Abstract

Epiphytes are considered indicators of forest ecological integrity, but the factors that explain their abundance are still not well understood. We here evaluated tree colonization by epiphytes in old-growth monospecific reforestation stands of Astronium urundeuva (M.Allemão) Engl. (Anacardiaceae) and Eucalyptus saligna Sm. (Myrtaceae), in comparison to a neighbor seasonal tropical forest fragment under similar environmental conditions. In each forest type, we identified and measured all trees (planted and colonizers) from 5-cm stem diameter in five 200 m² plots and quantified all vascular epiphytes per tree. Tree species were categorized by bark roughness, canopy deciduousness and growth rate. The abundance of epiphytes and the frequency of host trees were higher in the A. urundeuva plantation than in the native forest, with the E. saligna stand in an intermediate position. Also, we found that host traits influenced the abundance of epiphytes in their trunks. Host trees had average stem perimeter and height both higher than non-hosts, which indicates that colonization is more likely to occur in older trees. The average abundance of epiphytes per tree was higher in species with rough bark, but no relationship was found with canopy deciduousness or tree growth rate. We evidenced, therefore, that forest plantations, even if monospecific, can provide habitat for epiphytes. However, at community level, colonization success, either in native or restored forest, depends on the relative abundance of species whose bark type favors epiphytes establishment.

Keywords
Non-Tree Life Forms; Forest Restoration; Tropical Seasonal Forest; Epiphytism; Host Preference

Resumo

Epífitas são consideradas indicadores de integridade ecológica em florestas, mas os fatores que explicam sua abundância ainda não são bem compreendidos. Neste estudo, avaliamos a colonização por epífitas em antigos talhões monoespecíficos de Astronium urundeuva (M.Allemão) Engl. (Anacardiaceae) e Eucalyptus saligna Sm. (Myrtaceae), em comparação com um fragmento vizinho de floresta estacional semidecidual sob condições ambientais semelhantes. Em cada tipologia florestal, identificamos e medimos todas as árvores (plantadas e que colonizaram os locais) a partir de 5 cm de diâmetro à altura padrão, em cinco parcelas de 200 m². Nelas, também quantificamos todas as epífitas vasculares por árvore. Em busca de uma explicação funcional para as diferenças entre espécies, utilizamos rugosidade da casca, deciduidade da copa e taxa de crescimento como atributos potencialmente relevantes. A abundância das epífitas e a frequência de forófitos foi maior no talhão de A. urundeuva do que na floresta nativa, com o talhão de E. saligna ocupando uma posição intermediária. Encontramos evidências, também, de que os atributos dos forófitos influenciaram a abundância de epífitas em seus troncos. Os forófitos apresentaram maior perímetro médio e altura que as árvores não hospedeiras, o que indica que a colonização é mais provável de ocorrer em árvores mais velhas. A abundância média de epífitas por árvore foi maior em espécies com casca rugosa, mas nem a deciduidade da copa, nem a velocidade de crescimento exerceram efeito neste aspecto. Evidenciamos, portanto que, plantações florestais, ainda que monoespecíficas, podem prover habitat para epífitas. Contudo, em nível de comunidade, o sucesso da colonização, seja em florestas nativas ou restauradas, depende da abundância relativa de espécies cujo tipo de casca favorece o estabelecimento de epífitas.

Palavras-chave
Formas de Vida Não-Arbóreas; Restauração Florestal; Epifitismo; Preferência de Hospedeiro

Introduction

When tropical forests recover from disturbances (either naturally or via active restoration), it is well known that epiphytes are the latest plant group to colonize and re-establish in that ecosystem (Lisboa et al., 1991LISBOA, P.L.B., MACIEL, U.N. & PRANCE, G.T. (1991). Some effects of colonization on the tropical flora of Amazonia: A case study from Rondônia. Kew Bulletin 46(2):187–204., Kanowski et al., 2003KANOWSKI, J., CATTERALL, C., WARDELL-JOHNSON, G., PROCTOR, H. & REIS, T. (2003). Development of forest structure on cleared rainforest land in eastern Australia under different styles of reforestation. Forest Ecology and Management 183(1–3):265–280., Martin et al., 2013MARTIN, P.A., NEWTON, A.C. & BULLOCK, J.M. (2013). Carbon pools recover more quickly than plant biodiversity in tropical secondary forests. Proc. R. Soc. B. 280(1773):1–8., Novais et al., 2020NOVAIS, S., SÁYAGO, R., CRISTÓBAL-PEREZ, E.J., SALGUERO-HERNÁNDEZ, G., MARTÉN-RODRÍGUEZ, S., LOPEZARAIZA-MIKEL, M. & QUESADA, M. 2020. Anthropogenic and hurricane disturbances had similar negative effects on epiphytic Tillandsia species in a tropical dry forest. Forest Ecology and Management 458:1–7., Parra-Sanchez & Banks-Leite 2020PARRA-SANCHEZ, E. & BANKS-LEITE. (2020) The magnitude and extent of edge effects on vascular epiphytes across the Brazilian Atlantic Forest. Scientific Reports 10:1–11.). Intrinsic characteristics of the group, such as slow growth and requirements for specific substrate and humidity in the canopy (Zotz 1995ZOTZ, G. (1995). How fast does an epiphyte grow? Selbyana 16(2):150–154., Hietz 1999HIETZ, P. (1999). Diversity and conservation of epiphytes in a changing environment. Pure and Applied Chemistry 70:1–11.), besides dispersal limitations due to low landscape permeability, affect their arrival and establishment (Reid et al., 2016REID, J.L., CHAVES-FALLAS, J.M., HOLL, K.D. & ZAHAWI, R.A. (2016). Tropical forest restoration enriches vascular epiphyte recovery. Applied Vegetation Science 19(3):508–517.). For these reasons, epiphytes presence may be a good indicator of forest ecosystem health (Hietz 1999HIETZ, P. (1999). Diversity and conservation of epiphytes in a changing environment. Pure and Applied Chemistry 70:1–11.) and thus to assess forest restoration success or guiding adaptive management interventions.

