Abstract

Vascular epiphytes stand out in tropical forests in terms of diversity. However, no comprehensive review of the group in the Amazon region has been performed so far. We carried out a literature review on the scientific knowledge of vascular epiphytes in the Amazon aiming to identify the main gaps, limitations and perspectives for studies on the subject. Searches were conducted in Google Scholar, Scopus and Web of Science using inclusion and exclusion criteria. 291 articles published in the period 1933-2022, mostly the 21st century, were included in the review. Brazil was the most studied country. However, knowledge gaps were found in regions located in the Brazilian arc of deforestation as well as in areas of Bolivia, Guyana, French Guiana and Suriname. There was a predominance of studies related to the floristics, systematics and biogeography of spermatophytes and ferns, focusing on the diversity and taxonomy of certain families (e.g. Orchidaceae). However, we found gaps for more comprehensive research, considering population dynamics, dominance (biomass), guidelines for evaluation of epiphyte and systematization of data for Amazon. We indicate the need of studies focused on ecology, floral and reproductive biology, biochemistry, phytochemistry, anatomy and physiology. Future research should also consider the impacts of current trends in deforestation and climatic changes on the diversity of vascular epiphytes in the Amazon.

Keywords:
Amazon; Amazon rainforest; Brazil; diversity; epiphytism; fern; orchids; scientometric; systematic review; vascular epiphytes

Introduction

Vascular epiphytes, defined as plants that germinate and grow on trees in a non-parasitic relationship, are a highly diverse group in tropical forests represented by ca. 31,000 species distributed in 79 families, wich corresponds to about 10% of the vascular plant species of the world (Zotz 2016Zotz G. 2016. Plants on plants - the biology of vascular epiphytes. Oldenburg, Springer.; Zotz et al. 2021Zotz G, Weigelt P, Kessler M, Kreft H, Taylor A. 2021. EpiList 1.0: a global checklist of vascular epiphytes. Ecology 102: e03326. doi: 10.1002/ecy.3326.
https://doi.org/10.1002/ecy.3326... ). A total of 3,849 epiphytic species occurs in the neotropics and 518 epiphytic species occurs in the Amazon (Marcusso et al. 2022Marcusso GM, Kamimura V, Borgiani R, Menini Neto L, Lombardi JA. 2022. Phytogeographic meta-analysis of the vascular epiphytes in the Neotropical region. The Botanical Review 88: 388-412. doi: 10.1007/s12229-021-09270-2.
https://doi.org/10.1007/s12229-021-09270... ; Quaresma et al. 2022Quaresma A, Zartman CE, Piedade MTF et al. 2022. The Amazon epiphyte network: a first glimpse into Continental-Scale patterns of Amazonian vascular epiphyte assemblages. Frontiers in Forests and Global Change 5: 828759. doi: 10.3389/ffgc.2022.828759.
https://doi.org/10.3389/ffgc.2022.828759... ). Epiphytic species are of major ecological importance, as they act as a source of organic matter by generating litter, contribute to nutrient cycling and rainfall interception, and serve as habitats and food resources for animals, favoring the diversification of the canopy fauna (Benzing 1990Benzing DH. 1990. Vascular epiphytes: General biology and related biota. Cambridge, Cambridge University Press. ; Kersten 2010Kersten RA. 2010. Epífitas vasculares - Histórico, participação taxonômica e aspectos relevantes, com ênfase na Mata Atlântica. Hoehnea 37: 9-38.; Mendieta-Leiva et al. 2020a Mendieta-Leiva G, Ramos FN, Elias JPC et al. 2020a. EpIG-DB: A database of vascular epiphyte assemblages in the Neotropics. Journal of Vegetation Science 31: 518-528. doi: 10.1111/jvs.12867.
https://doi.org/10.1111/jvs.12867... ; Taylor et al. 2021Taylor A, Zotz G, Weigelt P, Cai L, Karger DK, König C, Kreft H. 2021. Vascular epiphytes contribute disproportionately to global centres of plant diversity. Global Ecology and Biogeography 31: 62-74. doi: 10.1111/geb.13411.
https://doi.org/10.1111/geb.13411... ).

Despite the high taxonomic diversity, vascular epiphytes are poorly studied when compared to other components of the forest (Mendieta-Leiva & Zotz 2015Mendieta-Leiva G, Zotz G. 2015. A conceptual framework for the analysis of vascular epiphyte assemblages. Perspectives in Plant Ecology, Evolution and Systematics 17: 510-521. doi: 10.1016/j.ppees.2015.09.003.
https://doi.org/10.1016/j.ppees.2015.09.... ; Zotz 2016Zotz G. 2016. Plants on plants - the biology of vascular epiphytes. Oldenburg, Springer.). Studies about this synusia in the Amazon are also incipient when compared to those carried out in Central America and in the southeast and southern Brazil (Mendieta-Leiva et al. 2020a Mendieta-Leiva G, Ramos FN, Elias JPC et al. 2020a. EpIG-DB: A database of vascular epiphyte assemblages in the Neotropics. Journal of Vegetation Science 31: 518-528. doi: 10.1111/jvs.12867.
https://doi.org/10.1111/jvs.12867... ). Furthermore, the factors that influence the occurrence and diversity of epiphytes are still not completely clear (Mendieta-Leiva & Zotz 2015Mendieta-Leiva G, Zotz G. 2015. A conceptual framework for the analysis of vascular epiphyte assemblages. Perspectives in Plant Ecology, Evolution and Systematics 17: 510-521. doi: 10.1016/j.ppees.2015.09.003.
https://doi.org/10.1016/j.ppees.2015.09.... ; 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. doi: 10.1093/aobpla/plu092.
https://doi.org/10.1093/aobpla/plu092... ; Zotz 2016Zotz G. 2016. Plants on plants - the biology of vascular epiphytes. Oldenburg, Springer.; Spicer & Woods 2022Spicer ME, Woods CL. 2022. A case for studying biotic interactions in epiphyte ecology and evolution. Perspectives in Plant Ecology, Evolution and Systematics 54: 125658. doi: 10.1016/j.ppees.2021.125658.
https://doi.org/10.1016/j.ppees.2021.125... ).

