Epiphyte-phorophyte relationships: assessing the differences between Seasonal Semideciduous and Swamp Forests in Southeastern Brazil¹

Relações epífita-forófito: avaliando as diferenças entre florestas estacional semidecidual e paludosa no Sudeste do Brasil

ABSTRACT

Vascular epiphytes are responsible for a considerable portion of tropical biodiversity; however, the variation of epiphytes-phorophytes relationships in different vegetation types are still poorly understood. In this study, we aimed to assess the presence, abundance, vertical distribution, and life cycle (holoepiphyte and hemiepiphyte) of vascular epiphytes in two vegetation types [Seasonal Semideciduous Forest (- SSF), and Swamp Forest (- SF)] in order to determine any correlation with phorophyte size (diameter and height) and the specificity of phorophyte species to the epiphytic colonization. There was a higher number of phorophytes in SF; however, epiphytes density did not differ between the vegetation types. The recorded vertical distribution also showed different patterns: in the SSF, most epiphytes were found in the canopy, while in the SF they occurred mainly on the trunks of the trees. The abundance of epiphytes was positively correlated with the phorophyte size in the two vegetation types. In the SSF, colonization of phorophytes by epiphytes appeared to be less species-specific than in the SF, where trees density is likely to be a more significant factor to epiphytic colonization. The results showed the importance of the forest heterogeneity in the conservation and maintenance of vascular epiphytes assemblage, demonstrated by differences in the abundance and distribution of the epiphytes, even in contiguous forests.

Keywords:
atlantic forest; hemiepiphytes; holoepiphytes; host tree; vertical distribution

RESUMO

As epífitas vasculares são responsáveis por uma parcela considerável da biodiversidade tropical; no entanto, suas relações com os forófitos entre diferentes tipos de vegetação em que ocorrem ainda são pouco compreendidas. Neste trabalho, objetivamos avaliar a presença, a abundância, a distribuição vertical e a categoria ecológica (holoepífita e hemiepífita) das epífitas vasculares em dois tipos de vegetação [Floresta Estacional Semidecídua (- FES) e Floresta Paludosa (- FP)], com o intuito de investigar se há correlação com o tamanho dos forófitos (diâmetro e altura) e possíveis especificidades na colonização destes pelas epífitas. Na FP foi registrado um maior número de forófitos; no entanto, a abundância de epífitas não apresentou diferenças entre os dois tipos de vegetação. A distribuição vertical apresentou diferença entre os tipos de vegetação, com mais epífitas no fuste na FP, enquanto na FES a copa apresentou mais epífitas. Houve relação positiva da abundância de epífitas com o porte dos forófitos em ambas as fitofisionomias. Por outro lado, a densidade das espécies de árvores é provavelmente mais importante na FP para a colonização das epífitas. Os resultados mostraram a importância da heterogeneidade florestal na conservação e manutenção da assembleia de epífitos vasculares, demonstrada pelas diferenças na abundância e distribuição das epífitas, mesmo em florestas contíguas.

Palavras-chave:
árvore hospedeira; distribuição vertical; floresta atlântica; hemiepífitas; holoepífitas

Introduction

Traditionally, vascular epiphytes are defined as plants that grow on other live plants (phorophytes), using them only as mechanical support, either without floor connection (holoepiphytes) or connected just in a part of the life cycle (hemiepiphytes) (Madison 1977). Recently, some conceptual changes have been made by Zotz (2013, 2016), that accepted only the holoepiphytes and the traditionally primary hemiepiphytes as epiphytes, excluding the secondary hemiepiphytes or nomadic vines (as per Zotz 2013), by the fact that they are unlikely to lose ground connection after climbing up. These changes regards different epiphyte-phorophyte relationships. Besides these intricate relationships with the trees, the diversity of this guild represent a significant portion of the tropical biodiversity (Gentry & Dodson 1987, Kersten 2010, Zotz 2013), corresponding to 50% of the total flowering and non-flowering plant richness in some localities (Kersten 2010).