Studies have shown low abundance of epiphytes in secondary and restored tropical forests (Suganuma & Durigan 2015SUGANUMA, M.S. & DURIGAN, G. (2015). Indicators of restoration success in riparian tropical forests using multiple reference ecosystems. Restoration Ecology 23(3):238–251., Garcia et al., 2016GARCIA, L.C., HOBBS, R.J., RIBEIRO, D.B., TAMASHIRO J.Y., SANTOS, F.A. & RODRIGUES, R.R. (2016). Restoration over time: is it possible to restore trees and non-trees in high-diversity forests? Applied Vegetation Science 19(4):655–666.), and the viability of increasing epiphyte presence in forest ecosystems undergoing restoration has been recently investigated. Different attempts to restore epiphyte community include reintroducing them on planted trees (Duarte & Gandolfi 2017DUARTE, M.M. & GANDOLFI, S. (2017). Diversifying growth forms in tropical forest restoration: Enrichment with vascular epiphytes. Forest Ecology and Management 401:89–98., Domene 2018DOMENE, F. (2018). Reintroduction of vascular epiphytes in forest restoration plantations. Doctoral dissertation, São Paulo University., Benavides et al., 2023BENAVIDES, A.M., CALDERÓN-CARO, J. & CANAL, D. (2023). Surviving in a new host: Eight years of monitoring translocated aroids, bromeliads, and orchids in the Andean forests in Colombia. Frontiers in Forests and Global Change 6:1–9., Sasamori et al., 2023SASAMORI, M.H., ENDRES JÚNIOR, D., AMARAL, S.V. & DROSTE, A. (2023). Translocation of the epiphytic bromeliad Vriesea incurvata: an efficient tool for biodiversity restoration in the Atlantic Forest. Brazilian Journal of Environmental Sciences 57(4):677–688.) or stimulating natural colonization by tree planting in different spatial arrangements (Reid et al., 2016REID, J.L., CHAVES-FALLAS, J.M., HOLL, K.D. & ZAHAWI, R.A. (2016). Tropical forest restoration enriches vascular epiphyte recovery. Applied Vegetation Science 19(3):508–517.). Despite limited evidence of success provided by those studies, re-introduction of these plants in forest restoration projects has been recommended, whenever budget restrictions allow (Duarte & Gandolfi 2017DUARTE, M.M. & GANDOLFI, S. (2017). Diversifying growth forms in tropical forest restoration: Enrichment with vascular epiphytes. Forest Ecology and Management 401:89–98.). Little scientific research has been done, however, to evaluate whether spontaneous colonization of planted trees by epiphytes could be enhanced by the selection of a particular group of tree species. Host tree characteristics that favor the colonization and perpetuation of epiphytes might be crucial to assist in planning and decision-making of forest restoration projects, since species’ conservation is utterly dependent on environmental recovery (Reid et al., 2016REID, J.L., CHAVES-FALLAS, J.M., HOLL, K.D. & ZAHAWI, R.A. (2016). Tropical forest restoration enriches vascular epiphyte recovery. Applied Vegetation Science 19(3):508–517.).

Epiphytes are plants which use other plants (phorophytes or hosts) as support in some part of their life cycle, with no soil connection nor using nutrients from the hosts directly (Madison 1977MADISON, M. (1977). Vascular epiphytes: their systematic occurrence and salient features. Selbyana 2(1):1–13., Kress 1986KRESS, J. (1986). The systematic distribution of vascular epiphytes: an update. Selbyana 9(1):2–22.). Epiphytes form a synusiae whose abundance can be related to microclimatic conditions and successional stage, with higher abundance being expected in wetter habitats and mature forests (Richards 1996RICHARDS, P.W. (1996). The tropical rain forest, an ecological study. (2 ed.) Cambridge University Press, Cambridge., Novais et al., 2020NOVAIS, S., SÁYAGO, R., CRISTÓBAL-PEREZ, E.J., SALGUERO-HERNÁNDEZ, G., MARTÉN-RODRÍGUEZ, S., LOPEZARAIZA-MIKEL, M. & QUESADA, M. 2020. Anthropogenic and hurricane disturbances had similar negative effects on epiphytic Tillandsia species in a tropical dry forest. Forest Ecology and Management 458:1–7.). There is scientific evidence for epiphyte preference for certain species of phorophytes (Kersten 2010KERSTEN, R.A. (2010). Epífitas vasculares - Histórico, participação taxonômica e aspectos relevantes, com ênfase na Mata Atlântica. Hoehnea 37(1):9–38., Couto et al., 2022COUTO, D.R., FRANCISCO, T.M. & NASCIMENTO, M.T. (2022). Commensalistic epiphyte–phorophyte networks in woody vegetation of tropical inselbergs: Patterns of organization and structure. Austral Ecology 47(5):911–927.), which indicates a relationship between colonization success and traits of host trees. Bark roughness of the host tree has been considered a relevant trait (Kernan & Fowler 1995KERNAN, C. & FOWLER, N. (1995). Different substrate use by epiphytes in Corcovado National Park, Costa Rica: a source of guild structure. Journal of Ecology 83(1):65–73., Carlsen 2000CARLSEN M. (2000). Structure and diversity of the vascular epiphyte community in the overstory of a tropical rain forest in Surumoni, Amazonas State, Venezuela. Selbyana 21:7–10., Callaway et al., 2002CALLAWAY, R.M., REINHART, K.O., MOORE, G.W., MOORE, D.J. & PENNINGS, S.C. (2002). Epiphyte host preferences and host traits: mechanisms for species-specific interactions. Oecologia 132(2):221–230., Hernandez-Garcia 2021HERNANDEZ-GARCIA, A., ZAVALA-RUIZ, J.M., JAEN-CONTRERAS, D. & BALTAZAR-BERNAL, O. (2021). Laelia anceps Lindl. (Orchidaceae) adaptation on phorophytes within an anthropized landscape. Agro Productividad 14:75–83.), as it determines water retention capacity, which is important in the epiphyte establishment phase (Kersten 2010KERSTEN, R.A. (2010). Epífitas vasculares - Histórico, participação taxonômica e aspectos relevantes, com ênfase na Mata Atlântica. Hoehnea 37(1):9–38.). However, a recent review at global scale (Tay et al., 2023) showed that it is not just about bark roughness, with how an epiphyte attaches itself to the substrate being a crucial issue.