Systematic reviews are scientific investigations based on explicit and reproducible methods that allow us to synthesize results from a comprehensive search of relevant articles on a given topic, enabling careful evaluation and interpretation to provide the current state of the art or focus of the research on the theme (Grant & Booth 2009Grant MJ, Booth A. 2009. A typology of reviews: an analysis of 14 review types and associated methodologies. Health Information & Libraries Journal 26: 91-108. doi: 10.1111/j.1471-1842.2009.00848.x.
https://doi.org/10.1111/j.1471-1842.2009... ; Mengist et al. 2020aMengist W, Soromessa T, Legese G. 2020a. Method for conducting systematic literature review and meta-analysis for environmental science research. MethodsX 7: 100777. doi: 10.1016/j.mex.2019.100777.
https://doi.org/10.1016/j.mex.2019.10077... ). There are several literature reviews articles that help us understand the importance of epiphytes and the diversity of the group (Kersten 2010Kersten RA. 2010. Epífitas vasculares - Histórico, participação taxonômica e aspectos relevantes, com ênfase na Mata Atlântica. Hoehnea 37: 9-38.; 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. doi: 10.1093/aobpla/plu092.
https://doi.org/10.1093/aobpla/plu092... ; Ladino et al. 2019Ladino G, Ospina‐Bautista F, Varón JE, Jerabkova L, Kratina P. 2019. Ecosystem services provided by bromeliad plants: A systematic review. Ecology and Evolution 9: 7360-7372. doi: 10.1002/ece3.5296.
https://doi.org/10.1002/ece3.5296... ; Jover et al. 2020Jover A, Ramos A, Cabrera A, Suárez AM, Machell J, Pérez-Lloréns JL. 2020. Epiphytic macroalgae and hosts of the marine shelf of Cuba: Current status, composition and diversity. Regional Studies in Marine Science 34: 101108. doi: 10.1016/j.rsma.2020.101108.
https://doi.org/10.1016/j.rsma.2020.1011... ; Khapugin 2020Khapugin AA. 2020. A global systematic review on orchid data in protected areas. Nature Conservation Research 5:19-33. doi: 10.24189/ncr.2020.019.
https://doi.org/10.24189/ncr.2020.019... ; Nugraha et al. 2020Nugraha AS, Triatmoko B, Wangchuk P, Keller PA. 2020. Vascular epiphytic medicinal plants as sources of therapeutic agents: Their ethnopharmacological uses, chemical composition, and biological activities. Biomolecules 10: 181. doi: 10.3390/biom10020181.
https://doi.org/10.3390/biom10020181... ; Spicer & Woods 2022Spicer ME, Woods CL. 2022. A case for studying biotic interactions in epiphyte ecology and evolution. Perspectives in Plant Ecology, Evolution and Systematics 54: 125658. doi: 10.1016/j.ppees.2021.125658.
https://doi.org/10.1016/j.ppees.2021.125... ), but no one of them has specifically focused on the vascular epiphytes of the Amazon. Moreover, large gaps in floristic-taxonomic inventories of this group in the region have been pointed out by some authors (e.g. Mendieta-Leiva et al. 2020a Mendieta-Leiva G, Ramos FN, Elias JPC et al. 2020a. EpIG-DB: A database of vascular epiphyte assemblages in the Neotropics. Journal of Vegetation Science 31: 518-528. doi: 10.1111/jvs.12867.
https://doi.org/10.1111/jvs.12867... ; Quaresma et al. 2022Quaresma A, Zartman CE, Piedade MTF et al. 2022. The Amazon epiphyte network: a first glimpse into Continental-Scale patterns of Amazonian vascular epiphyte assemblages. Frontiers in Forests and Global Change 5: 828759. doi: 10.3389/ffgc.2022.828759.
https://doi.org/10.3389/ffgc.2022.828759... ).

Therefore, the objective of the present study was to summarize the scientific knowledge about vascular epiphytes in the Amazon so as to identify the main limitations, gaps, and perspectives for researches on the theme.

Material and methods

The research was carried out using the SALSA (Search, Appraisal, Synthesis, and Analysis) methodology (Grant & Booth 2009Grant MJ, Booth A. 2009. A typology of reviews: an analysis of 14 review types and associated methodologies. Health Information & Libraries Journal 26: 91-108. doi: 10.1111/j.1471-1842.2009.00848.x.
https://doi.org/10.1111/j.1471-1842.2009... ) and the PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) research protocol (Moher et al. 2009Moher D, Liberati A, Tetzlaff J, Altman DG. 2009. Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. The BMJ 8: 336-341. doi: 10.1136/bmj.b253.
https://doi.org/10.1136/bmj.b253... ) with data obtained from the Google Scholar, Scopus and Web of Science databases. We adopted search terms (keywords) related to vascular epiphytes in the Amazon, which included the six most representative families of epiphytes in the Amazon (Orchidaceae, Araceae, Bromeliaceae, Polypodiaceae, Clusiaceae, and Dryopteridaceae; Taylor et al. 2021Taylor A, Zotz G, Weigelt P, Cai L, Karger DK, König C, Kreft H. 2021. Vascular epiphytes contribute disproportionately to global centres of plant diversity. Global Ecology and Biogeography 31: 62-74. doi: 10.1111/geb.13411.
https://doi.org/10.1111/geb.13411... ; Quaresma et al. 2022Quaresma A, Zartman CE, Piedade MTF et al. 2022. The Amazon epiphyte network: a first glimpse into Continental-Scale patterns of Amazonian vascular epiphyte assemblages. Frontiers in Forests and Global Change 5: 828759. doi: 10.3389/ffgc.2022.828759.
https://doi.org/10.3389/ffgc.2022.828759... ) and the types of Amazonian vegetation, according to surveys carried out in the region (Fig. 1) (Junk et al. 2011Junk WJ, Piedade NTF, Schöngart J, Cohn-Haft M, Adeney JM, Wittmann F. 2011. A classification of major naturally-occurring Amazonian lowland wetlands. Wetlands 31: 623-640. doi: 10.1007/s13157-011-0190-7.
https://doi.org/10.1007/s13157-011-0190-... ; Cardoso et al. 2017Cardoso AD, Särkinen T, Alexander S et al. 2017. Amazon plant diversity revealed by a taxonomically verified species list. Proceedings of the National Academy of Sciences 114: 10695-10700. doi: 10.1073/pnas.1706756114.
https://doi.org/10.1073/pnas.1706756114... ; Quaresma et al. 2022Quaresma A, Zartman CE, Piedade MTF et al. 2022. The Amazon epiphyte network: a first glimpse into Continental-Scale patterns of Amazonian vascular epiphyte assemblages. Frontiers in Forests and Global Change 5: 828759. doi: 10.3389/ffgc.2022.828759.
https://doi.org/10.3389/ffgc.2022.828759... ).

