Large old trees play an important role in the forest ecosystems, contributing to the vegetation heterogeneity, population dynamics, and essential ecosystem services, such as potential control over the carbon cycle on a global level (Zhang et al. 2016, Bohn & Huth 2017, Lutz et al. 2018, Mensah et al. 2020). Studies have shown that they are highly sensitive to environmental disturbances and play a significant role in the way an ecosystem responds to them (Lutz et al. 2013). In this study, araucaria giant trees in an old-growth Araucaria Forest, with their unique set of architectural and morphological characteristics of trees, offer different conditions on base main trunks and reiterated trunks with large diameter that favorable for growth of epiphyte plants, thus contributing to their diversity (Scipioni et al. 2022).(Gentry & Dodson 1987, Zotz & Vollrath 2003, Zotz 2007).
Because of difficulties of access requiring use of specialized climbing techniques for data collection (Lowman 2004), studies addressing diversity of epiphytes on large forest trees are rare (Sillett 1999). Due to the decline in the number of giant trees in the Atlantic forest of Brazil and recognizing them not only as isolated individuals, but as complex systems, we here present complementary data that reinforce the need for conservation of old-growth forests and their associated life forms that are under constant threat.
Compared with other surveys of the same forest physiognomy shown in Appendix A (Supplementary Material), species richness of vascular epiphyte species on 9 giant phorophytes may be considered high. In a survey of Araucaria angustifolia, without criteria for exclusively large phorophyte species, Ruiz (2017) identified 25 species of vascular epiphytes on 30 phorophytes, lower mean species richness per phorophyte. Similarly, Becker et al. (2015), evaluating the presence of vascular epiphytes in an Araucaria Forest, found 27 species distributed on 20 phorophytes of Araucaria angustifolia and Dicksonia sellowiana (tree fern).
The greater diversity of epiphyte species in our study must be related to the larger size and age of the sampled phorophytes (~ 250–450 years). It showed the highest epiphyte richness in a forest of the same physiognomy compared to other studies with the highest number of sampled trees (Appendix A). Although several studies of the Araucaria Forest have shown a greater species richness of the epiphytes, such results are generally influenced by the size of the area and number of sampled phorophytes. Flores-Palacios and García-Franco (2006) have demonstrated a positive and linear relationship between the phorophyte size and the species richness of epiphytes they support, concluding that the relationship is valid both for certain species of phorophytes, and for the tree communities as a whole. However, the positive and linear correlation in large old trees is not observed (DBH > 0.9 m), demonstrating high richness variability (Fig. 1C) due to species saturation in certain trees and others with potential space for colonization of new vascular epiphytes. Our sampling effort was based on the size of the phorophytes, performed on nine trees. With the sampling sufficiency, shown in the rarefaction curve, it was possible to stabilize the sampling and demonstrate reduced chances of finding new species in new surveys. However, diversity can vary when large old trees are regularly distributed in the forest and with broader sampling in conifers and hardwoods, which have different size and form of crowns, trunks, and tree bark texture, covering more ecological zones for vascular epiphytic species.
The size and age of the phorophytes determine vertical microclimatic gradients (stratification) within the tree, as well as within the forest as a whole (Shaw 2004), allowing the canopy biota to find larger and heterogeneous colonizable spaces (Benzing 1995; Sillett and van Pelt 2007), as has been observed in Ocotea porosa, with more epiphyte species found in the canopy and justifying their association with species richness (Acebey & Krömer 2001, Mancinelli & Esemann-Quadros 2007, Díaz et al. 2010, Padilha et al. 2015). Whereas in Araucaria angustifolia, the association of species richness was the highest with the base of the trunk of giant individuals due to buttressing (Scipioni et al. 2019a, 2022) and fissured barks are important to certain groups of vascular epiphytes (e.g.bromeliads) (Ceballos et al. 2016).
The prevalence of holoepiphytes, characterized by the epiphyte habit throughout their entire life cycle and by specific attributes for fixation and permanence on the phorophytes (Benzing 1990), over other categories of epiphytes is commonly demonstrated in several studies (Dittrich et al. 1999; Bianchi et al. 2012).
Vertical distribution of epiphytes over the ecological zones of large phorophytes was variable and may be due to such factors as humidity, luminosity, and availability of space, in addition to a greater tree ramification, which augments surface for their attachment and their abundance (Benzing 1990). Predominant species in the basal region are generally more dependent on the understory moisture or more sensitive to luminosity in the canopy.
Among the limiting resources of the canopy, there is also the relative scarcity of nutrients, due to the absent or incipient soil, substrate instability, but mostly to water stress (Lüttge 1989). Studies have shown that humidity is one of the main factors with the greatest influence on the structure of epiphyte communities, especially those of ferns (Becker et al. 2015), corroborating our findings of the lower number of species of this group in the upper portion of large old trees. Nevertheless, an expressive number of epiphyte species occurs in the treetops of old trees exceeding 30 m in height, reinforcing the thesis that the vertical division of phorophytes into ecological zones exerts a strong influence on vascular epiphytes, due to their preference for distinct habitats with gradients of light and humidity, with some species occurring exclusively or preferentially in certain segments of the phorophyte (Rogalski and Zanin 2003), as can be seen in Fig. 5 and Table 2.
Among the botanical families of epiphytes with higher values of importance on large old trees, with morphophysiological characteristics adapted to conditions of greater physiological stress in acquiring water and nutrients(Benzing 1990) stood out Bromeliaceae, Cactaceae, and Polypodiaceae, confirming other studies carried out in the Atlantic Forest (Kersten & Silva 2001; Gonçalves & Waechter 2002), which showed, besides the above named families, the prominence of Orchidaceae, Piperaceae, and Gesneriaceae. These families are of a wide geographic distribution, with centers of diversity in southern and southeastern Brazil. Not requiring specific conditions for their establishment and being morpho-physiologically very adaptable, they occupy phorophytes with higher frequency, regardless of the ecological zone for establishment. Such mechanisms of capture, storage, and reduction of water loss as photosynthetic metabolism CAM, reduced leaves, presence of trichomes, tissue succulence, poikilohydry, rosette leaves forming tanks, among others (Bonnet et al. 2014), allow for their presence in diverse habitat niches provided by the large old trees.
Subtropical large old-growth trees are characterized by great abundance and species richness of vascular epiphytes. From the base of the trunk to the canopy they have clustered epiphytes of high number of individuals. Large old-growth trees have bromeliad colonies occupying areas greater than 1 m2 at the base of the trunk, something that is uncommon in trees of sizes less than 1 m in diameter (dhb), representing important phorophytes for the epiphytic community, providing shelter for flora and fauna, carbon sequestration, water retention and nutrient recycling, as well as elements that favor the biodiversity of vascular epiphytes in the Atlantic Forest. Such trees are rare and endangered in Brazil (Scipioni 2019; Scipioni et al. 2019a, b). Scientific studies and environmental policies to protect these elements of the landscape have become urgent (Lindenmayer et al. 2014). Our study did not find new species of vascular epiphytes on large old-growth trees. However, it has high richness due to the number of individuals sampled when compared to other studies. Large old trees may still harbor new species of plants, fungi and animals and represent a research frontier that should be prioritized in regions with high losses of forest cover (> 50%) worldwide.