In this study, we assessed three distinct types of forests located in similar environmental conditions: one homogeneous forest plantation of an exotic species (Eucalyptus saligna Sm., Myrtaceae), another of a Brazilian native species (Astronium urundeuva (M.Allemão) Engl., Anacardiaceae), and a native tropical seasonal forest fragment with no evidence of recent disturbance. We aimed at verifying whether epiphyte abundance differs between forest types and between host species as related to their traits. At community level, we expected that epiphyte abundance would be higher in the native forest, given previous studies showing low abundance in monospecific plantations (Hietz 2005HIETZ, P. (2005). Conservation of vascular epiphyte diversity in Mexican coffee plantations. Conservation Biology 19(2):391–399.; Boelter et al., 2011BOELTER, R.C., ZARTMAN, C.E. & FONSECA, C.R. (2011). Exotic tree monocultures play a limited role in the conservation of Atlantic Forest epiphytes. Biodiversity and Conservation 20(6):1255–1272.). Our hypothesis was that tree species diversity permits a higher diversity of organisms that depend on them (Barthlott et al., 2001BARTHLOTT, W., SCHMIT-NEUERBURG, V., NIEDER, J. & ENGWALD, S. (2001). Diversity and abundance of vascular epiphytes: a comparison of secondary vegetation and primary montane rain forest in the Venezuelan Andes. Plant Ecology 152:145–156., Thomsen et al., 2018THOMSEN, M.S., ALTIERI, A.H., ANGELINI, C., BISHOP, M.J., GRIBBEN, P.E., LEAR, G., HE, Q., SCHIEL, D.R., SILLIMAN, B.R., SOUTH, P.M., WATSON, D.M., WERNBERG, T. & ZOTZ, G. (2018). Secondary foundation species enhance biodiversity. Nature Ecology & Evolution 2:634–639., Wagner & Zots 2020WAGNER, K. & ZOTZ, G. (2020). Including dynamics in the equation: Tree growth rates and host specificity of vascular epiphytes. Journal of Ecology 108(2):761–773.). To investigate whether the success of epiphyte colonization can be explained by the traits of the host tree, we explored size (height and stem perimeter), growth rate, canopy deciduousness, and bark roughness as predictors of epiphytes’ presence and abundance. We expected to find a positive relationship of epiphyte colonization with host tree size (Malizia 2003MALIZIA, A. (2003). Host tree preference of vascular epiphytes and climbers in a subtropical montane cloud forest of Northwest Argentina. Selbyana 24(2):196–205., Burns & Dawson 2005BURNS, K.C. & DAWSON, J. (2005). Patterns in the diversity and distribution of epiphytes and vines in a New Zealand Forest. Austral Ecology 30(8):883–891., Hirata et al., 2008HIRATA, A., KAMIJO, T. & SAITO, S. (2008). Host trait preferences and distribution of vascular epiphytes in a warm-temperate forest. In Forest Ecology, Springer, Dordrecht, p.247–254.), because it is a proxy for the substrate surface to be colonized. By favouring epiphyte fixation and water retention, bark roughness (Malizia 2003MALIZIA, A. (2003). Host tree preference of vascular epiphytes and climbers in a subtropical montane cloud forest of Northwest Argentina. Selbyana 24(2):196–205., Wagner et al., 2021WAGNER, K., WANEK, W. & ZOTZ, G. (2021). Functional traits of a rainforest vascular epiphyte community: trait covariation and indications for host specificity. Diversity 13(2):97.) should have a positive effect. Moreover, we expected more epiphytes on slow-growing trees, provided that fast growth could hamper epiphytes’ fixation on the stems (Hirata et al., 2008HIRATA, A., KAMIJO, T. & SAITO, S. (2008). Host trait preferences and distribution of vascular epiphytes in a warm-temperate forest. In Forest Ecology, Springer, Dordrecht, p.247–254.). Because hosts with seasonal deciduous canopy due to seasonal droughts have been reported to have less colonization by epiphytes (Einzmann et al., 2015EINZMANN, H.J., BEYSCHLAG, J., HOFHANSL, F., WANEK, W. & ZOTZ, G. (2015). Host tree phenology affects vascular epiphytes at the physiological, demographic and community level. AoB plants 7, plu073.), we expected that deciduous trees would have lower epiphyte abundance in the studied forests.

Material and Methods

1.