Many biotic factors influence the vascular epiphyte distribution patterns, as phorophyte size, bark types, toxins on bark, crown architecture, microhabitats provided by the phorophytes, bryophytes cover, dispersal syndromes of the epiphytes and forest types (ter Steege & Cornelissen 1989, Wolf 1994, Hernández et al. 1999, Arévalo & Betancur 2006, Wagner et al. 2015). In addition, abiotic factors, as luminosity and humidity, also influence the spatial distribution of the vascular epiphytes (Gentry & Dodson 1987, ter Steege & Cornelissen 1989, Wolf 1994, Hernández et al. 1999, Arévalo & Betancur 2006, Breier 2005, Joanitti 2013).

The diversity of vascular epiphytes are known to vary at both local (ter Steege & Cornelissen 1989, Arévalo & Betancur 2004, 2006, Kersten et al. 2009, Joanitti 2013) and on a large scale (Gentry & Dodson 1987, Nieder et al. 1999, Breier 2005, Leitman et al. 2015). Their distribution might follow ecological gradients, both horizontally - among different vegetation types and phorophytes (Benavides et al. 2011, Marcusso et al. 2016) - and vertically, exhibiting variations on the same phorophyte, from the floor to the canopy (ter Steege & Cornelissen 1989, Nieder et al. 1999, Rogalski et al. 2016). These distribution changes occur mainly due to the humidity that increases from the canopy to the ground, and to the luminosity and wind that follow the opposite way (Benzing 1995).

In Brazil, there is an increasing number of studies on quantitative and spatial distribution of epiphytes (e.g.Bonnet & Queiroz 2006, Kersten & Waechter 2011, Basílio et al. 2015), but few investigate phorophytes colonization trends by epiphytes (e.g.Fontoura et al. 2009, Alves et al. 2008, Silva et al. 2010), and between vegetation types (e.g.Kersten et al. 2009, Joanniti 2013, Rogalski et al. 2016, Padilha et al. 2017). The Seasonal Semideciduous Forest (SSF) and Swamp Forest (SF) are two forest types of the Atlantic Forest Domain that can show contiguous occurrence and differences in some of the features responsible for vascular epiphytes diversity and distribution, such as humidity, especially because of the waterlogged soil in the SF (Ivanauskas et al. 1997, Marcusso & Monteiro 2016).

In this context, Kersten et al. (2009) found higher epiphytes diversity and abundance in an alluvial forest than in a contiguous no alluvial forest in the Atlantic Forest domain. Moreover, Quaresma et al. (2017) observed that the nutritional aspects of the soil influences the epiphytes diversity in two seasonally floodplain forest types in the Amazon, where the most richness nutritional one, the Várzea forest, supported more epiphytes than the nutritional-poor Igapó forest. These results show the importance of understanding what patterns of diversity might occur in different forest types like SSF and SF.

Thus, the lack of adequate studies evaluating the colonization and the relationships between vascular epiphytes and phorophytes in these forest types, and how they influence the epiphytes led us to investigate the following questions: (1) Are there variations in the presence, abundance, vertical distribution and life cycle of vascular epiphytes in these two forest types? (2) Are there correlations between vascular epiphytes abundance and phorophytes size? (3) Do vascular epiphytes have affinities for certain host tree species?

Material and methods

Study area - The study was conducted in Botucatu city, São Paulo State, Southeastern Brazil (figure 1), at the Escola do Meio Ambiente (22º55’23”S and 48º27’28”W). The site is located in Paraná Basaltic Plateau, a geomorphologic province that is characterized in three units: Peripheral Depression, Botucatu Cuestas and Western Plateau (Ponçano et al. 1981). The soils are formed from Bauru and Serra Geral group, and the main types are the latosol, neosol and patches of hydromorphic soils (e.g. organosol and argisol) (Campos et al. 2004). According to Köeppen’s classification, its climate is subtropical humid with dry winter and hot summer (Cwa). The average annual temperature is 20.7 ºC, with a long-term mean precipitation of 1358 mm, the rainiest months from October to March (average of 169 mm), and the driest from April to September (average of 57.5 mm) (CEPAGRI 2018).

Figure 1
Location of the studied area indicated by a triangle in Botucatu municipality, São Paulo State (in black), Southeastern Brazil.