All articles published until 2022 were retrieved and subjected to application of inclusion and exclusion criteria in order to allow the collection and analysis of the maximum number of publications (Moher et al. 2009Moher D, Liberati A, Tetzlaff J, Altman DG. 2009. Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. The BMJ 8: 336-341. doi: 10.1136/bmj.b253.
https://doi.org/10.1136/bmj.b253... ; Mengist et al. 2020aMengist W, Soromessa T, Legese G. 2020a. Method for conducting systematic literature review and meta-analysis for environmental science research. MethodsX 7: 100777. doi: 10.1016/j.mex.2019.100777.
https://doi.org/10.1016/j.mex.2019.10077... ). Studies carried out in any of the nine countries where the Pan-Amazon occurs (Bolivia, Brazil, Colombia, Ecuador, Guyana, French Guiana, Peru, Venezuela and Suriname) (Aragón 2018Aragón LE. 2018. A dimensão internacional da Amazônia: Um aporte para sua interpretação. Revista NERA 42: 15-33.) were included in the analysis as long as the predefined search terms had been found in the title, abstract or keywords. When necessary, the articles were read in full to check whether they were within the scope of the review. Articles that were unrelated to the proposed theme, articles produced outside the study area (Amazon), duplicate articles, presentations, lectures, expanded abstracts, dissertations, theses, and review articles were excluded (Mengist et al. 2020aMengist W, Soromessa T, Legese G. 2020a. Method for conducting systematic literature review and meta-analysis for environmental science research. MethodsX 7: 100777. doi: 10.1016/j.mex.2019.100777.
https://doi.org/10.1016/j.mex.2019.10077... ).

The selected articles were classified as quantitative or descriptive to carry out a narrative analysis of the data. We extracted the following information of each article: (1) year of publication; (2) country where the study was conducted; (3) coordinates of the study site; (4) keywords; (5) category of the study [based on the thematic areas of the most recent Brazilian Botanical Congress (Congresso Nacional de Botânica 2022Congresso Nacional de Botânica. 2022. Botânica: Para que e para quem? Desafios, avanços e perspectivas na sociedade contemporânea. In: Anais do 72º Congresso Nacional de Botânica, realizado de 24 a 28 de outubro de 2022. Sociedade Botânica do Brasil, Feira de Santana.)]; (6) sampling methodology; (7) journal where the article was published and Impact Factor of the journals indexed in the Journal Citation Reports (JCR), considering the year 2021 as a reference (https://clarivate.com/); (8) number of citations; and (9) affiliation and country of origin of the authors.

Raw data were tabulated in Excel 2018 spreadsheets and organized into graphs and tables with the aid of the R software (R CORE TEAM 2022R CORE TEAM. 2022. R: A language and environment for statistical computing. R Foundation for Statistical Computing. https://www.Rproject.org/. 10 Nov 2022.
https://www.Rproject.org/... ), using the Bibliometrix extension (biblioshyne) (Aria & Cuccurullo 2017Aria M, Cuccurullo C. 2017. Bibliometrix: An R-tool for comprehensive science mapping analysis. Journal of Informetrics 11: 959-975. ). We also prepared a map with the study locations based on geographic coordinates (latitude and longitude), when available in the articles. When the coordinates were not available, we used less precise information, such as municipality or locality to arbitrarily assign the location where these studies were carried out using Google Maps (https://www.google.com/maps) (Magdalena et al. 2018Magdalena UR, Silva LAE, Lima RO et al. 2018. A new methodology for the retrieval and evaluation of geographic coordinates within databases of scientific plant collections. Applied Geography 96:11-15. doi: 10.1016/j.apgeog.2018.05.002.
https://doi.org/10.1016/j.apgeog.2018.05... ).

Results

Temporal and spatial distribution of the studies

The searches resulted in a total of 3,980 articles: 3,479 from Google Scholar, 276 from the Web of Science, and 225 from Scopus. After application of the exclusion criteria, 291 articles - 155 retrieved from Google Scholar and 136 from the Web of Science and/or Scopus - about epiphytes in the Amazon were obtained. The 291 articles were published in 115 journals, from 1933 to 2022 (Fig. 2), associated with 646 authors. Regarding the language, English was the most used (195 articles), followed by Portuguese (71) and Spanish (25).

The first study of vascular epiphytes in the Amazon dates back to 1933 and it was a pioneering survey to describe the vegetation, including vascular and non-vascular plants, and environmental characteristics of Moraballi Creek, in the Cuyuni-Mazaruni region in Guyana (Davis & Richards 1933Davis TAW, Richards PW. 1933. The Vegetation of Moraballi Creek, British Guiana: An Ecological Study of a Limited Area of Tropical Rain Forest. Part I. Journal of Ecology 21: 350-384.). After this initial milestone, the next study was published only in 1963. Until 1999, publications on epiphytes from the Amazon were few and restricted to one or two articles per year. From 2000, there was a significant increase (p<0.001) in the number of studies, especially in 2014, 2020 and 2022 with 25, 23 and 22 published articles, respectively, although in 2021 the publications have decreased, totalizing only 10 articles.

Most studies were conducted in Brazil (53%, 154 articles), followed by Colombia (12%, 34 articles), Ecuador (8%, 23 articles), Peru (7 %, 21 articles), and Venezuela (4%, 11 articles). We highlight the low scientific production in punctual areas of the Brazilian Amazon (such as in the states of Maranhão and Tocantins and the south of the states of Amazonas and Pará), and also in Bolivia, Guyana and French Guiana, in addition to the absence of studies in Suriname (Fig. 3). Some studies were conducted in two or more Amazonian countries, such as the one presented by Cascante-Marin and Nivia-Ruiz (2013Cascante-Marin A, Nivia-Ruiz A. 2013. Neotropical flowering epiphyte diversity local composition and geographic affinities. Biodiversity and Conservation 12: 113-125. doi: 10.1007/s10531-012-0404-1.
https://doi.org/10.1007/s10531-012-0404-... ), which included floristic data from Peru and Ecuador and from six other non-Amazonian countries, and Quaresma et al. (2022Quaresma A, Zartman CE, Piedade MTF et al. 2022. The Amazon epiphyte network: a first glimpse into Continental-Scale patterns of Amazonian vascular epiphyte assemblages. Frontiers in Forests and Global Change 5: 828759. doi: 10.3389/ffgc.2022.828759.
https://doi.org/10.3389/ffgc.2022.828759... ), which included information on epiphytes from 32 localities in Brazil, Colombia, Guyana and French Guiana. We also highlight the study by Kessler (2001Kessler M. 2001. Pteridophyte species richness in Andean forests in Bolivia. Biodiversity and Conservation 10: 1473-1495. doi: 10.1023/A:1011811224595.
https://doi.org/10.1023/A:1011811224595... ), who conducted an extensive assessement of the richness of ferns in 65 study sites in Bolivia and found that 56% of the surveyed species were epiphytes.