Study site

The three forest types studied form a continuous patch of about 8 ha, located around the stream of a small tributary of the Paranapanema river, between the municipalities of Assis and Tarumã (São Paulo, Brazil), at an average elevation of 520 meters above sea level (Figure 1). Regional climate is Köppen’s Cfa, which is humid subtropical with hot summer (Alvares et al., 2013ALVARES, C.A., STAPE, J.L., SENTELHAS, P.C., GONÇALVES, J.D.M. & SPAROVEK, G. (2013). Köppen’s climate classification map for Brazil. Meteorologische Zeitschrift 22(6):711–728.). The average annual rainfall is 1450 mm, concentrated during summer (December to March), with an average annual temperature of 21.8°C (Durigan & Leitão-Filho 1995DURIGAN, G. & LEITÃO-FILHO, H.F. (1995). Florística e fitossociologia de matas ciliares do oeste paulista. Rev. Inst. Flor. 7:197–239.). Soil type is a clayish and fertile Haplic Lixisol according to WRB (2006)WRB-WORLD REFERENCE BASE FOR SOIL RESOURCES. (2006). World Soil Resources Reports No. 103. FAO, Rome. (Durigan & Leitão-Filho 1995DURIGAN, G. & LEITÃO-FILHO, H.F. (1995). Florística e fitossociologia de matas ciliares do oeste paulista. Rev. Inst. Flor. 7:197–239.). The original vegetation of the region is Seasonal Semideciduous Forest (IBGE 2012INSTITUTO BRASILEIRO DE GEOGRAFIA E ESTATÍSTICA - IBGE (2012) Manual técnico da vegetação brasileira: sistema fitogeográfico, inventário das formações florestais e campestres, técnicas e manejo de coleções botânicas, procedimentos para mapeamento. IBGE- Diretoria de Geociências, Rio de Janeiro.).

The forest types assessed were: (i) a monospecific plantation of aroeira (Astronium urundeuva), with an area of 2.5 ha (central coordinates 22º42’05”S and 50º30’54”W), with native plants colonizing the understory; (ii) a monospecific plantation of eucalyptus (Eucalyptus saligna) with an approximate area of 2.5 ha (central coordinates 22º42’10”S and 50º30’53”W), with abundant regeneration of native plants in its understory; (iii) an old-growth forest remnant, with an area of 3.0 ha (central coordinates 22º42’05”S and 50º31’04”W). E. saligna (henceforth Eucalyptus) is an exotic species widely cultivated in Brazil. A. urundeuva (henceforth Astronium), despite native in the seasonal Atlantic Forest (Souza et al., 2019SOUZA, V.C., TOLEDO, C.P., SAMPAIO, D., BIGIO, N.C., COLLETA, G.D., IVANAUSKAS, N.M. & FLORES, T.B. (2019). Guia das Plantas da Mata Atlântica – Floresta Estacional. Liana, Piracicaba.), has not been recorded in the study region (Durigan et al., 2004DURIGAN, G., SIQUEIRA, M.F., FRANCO, G.A.D.C. & CONTIERI, W.A. (2004). A flora arbustivo-arbórea do médio Paranapanema: base para restauração dos ecossistemas naturais. In: Pesquisas em conservação e recuperação ambiental no Oeste Paulista: resultados da cooperação Brasil/Japão (Vilas Bôas O., Durigan. G., orgs.). Páginas & Letras, São Paulo, p.199–239.).

The precise age of the planted stands could not be rescued, but both were planted simultaneously more than 40 years before sampling. No anthropogenic disturbances have been recorded in the native remnant at least for the last 40 years (Figure 2).

2.

Sampling design and data collection

In each forest type, we sampled five plots of 25 × 8 m (200 m²), 20 m apart from each other, at least 50 m away from the stream margin. In each plot, we identified and measured the stem diameter of all tree individuals with diameter at breast height (DBH) ≥ 5 cm and visually estimated the total height. We measured each stem individually and, to represent tree size in the analyses, we decided to convert the measure of stem diameter into perimeter, summing up them in cases of multi-stemmed trees. Epiphytes rely on bark surface available to be colonized. Therefore, we considered that perimeter would be a more suitable predictor variable to represent substrate surface than the mean diameter, the squared diameter, or the basal area. Should we have used basal area as predictor, for example, we could have risked underestimating available colonizing surface in multi-stemmed trees with similar basal area to single-stemmed trees. Within each forest type we considered all sampled trees as potential hosts, including native species that colonized the understory of the monospecific plantations.

The tree species recorded were functionally classified according to three traits: i) bark roughness (smooth or rough); ii) leaf phenology (deciduous or evergreen), and iii) growth rhythm (fast, moderate, or slow). For bark roughness we used the images from Ramos et al., (2015)RAMOS, V.S., DURIGAN, G., FRANCO, G.A., De SIQUEIRA, M.F. & RODRIGUES, R.R. (2015). Árvores da floresta estacional semidecidual: guia de identificação de espécies. 2nd ed. Edusp, São Paulo.; for leaf phenology, we consulted Backes and Irgang (2002)BACKES, P. & IRGANG, B. (2002). Árvores do Sul: guia de identificação & interesse ecológico; as principais espécies nativas sul-brasileiras. Inst. Souza Cruz, Rio de Janeiro. and the database from Universidade Estadual do Centro Oeste – Unicentro (https://sites.unicentro.br/wp/manejoflorestal/). To categorize the native species by growth rate, we used data taken from the permanent plot network installed since 1992 in the sampled native forest fragment (Giampietro 2005GIAMPIETRO R.L. 2005. Modificações na estrutura e composição florística de matas ciliares na região do Médio Paranapanema (1992-2004). Masters dissertation. Universidade de São Paulo, São Carlos, SP., data available at the BioTime data base Dornelas et al., 2018DORNELAS, M., ANTAO, L.H., MOYES, F., BATES, A.E., MAGURRAN, A.E., ADAM, D., ... ZETTLER, M.L. (2018). BioTIME: A database of biodiversity time series for the Anthropocene. Global Ecology and Biogeography 27(7):760–786.). For Eucalyptus and Astronium, we estimated the mean annual increase in diameter from data obtained in the sampling plots and the approximate age of the stands. Based on the distribution of values among species, we established the categories as: slow growth = annual diameter increment <1.5 mm/yr; moderate growth = 1.5–2.5 mm/yr; and fast growth ≥2.5 mm/yr.

