. decorticans is used in forest enrichment programmes, aligning with initiatives such as Forest Landscape Restoration (FAO et al., 2021), which are gaining traction regionally (Espírito Santo, 2023). This would also be a positive recommendation within the framework of actions aimed at the UN Decade on Ecosystem Restoration (UNEP & FAO, 2020). This approach would enable stakeholders to accelerate the implementation and monitoring of forest enrichment programmes, advancing global restoration goals and local conservation efforts.
In summary, our population census has provided quantitative data on the abundance and distribution of X. decorticans within a small Atlantic Forest fragment. Our findings improve our understanding of the ecological characteristics of species within regions afflicted by ongoing forest degradation, point the way to effective conservation action and underscore the pivotal role of private natural heritage reserves (Reservas Particular do Patrimônio Natural) in Brazil in the conservation of Endangered species such as X. decorticans.
Supplementary material
The supplementary material for this article is available at doi.org/10.1017/S0030605325102524
Author contributions
Study design: MIAH, RTV; fieldwork: MIAH, RTV, LSBC; data analysis: MIAH, RTV; writing: all authors.
Acknowledgements
This research was partially funded by the Universidade Federal do Espírito Santo scholarship to MIHA (process UFES 202422108DPQ). We thank Ecovila Bom Destino for providing fieldwork permission and assisting with logistics; Leo Gasparini, Emanoel Ferreira, Ana Luíza Batista, Lucas Bezerra, Cleberson Loureiro, Alexandre Magno, Germano Feijó, Gustavo Pezzani, Walder José Marianno, Fabiula Arantes and Humberto Passos Coelho for fieldwork support; and Hilton Monteiro Cristóvão for valuable data on the threatened birds occurring in the area.
Conflicts of interest
None.
Ethical standards
This research abided by the Oryx guidelines on ethical standards. Research in Espírito Santo State was carried out under IEMA permit NUBIO no. 028-R4A4/2015 - process no. 71911308.
Data availability
Data supporting the findings of this study are available within the article and its Supplementary Materials.
Open access