Among the 291 articles analyzed in this review, 62 were carried out in 30 conservation units of six countries (Table 1), especially in Brazil. Among the conservation units, the epiphytic floras of the Combu Island Environmental Protection Area and Caxiuanã National Forest, both in the state of Pará, and the Adolpho Ducke Forest Reserve, in the state of Amazonas, were the most studied, resulting in a total of 21 articles.

Keywords and categories of studies

A total of 2,360 keywords in English, Portuguese and Spanish (Fig. 4A) corresponding to 741 words in English were evaluated. The five most cited and with the highest number of co-occurrences were: “Amazon”, “Taxonomy”, “Epiphyte”, “Orchidaceae”, and “Diversity” (Fig. 4B). This result reflects the predominance of taxonomic studies and studies related to the diversity of epiphytes from Amazonian forests, in which Orchidaceae stands out among the families. The keywords and the approach of the studies allowed us to classify them in four categories: (1) systematics, floristics and/or biogeography of spermatophytes (195 articles); (2) systematics, floristics and/or biogeography of ferns (43 articles); (3) ecology, floral and/or reproductive biology (33 articles); and (4) biochemistry, phytochemistry, anatomy and/or physiology (20 articles) (Fig. 5).

A total of 67% of the articles were classified in the category one (systematics, floristics and/or biogeography of spermatophytes), which has been the main approach since the beginning of the studies. In turn, research related to other categories has declined in recent years. Among the articles classified in the category one, 101 correspond to floristic surveys and 89 are taxonomic studies. The former consist of checklists of vascular epiphytes resulting from inventories of the whole angiosperm flora or specific taxa (e.g. Araceae, Bromeliaceae or Orchidaceae) carried out in different areas and ecosystems of the Amazon, including information about the response of the floristic composition of the group to environmental changes, such as opening of roads (McCracken & Forstner 2014Mccracken SF, Forstner MR. 2014. Oil Road Effects on the Anuran Community of a High Canopy Tank Bromeliad (Aechmea zebrina) in the Upper Amazon Basin, Ecuador. PLoS One 9: e85470. doi: 10.1371/journal.pone.0085470.
https://doi.org/10.1371/journal.pone.008... ) and intensive management of açaí (Euterpe oleracea Mart.) (Quaresma & Jardim 2013Quaresma AC, Jardim MAG. 2013. O manejo do açaizeiro, Euterpe oleracea Mart., influencia a diversidade de bromélias epífitas em floresta de várzea? Biota Amazônia 3: 94-100. ; Ferreira-Filho et al. 2021Ferreira-Filho R, Barberena FVA, Costa JM. 2021. Orchidaceae in floodplains of the islands of Abaetetuba amazonian Brazil: a flora threatened by intensive management for açaí palm (Euterpe oleracea). Brittonia 73: 1-24. doi: 10.1007/s12228-020-09647-4.
https://doi.org/10.1007/s12228-020-09647... ). Besides the list of species, some of these articles also provide information on the local richness; abundance; spatial, vertical, horizontal and geographic distribution; spatial and temporal variation; and phytosociological structure of the epiphytes.

Studies with a taxonomic focus consisted of revisions, often covering the phylogeny or geographic distribution of the species, taxonomic notes, descriptions of new species, hybrid taxa, or new records from a given region or state. Most of the new species described in the articles are of the family Orchidaceae, especially of the genera Anathallis Barb. Rodr. (A. amazonica E. Pessoa & M. Alves, A. manausensis Krahl, Valsko & Chiron, and A. roseopapillosa E. Pessoa & J.J. Valsko), Catasetum Rich. ex Kunth [Catasetum × sheyllae (natural hybrid), C. sophiae Valsko, Krahl & Benelli, C. colidense M.E. Engels, C. kamatawara Damián, Mitidieri & Bonilla, and C. telespirense Benelli & Soares-Lopes], Dichaea Lindl. (D. bragae Valsko, Krahl & Holanda and D. integrilabia Valsko, Krahl & Chiron), and Epidendrum L. (E. aromoense X. Cornejo & E. Hágsater, E. dayseae Krahl & Hágsater, E. deditae Hágsater & Krahl, and E. olorteguii Damián, Hágsater & Mitidieri). These studies also include descriptions, illustrations and photographic records of type species, identification keys, nomenclatural discussions, and data on habitats, phenology and conservation.

There were descriptions of new species also of the families Araceae and Bromeliaceae, of the genera Heteropsis Kunth from Brazil [H. croatii M.L. Soares and H. robusta (G.S. Bunting) M.L. Soares)] (Soares et al. 2009Soares ML, Mayo SJ, Croat TB, Gribel R. 2009. Two new species and a new combination in Amazonian Heteropsis (Araceae). Kew Bull 64: 263-270. doi: 10.1007/s12225-009-9113-7.
https://doi.org/10.1007/s12225-009-9113-... ), Anthurium Schott (A. peregrinense O. López-Floriano, Croat & M. Correa) and Aechmea Ruiz & Pav. from Colombia (A. baudoensis Aguirre-Santoro & Betancur, A. confertiflora Aguirre-Santoro & Betancur, A. longipedunculata Betancur & Aguirre-Santoro, A. longiramosa Betancur & Aguirre-Santoro, A. viridispica Aguirre-Santoro & Betancur) (Aguirre-Santoro & Betancur 2011Aguirre-Santoro J, Betancur J. 2011. Cinco especies nuevas de Aechmea (Bromeliaceae: Bromelioideae) para Colombia. Brittonia 63: 300-313. doi: 10.1007/s12228-010-9169-6.
https://doi.org/10.1007/s12228-010-9169-... ; López-Floriano et al. 2022López-Floriano OM, Croat TB, Correa-Munera MA. 2022. A new species of Anthurium sect. Leptanthurium from Colombian Amazonia. Phytotaxa 572: 217-221. doi: 10.11646/phytotaxa.572.2.9 217.
https://doi.org/10.11646/phytotaxa.572.2... ). Among the new records of occurrence, Scaphyglottis punctulata (Rchb.f.) C. Schweinf., formerly restricted to highlands from Panama to Bolivia, was recorded in the Guiana Shield, in Brazil by Araújo et al. (2022Araújo AMA, Farroñay F, Perdiz RO, Pessoa E, Giacomin L. 2022. The discovery of Scaphyglottis punctulata (Laeliinae) in the highlands of brazilian amazonia with a key to the species of the region. Lankesteriana 22: 123-131. doi: 10.15517/lank.v22i2.51844.
https://doi.org/10.15517/lank.v22i2.5184... ), and some species of Araceae (Philodendron uleanum Engl.) and Orchidaceae [Catasetum hopkinsonianum G.F. Carr & V.P. Castro, Notylia peruviana (Schltr.) C. Schweinf., and Platystele edmundoi Pabst], previously reported to the states of Pará and Rondônia in Brazil and to other countries, were recorded in the state of Mato Grosso, Brazil, by Petini-Benelli et al. (2015Petini-Benelli A, Soares-Lopes CR, Silva D, Ribeiro R. 2015. Novos registros de epífitas vasculares para o estado de Mato Grosso, Brasil. Enciclopédia Biosfera 11: 2340-2351. ).