For each sampled tree, we recorded the presence or absence of epiphytes to obtain the percentage of host trees in each forest type. In each host tree, we counted all individuals of established vascular epiphytes. To properly separate individual epiphytes growing in clusters, we considered any clearly delimited group as one single individual, following previous studies (Sanford 1968SANFORD, W.W. 1968. Distribution of epiphytic orchids in semi-deciduous tropical forest in southern Nigeria. Journal of Ecology 56(3):697– 705., Wagner & Zots 2020WAGNER, K. & ZOTZ, G. (2020). Including dynamics in the equation: Tree growth rates and host specificity of vascular epiphytes. Journal of Ecology 108(2):761–773.). When analyzing rhizomatous epiphyte species (creeping habit), rhizome interruption was used as criterium to differentiate individuals. Although we aimed at epiphytes abundance and not composition, we roughly categorized the species in taxonomic groups, to provide an overall characterization of the epiphyte community present in the study areas. As in other studies (Wagner et al., 2015WAGNER, K., MENDIETA-LEIVA, G. & ZOTZ, G. (2015). Host specificity in vascular epiphytes: a review of methodology, empirical evidence and potential mechanisms. AoB plants 7, plu092.), all Pteridophyte species were considered as a single group and the other groups refer to the families recorded.

3.

Data analysis

For each forest type, we calculated the mean values of basal area, host tree density and epiphyte density per hectare. We calculated the frequency (%) of host trees in relation to the total number of individuals sampled in each plot. To compare these variables among forest types, we used analysis of variance (ANOVA), followed by Tukey test.

To explore the relationships between epiphytes and traits of individual trees, we also performed analysis of variance (ANOVA) followed by Tukey test. Data were log-transformed for specific models to meet normality assumptions and to reduce the influence of outliers, the variables transformed were: tree height, stem perimeter and number of epiphytes per tree. For the models assessing the tree height and stem perimeter (response variables) of host and non-host trees (predictor variable) we performed only the log transformation (Quinn & Keough 2002QUINN, G.P. & KEOUGH, M.J. (2002). Experimental design and data analysis for biologists. Cambridge University Press, New York, NY.). For the bark roughness model, we applied log+1 transformation in the response variable number of epiphytes per tree, due to the presence of zero values. To verify whether the abundance of epiphytes was associated with host tree traits, we carried out the analyses of variance (ANOVA) at host species level, to avoid bias due to the large differences in number of host individuals among species. We thus obtained the average number of epiphytes per tree for each host species. We then compared the epiphytes abundance between trait groups as follows: i) slow vs. moderate vs. fast growing, vi) deciduous vs. evergreen, and vii) rough vs. smooth bark.

We checked the assumptions for all models by graphical analyses and performed Levene’s test for homogeneity of variance across groups from car package (Fox & Weisberg 2019FOX, J. & WEISBERG, S. (2019). An R Companion to Applied Regression, Third Edition. Sage, Thousand Oaks CA. URL: https://socialsciences.mcmaster.ca/jfox/Books/Companion/.
https://socialsciences.mcmaster.ca/jfox/... ). All analyses were performed using the R program version 4.1.1 (R Core Team 2021R CORE TEAM. (2021). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/.
https://www.R-project.org/... ), for the Tukey post-hoc test we used the agricolae package (Mendiburu 2021MENDIBURU, F. (2021). Agricolae: Statistical Procedures for Agricultural Research. R package version 1.3–5.).

Results

In the whole area sampled, we recorded a total of 469 trees, from 56 species. Out of these, 197 trees (104 planted and 23 native colonizing species) were sampled in the Astronium stand, 187 trees (43 planted 25 native colonizing species) in the Eucalyptus stand, and 85 trees (31 species) in the native forest. Among the sampled trees, 254 (54%) were hosts, with a total of 3,394 epiphytes counted (see Table 1).

When the forest stands were compared, we found no differences in basal area [Figure 3(a), P = 0.12, with an average of 47.61 m² ha⁻¹ in the native forest, 35.57 m² ha⁻¹ in the Astronium stand, and 24.70 m² ha⁻¹ in the Eucalyptus stand. However, we found differences in epiphyte occurrence. Frequency [Figure 3(b), P = 0.0123], and density [Figure 3(c), P = 0.0059] of trees with epiphytes were both higher in the Astronium stand than in the native forest, not differing from the Eucalyptus stand, which stayed in an intermediate position. The average abundance of epiphytes per hectare in the Astronium stand was higher than in the other two forest types, which did not differ [Figure 3(d), P = 0.0010].

When host and non-host trees were compared (Figure 4), we found significant differences in their size. Average stem perimeter of host trees (51 cm), as a proxy for the substrate area to be colonized, was 46% greater than that of non-host trees (35 cm) [Figure 4(a), P < 0.0001]. Host trees, with average height of 15.2 m, were 50% taller than non-host trees (10.1 m) [Figure 4(b), P < 0.0001].