The site is located at an elevation of 850 meters with patches of Seasonal Semideciduous Forest (sensuIBGE 2012), Swamp Forest (sensuRodrigues 2000) and anthropic areas. The SSF covers 14 hectares, and it is characterized by about 30%-50% of the individual trees sheding leaves simultaneously during the driest season (IBGE 2012). In the studied area, the upper stratum of SSF is generally formed by emergent trees of 15-20 m tall, and average canopy of 13 m. The main tree species in the canopy are Ocotea velutina (Mart. ex Nees) Rohwer (Lauraceae), Croton floribundus Spreng. (Euphorbiaceae), Copaifera langsdorfii Desf. (Fabaceae), Machaerium villosum Vogel (Fabaceae), Aniba firmula (Nees & Mart.) Mez (Lauraceae) and Cordia sellowiana Cham. (Boraginaceae). In the understory, the most common species are Cordiera sessilis (Vell.) Kuntze (Rubiaceae), Metrodorea nigra A. St.-Hil. (Rutaceae), Actinostemon concepcionis (Chodat & Hassl.) Hochr. (Euphorbiaceae), Esenbeckia grandiflora Mart. (Rutaceae), Casearia sylvestris Sw. (Salicaceae), Maytenus gonoclada Mart. (Celastraceae), Mollinedia elegans Tul. (Monimiaceae) and Hirtella hebeclada Moric. ex DC. (Chrysobalanaceae). Epiphytic plants have low richness (Marcusso & Monteiro 2016), while climber plants are conspicuous in this forest.

SF is found in areas where groundwater is close to the soil surface (Ivanauskas et al. 1997, Rodrigues 2000). In the studied area, it covers approximately two hectares, with emergent trees reaching about 15-18 m height, with canopy averaging 10 m. The main tree species in the canopy are Protium heptaphyllum (Aubl.) Marchand (Burseraceae), Magnolia ovata (A.St.-Hil.) Spreng. (Magnoliaceae), Tapirira guianensis Aubl. (Anacardiaceae), Handroanthus umbellatus (Sond.) Mattos (Bignoniaceae), Pera glabrata (Schott) Poepp. ex Baill. (Peraceae) and Callophyllum brasiliense Cambess. (Callophylaceae). In the understory, the main species are Myrsine gardneriana A. DC. (Primulaceae), Hedyosmun brasiliense Mart. (Chloranthaceae) and Dendropanax cuneatus (DC.) Decne. & Planch. (Araliaceae). More species of vascular epiphytes occur in this type of forest (Marcusso & Monteiro 2016), but fewer climbers were observed.

Sampling - Fieldwork was carried out from June 2013 to June 2014. Trees were used as sample units in this study. We set seven linear transects, about 10 meters from each other, three in the SF (with a total length of 290 m, 240 m and 260 m) and four in the SSF (230 m, 210 m, 150 m and 200 m long). In the SF, only three transects were set because of the forest fragment size and shape. Nevertheless, the number of trees sampled was the same in both vegetation types. We used the point-centered quarter method (Cottam & Curtis 1956), in which every 10 meters the four nearest trees with circumference at breast height (CBH) ≥ 15 cm were sampled. The edges (e.g. 10 m) were not sampled to avoid the edge effect (Bianchi & Kersten 2014, Bernardi & Budke 2010). All sampled tree species were collected and identified by authors and specialists (cited in the acknowledgment). The taxonomic classification follows APG IV (2016) with nomenclature and authority according to Flora do Brasil 2020. When collected fertile, vouchers were deposited in the Herbário Rioclarense (HRCB).

For each sampled tree, we verified the presence (“phorophyte”) or absence (“tree”) of the vascular epiphytes. We noted the height that seedlings and adult plants were growing.

In each sampled tree, we verified the presence - In this case, a phorophyte - or absence - so, treated as tree - of the vascular epiphytes, including seedlings or adult plants, and noting the height that the epiphytes were growing (for details about epiphyte composition in the studied area, see Marcusso & Monteiro 2016).

The phorophytes were divided, visually, in three thirds so that we could evaluate the vertical distribution of the epiphytes (following Kersten & Waechter 2011b), checked by the occurrence in the low trunk (lowermost third), high trunk (middle third) and crown (last third).