In the category two (“systematics, floristics and/or biogeography of ferns”), descriptive studies of the fern flora of Serra dos Carajás in the state of Pará (Moura & Salino 2016Moura IO, Salino A. 2016. Flora das cangas da Serra dos Carajás, Pará, Brasil: Dryopteridaceae. Rodriguésia 67: 1151-1157. doi: 10.1590/2175-7860201667509.
https://doi.org/10.1590/2175-78602016675... ) and Cuniã Ecological Station in the state of Rondônia (Sampaio et al. 2020Sampaio AF, Oliveira AE, Andrade RTG, Mazatto AG. 2020. Aspleniaceae (Polypodiales) da Estação Ecológica do Cuniã, Porto Velho, Estado de Rondônia, Brasil. Acta Biologica Catarinense 7: 28-36. doi: 10.21726/abc.v7i3.132.
https://doi.org/10.21726/abc.v7i3.132... ), both in Brazil, stood out. Some studies also included other epiphytic organisms such as bryophytes and macrolichens, which commonly grow intermingled in tropical forests (Mandl et al. 2010Mandl N, Lehnert M, Kessler M, Gradstein SR. 2010. A comparison of alpha and beta diversity patterns of ferns, bryophytes and macrolichens in tropical montane forests of southern Ecuador. Biodiversity and Conservation 19: 2359-2369. doi: 10.1007/s10531-010-9839-4.
https://doi.org/10.1007/s10531-010-9839-... ). Mandl et al. (2010)Mandl N, Lehnert M, Kessler M, Gradstein SR. 2010. A comparison of alpha and beta diversity patterns of ferns, bryophytes and macrolichens in tropical montane forests of southern Ecuador. Biodiversity and Conservation 19: 2359-2369. doi: 10.1007/s10531-010-9839-4.
https://doi.org/10.1007/s10531-010-9839-... demonstrated that epiphytic ferns are positively related to epiphytic liverworts and mosses in terms of diversity patterns in montane forests of Podocarpus National Park, Ecuador. The patterns of occurrence of epiphytic ferns in areas with different degrees of anthropic disturbance were the focus of the study by Oldekop et al. (2012Oldekop AJ, Bebbington AJ, Truelove NK, Tysklind N, Villamarín S, Preziosi RF. 2012. Co-occurrence patterns of common and rare leaf-litter frogs, epiphytic ferns and dung beetles across a gradient of human disturbance. PLoS One 7: e38922. doi:10.1371/journal.pone.0038922.
https://doi.org/10.1371/journal.pone.003... ) in Sumaco Biosphere Reserve (Ecuador), which demonstrated the dominance of common species in areas of secondary succession.

In the categories one and two, the most common methodologies used in floristic surveys included field expeditions and the establishment of plots, varying in number, shape and size. The evaluation of a predefined number of trees (phorophytes) was less frequent (only five studies). The consultation and analysis of herbarium specimens before field surveys was frequent in taxonomic studies.

The articles classified in the category three (ecology, floral and/or reproductive biology), focused predominantly on the families Araceae, Orchidaceae and Bromeliaceae. Micropropagation, in vitro germination and development, survival, growth, reproduction, vegetative propagation, and sustainability of extractivism and its impact on hemiepiphytes (specimens of the Araceae family) were the topics addressed. Werner and Gradstein (2008Werner FA, Gradstein SR. 2008. Seedling establishment of vascular epiphytes on isolated and enclosed forest trees in an Andean landscape, Ecuador. Biodiversity and Conservation 17: 3195-3207. doi: 10.1007/s10531-008-9421-5.
https://doi.org/10.1007/s10531-008-9421-... ), for example, investigated the relocation and survival of epiphyte species in rescue actions, which depend on microclimatic factors (temperature and humidity), phorophyte characteristics, and degree of forest isolation. Interactions between vascular epiphytes and animals were also addressed in some studies. The association with ants was reported in six articles. For example, Gibernau et al. (2007Gibernau M, Orivel J, Delabie JHC, Barabé D, Dejean A. 2007. An asymmetrical relationship between an arboreal ponerine ant and a trash-basket epiphyte (Araceae). Biological Journal of the Linnean Society 91: 341-346. doi: 10.1111/j.1095-8312.2007.00799.x.
https://doi.org/10.1111/j.1095-8312.2007... ) inventoried 44 ant species in 90% of the individuals of Philodendron insigne Schott (Araceae) evaluated. According to the authors, this association provides indirect protection to plants against herbivory and rewards ants through shelter or food resources (extrafloral nectaries of the plant).

In the articles classified in the category four (biochemistry, phytochemistry, anatomy and/or physiology), the chemical composition of oils from specimens of the genus Philodendron Schott [P. fragrantissimum (Hook.) G. Don, P. goeldii G.M. Barroso, P. maximum K. Krause, P. solimoesense A.C. Sm. and P. scabrum K. Krause] and the family Piperaceae [Peperomia serpens (Sw.) Loudon] were analyzed. Silva et al. (2016Silva JIM, Silva JIM, Souza MCS, Soares MLC, Costa RC. 2016. Óleos essenciais das raízes das espécies de Philodendron maximum, P. solimoesense e P. goeldii (Araceae). Revista Fitos 10: 1-93. doi: 10.5935/2446-4775.2016000877.
https://doi.org/10.5935/2446-4775.201600... ) showed that the chemical components present in extracts from these species have medicinal potential (antioxidant and antimicrobial) and possible pharmacological applications. We found only one published study in the area of phytochemistry, by Martinson et al. (2018Martinson GO, Pommerenke B, Brandt FB, Homeier J, Burneo JI, Conrad R. 2018. Hydrogenotrophic methanogenesis is the dominant methanogenic pathway in neotropical tank bromeliad wetlands. Environmental Microbiology Reports 10: 33-39. doi: 10.1111/1758-2229.12602.
https://doi.org/10.1111/1758-2229.12602... ), who evaluated the production rate of methane gas (CH₄) of bromeliads in mountainous tropical forests in Southern Ecuador (Reserva San Francisco).