When we compared the abundance of epiphytes between groups of host species by their traits (Figure 5), we found differences only related to bark roughness. While species with rough bark had an average of 17 epiphytes per tree, those with smooth bark had only 3 epiphytes per tree [Figure 5(a)]. No significant differences were found related to leaf phenology [Figure 5(b), P = 0.67] or growth rhythm [Figure 5(c), P = 1.44] of the host species.

As a rough characterization of the epiphyte community composition, we found, in decreasing order of frequency: Bromeliaceae (in 42% of trees, recorded in all forest types), Pteridophytes (in 34% of trees, in all forest types), Piperaceae (4% of trees, absent in the Eucalyptus stand), Cactaceae (3% of trees, all forest types), and, at last, Orchidaceae and Araceae, both recorded only in the Astronium stand, each one in a single tree sampled (Table 1).

Discussion

Epiphytes presence has been considered a good indicator of forest ecosystem health worldwide (Benzing 1998BENZING, D.H. (1998). Vulnerabilities of tropical forests to climate change: the significance of resident epiphytes. In: Potential impacts of climate change on tropical forest ecosystems. Springer, Dordrecht. p.379–400., Hietz 1999HIETZ, P. (1999). Diversity and conservation of epiphytes in a changing environment. Pure and Applied Chemistry 70:1–11.), but whether epiphyte abundance depends on the host tree traits, and therefore on community composition, is still controversial (Tay et al., 2023). Besides the importance of this issue for plant community ecology, it has practical implications for the real world, since restoring forests became a global challenge (Verdone & Seidl 2017VERDONE, M. & SEIDL, A. (2017). Time, space, place, and the Bonn Challenge global forest restoration target. Restoration ecology 25(6):903–911.). By exploring the epiphyte abundance in a native undisturbed forest in comparison with planted forest stands, our study contributes to the debate within the restoration context. The species diversity to be reintroduced has been an issue in forest restoration for a long time, considered by researchers to be essential for the success of restoration (Ruiz-Jaen & Aide 2005RUIZ-JAEN, M.C. & AIDE, T.M. (2005). Vegetation structure, species diversity, and ecosystem processes as measures of restoration success. Forest Ecology and Management 218(1-3):159–173., Rodrigues et al., 2009RODRIGUES, R.R., LIMA, R.A.F., GANDOLFI, S., NAVE, A.G. (2009). On the restoration of high diversity forests: 30 years of experiences in the Brazilian Atlantic Forest. Biol. Conserv. 142(6):1242–1251., Rodrigues et al., 2011RODRIGUES, R.R., GANDOLFI, S., NAVE, A.G., ARONSON, J., BARRETO, T.E., VIDAL, C.I. & BRANCALION, P.H.S. (2011). Large-scale ecological restoration of high-diversity tropical forests in SE Brazil, Forest Ecology and Management 261(10):1605–1613.). From our results we can infer that selecting the tree species matters, because different species provide different contributions in triggering colonization by epiphytes. Planting a high number of tree species, however, may not assure epiphyte abundance, if the species planted do not have the right traits to be a welcoming host.

1.

Can monospecific forest plantations catalyze colonization by epiphytes?

Several studies have shown that monospecific plantations catalyse colonization by tree species from the regional pool (Parrota et al., 1997PARROTA, J.A., TURNBULL, J.W. & JONES, N. (1997). Catalyzing native forest regeneration on degraded tropical lands. Forest Ecology and Management 99(1-2):1–7., Brockerhoff et al., 2008BROCKERHOFF, E.G., JACTEL, H., PARROTA, J.A., QUINE, C.P. & SAYER, J. (2008). Plantation forests and biodiversity: oxymoron or opportunity? Biodiversity and Conservation 17:925–951., Viani et al., 2010VIANI, R.A.G., DURIGAN, G. & MELO, A.C.G. (2010). A regeneração natural sob plantações florestais: desertos verdes ou redutos de biodiversidade? Ciência Florestal 20(3):533–552., Guerin et al., 2021GUERIN, N., MENDES, F.B.G., CIANCIARUSO, M.V., SUGANUMA, M.S. & DURIGAN, G. (2021). Pure or mixed plantings equally enhance the recovery of the Atlantic Forest. Forest Ecology and Management 484:1–9.), partially corroborating the Field of Dreams hypothesis (Palmer et al., 1997PALMER, M.A., AMBROSE, R.F. & POFF, N.L. (1997). Ecological theory and community restoration ecology. Restoration Ecology 5(4):291–300., Suganuma & Durigan 2021SUGANUMA, M.S. & DURIGAN, G. (2021). Build it and they will come, but not all of them in fragmented Atlantic Forest landscapes. Restoration Ecology 30(4):1–10.). However, this issue has not been explored for life forms other than trees. The only known study for the Atlantic Forest region addressing this issue concluded that monospecific plantations do not favor epiphyte colonization, and monospecific plantations with exotic species tend to be even worse as catalysts for epiphyte colonization (Boelter et al., 2011BOELTER, R.C., ZARTMAN, C.E. & FONSECA, C.R. (2011). Exotic tree monocultures play a limited role in the conservation of Atlantic Forest epiphytes. Biodiversity and Conservation 20(6):1255–1272.).However, we achieved very different results from those found by the cited author. . Refuting our first hypothesis, we found lower frequency of trees with epiphytes and lower abundance of epiphytes per host tree or per hectare in the native forest remnant compared to Astronium plantation (native species). The Eucalyptus stand (exotic species) did not differ from the native forest. We therefore concluded that monospecific stands can be as efficient or even more than the diverse native forest in catalysing epiphytes colonization. The low tree diversity of planted stands, which even after 40 years have lower tree species richness than the native forest, did not result in the expected low abundance of epiphytes. We did not assess epiphyte diversity, however, which could have been affected by tree species richness (Barthlott et al., 2001BARTHLOTT, W., SCHMIT-NEUERBURG, V., NIEDER, J. & ENGWALD, S. (2001). Diversity and abundance of vascular epiphytes: a comparison of secondary vegetation and primary montane rain forest in the Venezuelan Andes. Plant Ecology 152:145–156.).