Epiphytes were classified in holoepiphytes (never connecting to the floor) and hemiepiphytes (connection to the soil in part of the life cycle) (as per Benzing 1990). We considered the presence in all recorded strata when hemiepiphytes growing in one or more strata in the vertical distribution.

The abundance of vascular epiphytes was measured by coverage classes considering all the phorophyte (low trunk, high trunk and crown). The method we are using as proposed by Gonçalves & Waechter (2002) (see more details about these methods in Kersten & Waechter 2011), considering five classes, as follows: one (0-10% cover), three (11-30%), five (31-50%), seven (51-70%), and 10 (71-100%).

Statistical analysis - All statistical analysis was performed using R software (R core team 2017). We used vegan (Oksanen et al. 2013) and simpleboot (Peng 2019), adopting α ≤ 0.05 and 999 randomizations for the permutation-based methods. To test differences in the type of life cycle of vascular epiphytes between vegetation types, we used a Kolmogorov-Simonov test, after testing for normality, followed by a Fisher’s test. We performed a permutation-based analysis of variance (ANOVA), followed by pairwise t-tests using Bonferroni correction, to test for differences in the abundance of epiphytes among vegetation types and phorophyte variables (CBH and height).

To assess the colonization trends of phorophytes by vascular epiphytes, we performed a Correspondence Analysis (CA), by means of epiphyte individuals’ abundance on the phorophytes in each vegetation type (for details and explanations of the analytical methods used, see Laube & Zotz 2006, Wagner et al. 2015). Only tree species that serve as phorophytes in at least five individuals (68% of the phorophytes sampled) in each vegetation types were included in this analysis (table 1). Finally, to evaluate the relationships between individuals’ abundance (predict variable) and the number of phorophytes (response variable) for every tree species sampled, within each vegetation type, a linear regression by bootstrap method was carried out. We reported p and R² values from the bootstrap analysis outputs and we inspected scatterplots to determine any outlier and Pearson’s correlation.

Table 1
Tree species with the acronym used and phorophytes considered in the Correspondence Analysis, recorded in the Seasonal Semideciduous Forest and Swamp Forest in Botucatu municipality, São Paulo State, Brazil. (- means that the species does not occur in the vegetation type).

Tree species	Acronyms	Seasonal Semideciduous Forest	Swamp Forest
		Trees sampled / phorophytes (%)
Protium heptaphyllum (Aubl.) Marchand	Prohep	2/1 (50)	61/37 (60.6)
Magnolia ovata (A.St.-Hil.) Spreng.	Magova	-	46/28 (60.8)
Tapirira guianensis Aubl.	Tapgui	-	41/24 (58.5)
Cordiera sessilis (Vell.) Kuntze	Corses	27/4 (14.8)	-
Myrsine gardneriana A. DC.	Myrgar	-	23/11 (47.8)
Metrodorea nigra A. St.-Hil.	Metnig	20/3 (15)	2/1 (50)
Croton floribundus Spreng.	Croflo	17/8 (47)	2/1 (50)
Hedyosmun brasiliense Mart.	Hedbra	-	18/6 (33.3)
Esenbeckia grandiflora Mart.	Esegra	15/2 (13.3)	2/1 (50)
Maytenus gonoclada Mart.	Maygon	14/0 (0)	3/0 (0)
Actinostemon concepcionis (Chodat & Hassl.) Hochr.	Actcon	17/0 (0)	-
Dendropanax cuneatus (DC.) Decne. & Planch.	Dencun	-	16/11 (68.7)
Pera glabrata (Schott) Poepp. ex Baill.	Pergla	5/2 (40)	11/7 (63.6)
Casearia sylvestris Sw.	Cassyl	15/6 (40)	-
Hirtella hebeclada Moric. ex DC	Hirheb	13 / 1 (7.7)	1/1 (100)
Handroanthus umbellatus (Sond.) Mattos	Hanumb	-	13/11 (84.6)
Ocotea velutina (Nees) Mart. ex B.D.Jacks.	Ocovel	13 / 5 (38.5)	-
Copaifera langsdorfii Desf.	Coplan	12 / 5 (16.7)	-
Mollinedia elegans Tul.	Molele	11 / 5 (45.4)	-

Results

A total of 72 tree species were recorded in the SSF, of which 40 were phorophytes (56%), while 41 tree species were sampled in the SF, with 29 phorophytes (71%, table 2). The most abundant tree species in both vegetation types are given in table 1.