The anatomical studies analyzed the vegetative organs (leaves, scapes, roots and velamen) of specimens of Bromeliaceae, Dryopteridaceae and Orchidaceae. We highlight the study by Silva et al. (2015Silva IV, Oliveira RM, Rossi AAB, Silva AB, Oliveira DM. 2015. Use of anatomical root markers for species identification in Catasetum (Orchidaceae) at the Portal da Amazonia region, MT, Brazil. Acta Amazonica 45: 21-28. doi: 10.1590/1809-4392201401832.
https://doi.org/10.1590/1809-43922014018... ), who performed the anatomical characterization of the roots of eight species of Catasetum collected in Mato Grosso, Brazil, and identified adaptations to the epiphytic habit (e.g. morphophysiological changes in the cells of the velamen, exodermis, cortex and medulla). However, this study aimed to contribute to the taxonomic identification of the genus, which reinforces the predominance of studies with taxonomic purposes.

Journals and citations

Most articles were published in journals dedicated to systematics and taxonomy (Phytotaxa and Rodriguésia), general biology (Acta Botanica Brasilica and Acta Amazonica) and nature conservation (Biodiversity and Conservation) (Table 2). Overall, 60 journals (52%) had 2021 JCR impact factors ranging from 0.110 (Genetics and Molecular Research, one article) to 9.231 (Food Chemistry, one article). The other 55 journals did not have a 2021 JCR impact factor, including five of the twenty journals with the highest number of publications.

Of the total number of articles, 212 were cited in other publications, and 106 of them had more than 10 citations. The most cited articles were Grubb et al. (1963)Grubb PJ, Lloyd JR, Pennington TD, Whitmore TC. 1963. A comparison of montane and lowland rain forest in Ecuador I. The forest structure, physiognomy, and floristics. Journal of Ecology 51: 567-601. doi: 10.2307/2257748.
https://doi.org/10.2307/2257748... , Teer Steege and Cornelissen (1989)Teer Steege H, Cornelissen JHC. 1989. Distribution and ecology of vascular epiphytes in lowland rain forest of Guyana. Biotropica 21: 331-339. doi: 10.2307/2388283.
https://doi.org/10.2307/2388283... , Davis and Richards (1933)Davis TAW, Richards PW. 1933. The Vegetation of Moraballi Creek, British Guiana: An Ecological Study of a Limited Area of Tropical Rain Forest. Part I. Journal of Ecology 21: 350-384., and Kreft et al. (2004)Kreft H, Köster N, Küper W, Nieder J. 2004. Diversity and biogeography of vascular epiphytes in western Amazonia, Yasuni, Ecuador. Journal of Biogeography 31: 1463-1476. doi: 10.1111/j.1365-2699.2004.01083.x.
https://doi.org/10.1111/j.1365-2699.2004... , with 463, 393, 261 and 230 citations, respectively. Grubb et al. (1963)Grubb PJ, Lloyd JR, Pennington TD, Whitmore TC. 1963. A comparison of montane and lowland rain forest in Ecuador I. The forest structure, physiognomy, and floristics. Journal of Ecology 51: 567-601. doi: 10.2307/2257748.
https://doi.org/10.2307/2257748... and Teer Steege and Cornelissen (1989)Teer Steege H, Cornelissen JHC. 1989. Distribution and ecology of vascular epiphytes in lowland rain forest of Guyana. Biotropica 21: 331-339. doi: 10.2307/2388283.
https://doi.org/10.2307/2388283... consist of floristic surveys carried out, respectively, in Ecuador and Guyana. The other two most cited studies were also carried out in these countries, but were more focused on the diversity and distribution of vascular epiphytes. Pinheiro et al. (2011Pinheiro BG, Silva ASB, Souza GEP et al. 2011. Chemical composition, antinociceptive and anti-inflammatory effects in rodents of the essential oil of Peperomia serpens (Sw.) Loud. Journal of Ethnopharmacology 138: 479-486. doi: 10.1016/j.jep.2011.09.037.
https://doi.org/10.1016/j.jep.2011.09.03... ) was the most cited article (78 citations) among the ones carried out in the Brazilian Amazon and the 15^th among all analyzed in this review. In this study, the authors portray the medicinal potential of Peperomia serpens (Sw.) Loudon (Piperaceae), proving its anti-inflammatory efficacy for widespread use in folk medicine.

Authors’ affiliations and country of origin

Edlley Max Pessoa da Silva and Adriano Costa Quaresma stood out among the authors who studied vascular epyphytes in the Amazon, with 15 and 14 articles published in the period 2011-2022 (Fig. 6A), respectively. They are currently affiliated with the Federal University Mato Grosso and the National Institute for Research in the Amazon, respectively. E. Pessoa’s publications are primarily related to taxonomic studies of species of Orchidaceae in Central Amazonia, Brazil, and A. Quaresma has mainly studied the floristic composition, richness, diversity and distribution of vascular epiphytes in general or specifically of Bromeliaceae, with most of the studies conducted in the state of Pará, Brazil. Mário Augusto Gonçalves Jardim and Maria Teresa Fernandez Piedade stand out among A. Quaresma’s collaborators, and are among the 13 researchers with the highest number of publications (Fig. 6A).

The authors are affiliated with institutions in 20 countries (Fig. 6B). Researchers associated with Brazilian institutions were those who published the majority of the articles (171), followed by researchers from institutions based in Germany (37), United States (32), Colombia (27), Peru (15), Mexico (13), and Venezuela (9), in individual publications or parternships. Of the total of 171 articles, 137 were exclusively authored by researchers from Brazilian institutions and 34 articles involved cooperation with researchers from other countries (Germany, United States, France, Colombia, Mexico, United Kingdom, and Holland). The Emílio Goeldi Museum of Pará, the National Institute for Research in the Amazon, and the Federal University of Mato Grosso stand out among the Brazilian institutions with the greatest production of articles. The University of Goettingen in Germany and the Missouri Botanical Garden the United States were also instituitions with significant production.