2.

Does host tree size matter?

Our results support the positive correlation between epiphyte abundance and host size, as found by Malizia (2003)MALIZIA, A. (2003). Host tree preference of vascular epiphytes and climbers in a subtropical montane cloud forest of Northwest Argentina. Selbyana 24(2):196–205., Burns & Dawson (2005)BURNS, K.C. & DAWSON, J. (2005). Patterns in the diversity and distribution of epiphytes and vines in a New Zealand Forest. Austral Ecology 30(8):883–891., (Laube & Zots 2006LAUBE, S. & ZOTZ, G. (2006). Neither host-specific nor random: vascular epiphytes on three tree species in a Panamanian Lowland Forest. Annals of Botany 97(6):1103–1114.), Hirata et al., (2008)HIRATA, A., KAMIJO, T. & SAITO, S. (2008). Host trait preferences and distribution of vascular epiphytes in a warm-temperate forest. In Forest Ecology, Springer, Dordrecht, p.247–254., and Shen et al., (2022)SHEN, T., SONG, L., COLLART, F., GUISAN, A., SU, Y., HU, H., WU, Y. & DONG, J., Vanderpoorten, A. What makes a good phorophyte? Predicting occupancy, species richness and abundance of vascular epiphytes in a lowland seasonal tropical forest. Frontiers in Forests and Global Change 5:1–13.. However, other studies have failed to prove this relationship (Bennet 1986; Zimmerman & Olmstead 1992ZIMMERMAN, J.K. & OLMSTED, I.C. (1992). Host tree utilization by vascular epiphytes in a seasonally inundated forest (Tintal) in Mexico. Biotropica 24(3):402–407., Vergara-Torres et al., 2010VERGARA-TORRES, C.A., PACHECO-ÁLVAREZ, M.C. & FLORES-PALACIOS, A. (2010). Host preference and host limitation of vascular epiphytes in a tropical dry forest of central Mexico. Journal of Tropical Ecology 26(6):563–570.).When comparing the average size between host and non-host trees, we found a large difference, with an advantage for trees with epiphytes both in height (50% larger) and in stem perimeter (46% larger). We used the stem perimeter as the predictor variable because it is more directly correlated to substrate surface than stem diameter or basal area, especially in the cases of multi-stemmed trees. Our result can be explained, therefore, simply by the greater surface available for colonization or by taller trees providing higher light incidence on their trunks (Sillet 1999SILLET, S. (1999). Tree crown structure and vascular epiphyte distribution in Sequoia sempervirens rain forest canopies. Selbyana 20(1):76–97.). However, it can also be indirectly associated with the age of the trees, as larger trees tend to be older within a population, so they had more chances of being colonized, as they were exposed to the colonization process for a longer time. In our study, however, all trees planted within a stand were the same age, restricting this explanation to hosts in the native forest or to those growing in the understory of planted stands, for which differences in size could be related to differences in age.

3.

Are there traits of the host tree favoring epiphytes colonization?