Table 2
Trees, phorophytes, life cycle and mean size of the trees and phorophytes in the Seasonal Semideciduous Forest and Swamp Forest in Botucatu municipality, São Paulo State, Brazil. HEM: hemiepiphyte; HOL: holoepiphyte; CBH: circumference at breast height; cm: centimeters; m: meters. Different letters indicate significant differences in the mean values of life cycle between vegetation types (P < 0.05).

Trees, phorophytes and life cycle of the epiphytes	Seasonal Semideciduous Forest	Swamp Forest
Trees
Total number of sampled trees	316	316
Total of trees families sampled	29	27
Trees sampled without epiphytes	227 / 71.8%	138 / 43.7%
Trees sampled holding epiphytes	89 / 28.2%	178 / 56.3%
Trees species / Phorophytes species	70 / 40	41 / 29
Phorophytes and life cycle
Total number of sampled phorophytes	89	178
Phorophytes holding HOL	86 / 96.6%a	121 / 68%b
Phorophytes holding HEM	0 a	17 / 9.6% b
Phorophyte holding HOL and HEM	3 / 3.4% a	40 / 22% b
Structural aspects
Mean total CBH (cm)	49 ± 39	42.4 ± 28.5
Trees, phorophytes and life cycle of the epiphytes	Seasonal Semideciduous Forest	Swamp Forest
Mean phorophytes CBH (cm)	73.2 ± 48.1	51.4 ± 32.3
Mean total height (m)	10 ± 4	9.7 ± 4
Mean phorophytes height (m)	12.5 ± 4.6	10.7 ± 3.7

We found 42.2% of all sampled trees in both vegetation types holding epiphytes. More trees serve as support for epiphytes in the SF (56% of the sampled trees) than in the SSF (28%) (table 2). Epiphyte life cycle differed between the two vegetation types (P< 0.5), with both holoepiphyte and hemiepiphytes more common in the SF (table 2) than in the SSF, where only three trees hold hemiepiphytes. On the other hand, epiphyte coverage did not show differences between the two studied vegetation types (P = 0.1) (table 3).

Table 3
Abundance of vascular epiphytes assessed by coverage classes in the Seasonal Semideciduous Forest and Swamp Forest in Botucatu municipality, São Paulo State, Brazil. Percentages refer to the total number of sampled phorophytes.

Epiphytes coverage (%)	Seasonal Semideciduous Forest	Swamp Forest
0-10	67/75.3%	125/70.2%
10-30	16/18%	24/13.5%
30-50	6/6.7%	19/10.7%
50-70	0	8/4.7%
70-100	0	2/1.1%

Vertical distribution showed differences between vegetation types (P < 0.01), with more epiphytes found in the lower and higher trunks in the SF, whereas in the SSF they were mostly in the crown (figure 2). Epiphytes abundance in both vegetation types vary significantly in relation to the phorophytes height (ANOVA SSF: pseudo-F = 19.76; P < 0.005; SF: pseudo-F = 7.936; P < 0.005) and the CBH (ANOVA: SSF: pseudo-F = 20.51; P < 0.005; SF: pseudo-F = 7.671; P < 0.05). In general, we found a greater abundance of epiphytes (higher coverage classes) in the trees with the largest CBH and heights, in both vegetation types studied (figure 3).

Figure 2
Vertical distribution of vascular epiphytes in two vegetation types, Seasonal Semideciduous Forest and Swamp Forest in Botucatu municipality, São Paulo State, Brazil.

Figure 3
Mean values of height (a,b) and CBH (c,d - circumference at breast height) in relation to epiphytes coverage of the phorophytes in two vegetation types, Seasonal Semideciduous Forest and Swamp Forest in Botucatu municipality, São Paulo State, Brazil. Different letters indicate significant differences in the mean values of life cycle between vegetation types (P < 0.05).