Discussion

Advances in studies on vascular epiphytes in the Amazon in recent decades

Of the 3,980 publications retrieved from the three databases, most were found in Google Scholar. After application of the exclusion criteria, the final number of articles was reduced to 291, or approximately 7.3% of the total number. This was mainly the result of the exclusion of documents such as books, theses, dissertations, abstracts, and technical reports that appeared in searches made in Google Scholar. The large body of literature, also observed by Jover et al. (2020Jover A, Ramos A, Cabrera A, Suárez AM, Machell J, Pérez-Lloréns JL. 2020. Epiphytic macroalgae and hosts of the marine shelf of Cuba: Current status, composition and diversity. Regional Studies in Marine Science 34: 101108. doi: 10.1016/j.rsma.2020.101108.
https://doi.org/10.1016/j.rsma.2020.1011... ), requires a process of manual cleaning and organization of information and this is considered a disadvantage of using this platform (Orduna-Malea et al. 2015Orduna-Malea E, Ayllón JM, Martín-Martín A, López-Cózar ED. 2015. Methods for estimating the size of Google Scholar. Scientometrics 104: 931-949. doi: 10.1007/s11192-015-1614-6.
https://doi.org/10.1007/s11192-015-1614-... ). However, Google Scholar was responsible for 53% of the results obtained in this research and was, thus, essential to learn the current state of the art of research on epiphytes in the Amazon. Our review used a larger sample size than that used by the systematic study by Mengist et al. (2020b)Mengist W, Soromessa T, Legese G. 2020b. Ecosystem services research in mountainous regions: A systematic literature review on current knowledge and research gaps. Science of The Total Environment 702: 134581. doi: 10.1016/j.scitotenv.2019.134581.
https://doi.org/10.1016/j.scitotenv.2019... , who kept 5.9% (74 articles) of the total number of articles initially found (1,252) when conducting a survey of studies on ecosystem services of mountains in the northern hemisphere. In turn, our final sample was lower than that of Spicer & Woods (2022Spicer ME, Woods CL. 2022. A case for studying biotic interactions in epiphyte ecology and evolution. Perspectives in Plant Ecology, Evolution and Systematics 54: 125658. doi: 10.1016/j.ppees.2021.125658.
https://doi.org/10.1016/j.ppees.2021.125... ), who used 17% (233 articles) of the total number initially found (1,764) during a review of biotic interactions involving epiphytes.

Regarding the number of publications per year, the knowledge about vascular epiphytes in the Amazon, systematized in the form of scientific articles, has been built for almost 90 years, although there is a clear gap in the decades of 1940-1970. Only 24 articles were published in the period 1933-2000 and 267 articles were published in the following 22 years, indicating that the vascular epiphytes of the Amazon began to be more studied in the 21st century, which may actually be related to few investigations in the last century or late start of processing of databases consulted (Khapugin 2020Khapugin AA. 2020. A global systematic review on orchid data in protected areas. Nature Conservation Research 5:19-33. doi: 10.24189/ncr.2020.019.
https://doi.org/10.24189/ncr.2020.019... ). However, research gaps until the 20th century, are not exclusive to the Amazon phytogeographic domain. Gaps in the study of vascular epiphytes in the Brazilian Atlantic Forest were also identified (Kersten 2010Kersten RA. 2010. Epífitas vasculares - Histórico, participação taxonômica e aspectos relevantes, com ênfase na Mata Atlântica. Hoehnea 37: 9-38.). In turn, the decrease in the number of publications in 2021, the is possibly associated with the COVID-19 pandemic, which affected the development of researches (access to institutions or study areas) and, consequently, the scientific production worldwide (Chang et al. 2022Chang K, Tao J, Fang C et al. 2022. Evolution of research topics on the Tibetan Plateau environment and ecology from 2000 to 2020: A paper mining. Environmental Science and Pollution Research 29: 12933-12947. doi:10.1007/s11356-021-17149-3.
https://doi.org/10.1007/s11356-021-17149... ). Yet, we can state that further investigations about vascular epiphytes in the Amazon are necessary and have been increasing in the last decades.

Brazil was the country where the greatest number of studies on vascular epiphytes was carried out. This can be associated to the fact that most of the Amazon (58%) is located within the Brazilian territory (Aragón 2018Aragón LE. 2018. A dimensão internacional da Amazônia: Um aporte para sua interpretação. Revista NERA 42: 15-33.). However, we identified that these studies are more concentrated in the vicinity of the main research institutions (e.g. Instituto Nacional de Pesquisas da Amazônia, Museu Paraense Emílio Goeldi and Universidade Federal do Mato Grosso), and there is also a lack of inventories in Brazilian regions that coincide with the deforestation arc (Gomes et al. 2019Gomes VHF, Vieira ICG, Salomão RP, Teer Steege H. 2019. Amazonian tree species threatened by deforestation and climate change. Nature Climate Change 9: 547-553. doi: 10.1038/s41558-019-0500-2.
https://doi.org/10.1038/s41558-019-0500-... ; Quaresma et al. 2022Quaresma A, Zartman CE, Piedade MTF et al. 2022. The Amazon epiphyte network: a first glimpse into Continental-Scale patterns of Amazonian vascular epiphyte assemblages. Frontiers in Forests and Global Change 5: 828759. doi: 10.3389/ffgc.2022.828759.
https://doi.org/10.3389/ffgc.2022.828759... ). Furthermore, although the Amazon occupies a large territorial proportion (>50%) of Guyana, French Guiana, Suriname, Bolivia and Peru (Aragón 2018Aragón LE. 2018. A dimensão internacional da Amazônia: Um aporte para sua interpretação. Revista NERA 42: 15-33.), a smaller number of publications come from these countries (Fig. 3), what highlights the need for studies in these areas. We also highlight the studies carried out in protected areas. The analysis of biodiversity in protected areas is essential to identify trends in species richness or abundance and assess the efficiency of conservation measures (Barnes et al. 2016Barnes MD, Craigie ID, Harrison LB et al. 2016. Wildlife population trends in protected areas predicted by national socio-economic metrics and body size. Nature Communications 7: 12747. doi: 10.1038/ncomms12747.
https://doi.org/10.1038/ncomms12747... ). These assessments are especially important for epiphytes because the presence of this group indicates an increase in the structural complexity of forests (Richards 2020Richards JH. 2020. Assessing the strength of climate and land-use influences on montane epiphyte communities. Conservation Biology 35: 1496-1506. doi: 10.1111/cobi.13679.
https://doi.org/10.1111/cobi.13679... ).