Studies have shown the existence of “functional specificity” (Malizia 2003MALIZIA, A. (2003). Host tree preference of vascular epiphytes and climbers in a subtropical montane cloud forest of Northwest Argentina. Selbyana 24(2):196–205., Wagner et al., 2021WAGNER, K., WANEK, W. & ZOTZ, G. (2021). Functional traits of a rainforest vascular epiphyte community: trait covariation and indications for host specificity. Diversity 13(2):97., Couto et al., 2022COUTO, D.R., FRANCISCO, T.M. & NASCIMENTO, M.T. (2022). Commensalistic epiphyte–phorophyte networks in woody vegetation of tropical inselbergs: Patterns of organization and structure. Austral Ecology 47(5):911–927.), with certain traits of the host tree species turning them into preferred or limiting hosts (Hernandez-Perez et al., 2018). In studies addressing plant-plant interactions, it is not uncommon that host specificity is not proven at the species level, but that hosts show some functional pattern related to the demands of plants that depend on them (Norton & Carpenter 1998NORTON, D.A. & Carpenter, M.A. (1998). Mistletoes as parasites: host specificity and speciation. Trends in Ecology & Evolution 13(3):101–105., Campos et al., 2021). Our study supports the existence of traits favoring epiphytes colonization, with bark roughness standing out, as previously demonstrated by Benzing (1990)BENZING, D.H. (1990). Vascular epiphytes: General Biology and Related Biota. Cambridge University Press, Cambridge., Malizia (2003)MALIZIA, A. (2003). Host tree preference of vascular epiphytes and climbers in a subtropical montane cloud forest of Northwest Argentina. Selbyana 24(2):196–205., and Wagner et al., (2021)WAGNER, K., WANEK, W. & ZOTZ, G. (2021). Functional traits of a rainforest vascular epiphyte community: trait covariation and indications for host specificity. Diversity 13(2):97.. The tridimensional structures in rough bark can give the species a better performance as host (Benzing 1990BENZING, D.H. (1990). Vascular epiphytes: General Biology and Related Biota. Cambridge University Press, Cambridge., Brown 1990BROWN, D.A. (1990). El epifitismo en las selvas montanas del Parque Nacional “El Rey” Argentina: Composición florística y padrón de distribución. Revista de Biologia Tropical 38:155–166., Kersten et al., 2009KERSTEN, R.A., BORGO, M. & SILVA, S.M. (2009). Diversity and distribution of vascular epiphytes in an insular Brazilian coastal forest. Revista de Biologia Tropical 57(3):749–759., Sáyago et al., 2013SÁYAGO, R., LOPEZARAIZA-MIKEL, M., QUESADA, M., ÁLVAREZ-AÑORVE, M.Y., CASCANTE-MARÍN, A. & BASTIDA, J.M. (2013). Evaluating factors that predict the structure of a commensalistic epiphyte–phorophyte network. Proc. R. Soc. B. 280(1756):1–9.). Water retention by rough, porous bark favors the anchorage of bromeliad seeds, promoting their survival and protecting them from drought at early stages (Reyes-Garcia et al., 2008REYES-GARCÍA, C., GRIFFITHS, H., RINCÓN, E., HUANTE, P. (2008). Niche differentiation in tank and atmospheric epiphytic bromeliads of a seasonally dry forest. Biotropica 40(2):168–175., Hietz & Hietz-Seifert 1995HIETZ, P. & HIETZ-SEIFERT, U. (1995). Composition and ecology of vascular epiphyte communities along an altitudinal gradient in central Veracruz, Mexico. Journal of Vegetation Science 6(4):487–498., Castro-Hernandez et al., 1999CASTRO HERNÁNDEZ, J.C., WOLF, J.D., GARCÍA-FRANCO, J.G. & GONZÁLEZ-ESPINOSA, M. (1999). The influence of humidity, nutrients, and light on the establishment of the epiphytic bromeliad Tillandsia guatemalensis in the highlands of Chiapas, Mexico. Revista de Biología Tropical 47(4):763–773., Wolf & Konings 2001WOLF, J.H. & KONINGS, C.J. (2001). Toward the sustainable harvesting of epiphytic bromeliads: a pilot study from the highlands of Chiapas, Mexico. Biological conservation 101(1):23–31., Winkler et al., 2005WINKLER, M., HÜLBER, K. & HIETZ, P. (2005). Effect of canopy position on germination and seedling survival of epiphytic bromeliads in a Mexican humid montane forest. Annals of Botany 95(6):1039–1047., Geraldino et al., 2010GERALDINO, H.C.L., CAXAMBÚ, M.G. & SOUZA, D.C. (2010). Composição florística e estrutura da comunidade de epífitas vasculares em uma área de ecótono em Campo Mourão, PR, Brasil. Acta Botanica Brasilica 24(2):469–482.). Bark traits, therefore, explain the high abundance of epiphytes in the Astronium stand, because this planted species, with its rough bark, corresponds to more than half the trees in the community.

Contrary to our expectations, however, neither tree growth rate nor leaf phenology explained differences in epiphytes abundance among host species. Rasmussem & Rasmussem (2018), in a review about epiphyte habitat, suggested that these plants face the challenge of adapting to a constantly changing environment, so that slow growth could be favorable, but this was also not proven by Hirata et al., (2008)HIRATA, A., KAMIJO, T. & SAITO, S. (2008). Host trait preferences and distribution of vascular epiphytes in a warm-temperate forest. In Forest Ecology, Springer, Dordrecht, p.247–254.. Deciduous canopy is reported to exert a negative influence due to exposing epiphytes to drought conditions in seasonal climates, impairing their establishment and growth (Einzmann et al., 2015EINZMANN, H.J., BEYSCHLAG, J., HOFHANSL, F., WANEK, W. & ZOTZ, G. (2015). Host tree phenology affects vascular epiphytes at the physiological, demographic and community level. AoB plants 7, plu073.). Despite the long dry season in our study sites, deciduousness seemed not to be a relevant trait, since the fully deciduous A. urundeuva was among the most favorable host species.

Conclusion

Comparing old monospecific plantations and an old-growth forest in the same landscape, under the same soil and climate conditions, provided us a unique opportunity to investigate the relationship between epiphyte abundance and the tree community diversity and composition, which are, ultimately, driven by the size and traits of individual trees. We concluded that the abundance of epiphytes per tree in the studied forests is primarily determined by the bark traits, with rough bark favoring colonization by epiphytes, supporting the hypothesis of “functional specificity”. Since bark roughness is an evolutionary trait of the species, it is the proportion of species with smooth or rough bark in the community that will determine the abundance of epiphytes in the forest. The attribute is especially advantageous in seasonal forests, where there is water restriction for part of the year. This finding has relevant implications for management interventions or ecological restoration, in cases where restoring epiphyte populations is among the project’s goals. The expected negative influence of deciduousness on epiphyte abundance was not confirmed in our study, although it may occur in other forests under more stressful climatic conditions.

Although we found a positive correlation between tree size and the number of epiphytes, this correlation is likely more related to the age of the phorophyte than to the intrinsic growth rate of the species, because the abundance of epiphytes per host tree did not differ between slow, moderate, or fast-growing species. It is reasonable to expect, therefore, that the abundance of epiphytes within a forest, whether secondary or restored, will increase over time, until it reaches levels compatible with old-growth forests under similar climatic conditions, with higher abundance being expected in wetter habitats.

Acknowledgments

We thank Roberto de Rezende Barbosa, the landowner of Fazenda Berrante, for allowing us to carry out this study, and for providing us historical information about the studied forests. We also thank Natashi A.L. Pilon for helping us with data analyses, and Rodolfo C.R. Abreu for insightful suggestions on the draft of this manuscript.

G.D. and VLE thank the National Council of Scientific and Technological Development – CNPq for productivity grants (#309709/2020-2 and #310089/2020-4, respectively).

Data Availability

All data collected and used to base our analysis, and therefore, this study, are available in the Dataverse at https://doi.org/10.48331/scielodata.5E2RBE.

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