The first two axes of the CA ordination (figure 4) were significant in both vegetation types (P < 0.05). In the SSF, the first axis explained 63.1% of the total of variance and the second axis 31.1%, while for the SF, the first axis explained 87.1% and the second axis 12.9%. The CA showed a segregation trend of phorophytes, according to their epiphytes coverage, and revealed different species associated with each coverage note (figure 4). In general, the ordination diagram showed Ocotea velutina, Mollinedia elegans and Croton floribundus related to the higher epiphyte coverage in the SSF (figure 4a), and Protium heptaphyllum, Handroanthus umbellatus, Magnolia ovata and Tapirira guianensis in the SF.

Figure 4
Correspondence analysis between phorophyte species and epiphyte coverage notes (numbers) in the Seasonal Semideciduous Forest (A) and Swamp Forest (B) Forest in Botucatu municipality, São Paulo State, Brazil (acronyms according to table 1).

Overall, we observed a strong association (correlation values) between the abundance of tree species and phorophytes in both vegetation types (figure 5). However, both adjusted (R²) and fitted values (p-values) of linear regressions differed, with the variation in the number of phorophytes with the variation in the number of individuals being stronger in the SF.

Figure 5
Linear regression between the number of tree individuals and phorophytes density in the Seasonal Semideciduous Forest (a) and in the Swamp Forest (b) in Botucatu municipality, São Paulo State, Brazil. ●: tree species; grey area - Confidence interval for the regression line.

Discussion

Macroclimate strongly influence vascular epiphytes distribution at a large scale and, in the same way, microclimate is also an important variable (Gentry & Dodson 1987, Breier 2005, Furtado & Menini Neto 2018), even in contiguous different forest types. Small moister areas in a given vegetation type can promote the epiphytic colonization (Waechter & Baptista 2004, Kersten et al. 2009, Bonnet et al. 2010a, Joanitti 2013, Furtado & Menini Neto 2018), as demonstrated in the present study by the higher number of phorophytes recorded in the SF. Considering that epiphytes tend to be more limited by water availability than nutrients (Laube & Zotz 2003, Becker et al. 2015), this riparian forest embed in a seasonal macroclimate region would have moister microclimatic conditions, because of water evaporation provided by waterlogged soils, affecting positively vascular epiphytes (Waechter & Baptista 2004, Kersten et al. 2009, Bonnet et al. 2010b, Wagner et al. 2015, Padilha et al. 2017).

The differences of life cycle between the vegetation types (table 2) might be mainly due to the abundance of Philodendron appendiculatum Nadruz & Mayo (Araceae) in SF, a species recorded as primary and secondary hemiepiphyte (Marcusso & Monteiro 2016). The higher abundance of P. appendiculatum in SF is probably the reason of more epiphytes in the trunks in this forest, as this species is common in this stratum. This species is almost absent in SSF. The prevalence of the secondary hemiepiphytes in the lower strata caused by Araceae (Rogalski et al. 2016) supports the observed vertical distribution found here.

More epiphytes growing on the crown in the SSF suggest that the higher luminosity may offer better conditions to the shade-intolerant species; besides, its predominantly horizontal substrate may have more accumulation of organic matter, as opposed to the trunk, that is usually vertical (ter Steege & Cornelissen 1989, Nieder et al. 2001, Martínez-Melendez et al. 2008, Zhao et al. 2015). Alternatively, regarding the SF, the prevalence of epiphytes in the trunk may occur perhaps because of differential humidity and light in the vertical gradient (Benzing 1990, Bathagin et al. 2012). In the SF, as humidity is high in the understory, shade-tolerant species may be favoured in this vegetation type (e.g.Bathagin et al. 2012).

Relationships between vascular epiphytes and the phorophyte size as recorded here are supported by others studies as well (Breier 2005, Flores-Palacios & García-Franco 2006, Bonnet et al. 2007, Orihuela & Waechter 2009, Bonnet et al. 2010 a, Obermüller et al. 2012, Zhao et al. 2015). The size of a phorophyte tend to be associated with tree age (Yeaton & Gladstone 1982, Zotz & Vollrath 2003, Zhao et al. 2015), therefore older phorophytes would support more epiphytes as there will be longer time in which they are available to be colonized (Bonnet et al. 2010a, Zhao et al. 2015).

The most abundant tree species in the SF were also those with more phorophytes, in agreement with Fontoura et al. (2009), but this relationship was weak in the SSF. Some abundant tree species in the SSF have none or little epiphytes either because they have small diameter and smooth bark (e.g. Actinostemon), or perhaps there are other factors affecting epiphyte distribution (e.g. Maytenus) offering few suitable substrates to the colonization by epiphytes (Trapnell & Hamrick 2006, Zhao et al. 2015). Factors as bark type (Sanford 1974, Wyse & Burns 2011), inhibitory substances, mycorrhiza presence (Trapnell & Hamrick 2006, Martínez-Melendez et al. 2008, Sathiyadash et al. 2012, Einzmann et al. 2015), lack of bryophytes cover (Zotz & Vollrath 2003), low water-holding capacity (Callaway et al. 2002), host tree phenology (Einzmann et al. 2015) or chance (Fontoura et al. 1995, Zotz & Vollrath 2003) are known to influence colonization by epiphytes.

In SF, some phorophyte species have higher epiphytes cover. Most abundant tree species were also the best phorophytes, like P. heptaphyllum and M. ovata. The abundance of phorophyte species and the lack of restrictive humidity conditions do not act as barriers to colonization on suitable substrates in SF, as it may occur in the SSF. The lower tree species richness in SF (due to hypoxia caused by the waterlogged soils, Ivanauskas et al. 1997) is an important factor when phorophyte specificity is analyzed (Callaway et al. 2002, Wagner et al. 2015). In the forest with more species of phorophytes, regarding the colonization by epiphyte, specificity tend to be lower than in poor tree species forest, as in the SF (Laube & Zotz 2006, Fontoura et al. 2009, Wagner et al. 2015). According to Ceballos et al. (2016), the interactions between vascular epiphytes and phorophytes are mainly related to the species density, additionally to the tree size and tree bark texture. These may help to justify the low phorophyte specificity in the SSF (Fontoura 1995, Fontoura et al. 2009, Silva et al. 2010, Benavides et al. 2011, Joanitti 2013).

Summarizing, vascular epiphytes distribution showed differences between the vegetation types studied. The hemiepiphytes are practically absent in the SSF, while the reverse happens in the SF, with both hemi and holoepiphytes growing more in the trunk, where its moister conditions allow the growth of shade-tolerant types in the understory of the SF. Nonetheless, in the SSF, epiphytes occurred more in the canopy, mainly represented by xerophytic and heliophytic species, likely because of the dry conditions acting as a barrier to the colonization of more shade-tolerant species in the lower strata. In the SSF, the epiphyte colonization is positively correlated with phorophytes size, and it is likely that humidity might limit the colonization in small trees. Besides, low phorophytes specificity may occur. In the SF, where the humidity is not a limiting factor, tree density may be more important to drive epiphyte colonization than the phorophytes size, as the most abundant tree species had more phorophytes and higher epiphyte cover.

These results could help the management of restored forests, where biological enrichment might be necessary to increase the diversity of the vascular epiphytes (e.g.Duarte & Gandolfi 2017). In addition, old and high trees show their role as holding high biomass and allowing maintenance of a higher local pool of epiphyte species. Forests where selective logging is allowed, management might be necessary to decrease the impact on the vascular epiphytes, maintaining these strategic phorophytes (Wolf 2005).

Acknowledgments

We thank the Conselho Nacional de Desenvolvimento Científico e Tecnológico (process 133495/2013-2) for the MSc scholarship to the first author; Eliana Gabriel for the permission to access and study in the Escola do Meio Ambiente vegetation; Pablo Sanine for help in the field work; Gabriel Pavan Sabino, Leonardo Biral, Rodrigo Ferreira de Morais, Pedro Luís Rodrigues de Moraes, Bruno Sampaio Amorim and Ernesto Pedro Dickfeldt for helping with tree identification; Henrique Lauand Ribeiro for the map design; and Cláudia Baider and two anonymous referee for the valuable contribution in the manuscript version.

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Publication Dates

• Publication in this collection
  22 July 2019
• Date of issue
  2019

History

• Received
  12 Mar 2018
• Accepted
  23 Apr 2019