Main approaches, gaps and perspectives of studies on vascular epiphytes in the Amazon

We found that floristic surveys of spermatophytes and ferns prevailed over the other approaches. Floristic surveys were also predominant in the study by Bargali et al. (2022Bargali H, Kumar A, Singh P. 2022. Plant studies in Uttarakhand, Western Himalaya-A comprehensive review. Trees, Forests and People 8: 100203. doi: 10.1016/j.tfp.2022.100203.
https://doi.org/10.1016/j.tfp.2022.10020... ). This approach is common because of the need to know the flora and identify centers of biodiversity and priority areas for conservation and they help to find biological, biogeographical and ecological patterns and carry out quantitative comparisons of local diversity (Khapugin 2020Khapugin AA. 2020. A global systematic review on orchid data in protected areas. Nature Conservation Research 5:19-33. doi: 10.24189/ncr.2020.019.
https://doi.org/10.24189/ncr.2020.019... ; Zotz et al. 2021Zotz G, Weigelt P, Kessler M, Kreft H, Taylor A. 2021. EpiList 1.0: a global checklist of vascular epiphytes. Ecology 102: e03326. doi: 10.1002/ecy.3326.
https://doi.org/10.1002/ecy.3326... ). Floristic information has confirmed the notorious diversity of plants associated with the canopy in several natural ecosystems of the Amazon (Taylor et al. 2021Taylor A, Zotz G, Weigelt P, Cai L, Karger DK, König C, Kreft H. 2021. Vascular epiphytes contribute disproportionately to global centres of plant diversity. Global Ecology and Biogeography 31: 62-74. doi: 10.1111/geb.13411.
https://doi.org/10.1111/geb.13411... ; Quaresma et al. 2022Quaresma A, Zartman CE, Piedade MTF et al. 2022. The Amazon epiphyte network: a first glimpse into Continental-Scale patterns of Amazonian vascular epiphyte assemblages. Frontiers in Forests and Global Change 5: 828759. doi: 10.3389/ffgc.2022.828759.
https://doi.org/10.3389/ffgc.2022.828759... ). However, we also noticed that few studies carried out a more comprehensive approach, considering frequency, dominance, abundance, population dynamics (growth and reproduction), information from support trees and factors that influence the occurrence of epiphytes (Kersten 2010Kersten RA. 2010. Epífitas vasculares - Histórico, participação taxonômica e aspectos relevantes, com ênfase na Mata Atlântica. Hoehnea 37: 9-38., Mendieta-Leiva & Zotz 2015Mendieta-Leiva G, Zotz G. 2015. A conceptual framework for the analysis of vascular epiphyte assemblages. Perspectives in Plant Ecology, Evolution and Systematics 17: 510-521. doi: 10.1016/j.ppees.2015.09.003.
https://doi.org/10.1016/j.ppees.2015.09.... ). This gap may be related to the difficulty of evaluating plants, for example, biomass studies require great field efforts, mainly in accessing the forest canopy and removing specimens for evaluation, with mostly destructive methods. In addition, there is still no clear understanding of the factors that contribute to the occurrence of epiphytes in anthropized areas, such as pastures with invasive trees and monocultures, which occupy large areas in the Amazon landscape (Projeto BioMaps Amazônia 2022 MapBiomas Amazônia. 2022. Mapeamento anual de cobertura e uso da terra na Amazônia. Mapbiomas 7. https://mapbiomas-br-site.s3.amazonaws.com/MapBiomas_AMAZ%C3%94NIA_Setembro_2022_03092022.pdf. 03 May 2023.
https://mapbiomas-br-site.s3.amazonaws.c... ).

As for the taxonomic studies, we noticed that the identification of new species and expansion of the distribution were frequent approaches throughout the period studied. However, the systematization of this information is important for the recognition of the real diversity of species that occur in the Amazon and their distribution in the Amazon Countries. In addition, the lack of comprehensive and reliable data on the richness and distribution of vascular epiphytes in the Amazon are research gaps that hinder assessments biogeographical, of niche modeling and extinction risk (Marcusso et al. 2022Marcusso GM, Kamimura V, Borgiani R, Menini Neto L, Lombardi JA. 2022. Phytogeographic meta-analysis of the vascular epiphytes in the Neotropical region. The Botanical Review 88: 388-412. doi: 10.1007/s12229-021-09270-2.
https://doi.org/10.1007/s12229-021-09270... ; Quaresma et al. 2022Quaresma A, Zartman CE, Piedade MTF et al. 2022. The Amazon epiphyte network: a first glimpse into Continental-Scale patterns of Amazonian vascular epiphyte assemblages. Frontiers in Forests and Global Change 5: 828759. doi: 10.3389/ffgc.2022.828759.
https://doi.org/10.3389/ffgc.2022.828759... ).

We also identified that the sampling of floristic surveys is carried out using plots which are heterogeneous in number, shape and size, while the evaluation of the support tree (phorophytes) as a plot is still little used, although it is recommended by Wolf et al. (2009Wolf J, Gradstein S, Nadkarni N. 2009. A protocol for sampling vascular epiphyte richness and abundance. Journal of Tropical Ecology 25: 107-121. doi: 10.1017/S0266467408005786.
https://doi.org/10.1017/S026646740800578... ) and Mendieta-Leiva et al. (2020a Mendieta-Leiva G, Ramos FN, Elias JPC et al. 2020a. EpIG-DB: A database of vascular epiphyte assemblages in the Neotropics. Journal of Vegetation Science 31: 518-528. doi: 10.1111/jvs.12867.
https://doi.org/10.1111/jvs.12867... ). The most plausible justification for the use of plots in the evaluation of epiphytes is the possibility of comparison between sample units and the statistical methods are more applicable, although this evaluation consists of a more extensive field work. Methodologies that consider the support tree as a plot are subject to the researcher's subjectivity in choosing phorophytes with greater epiphyte richness. Therefore, discussions on methodology and guidelines for surveys still need to be debated to resolve issues related to surveying epiphytes.

In the ecological context, we did not find studies that evaluated the effects of interception of precipitation by epiphytes in the forests of Amazon, considering the high rainfall in the region and this being a subject that has been studied in other regions (Van Stan II & Pypker 2015Van Stan II T, Pypker TG. 2015. A review and evaluation of forest canopy epiphyte roles in the partitioning and chemical alteration of precipitation. Science of The Total Environment 536: 813-824. doi: 10.1016/j.scitotenv.2015.07.134.
https://doi.org/10.1016/j.scitotenv.2015... ; Mendieta-Leiva et al. 2020bMendieta-Leiva G, Porada P, Bader MY. 2020b. Interactions of epiphytes with precipitation partitioning. In: Van Stan II J, Gutmann E, Friesen J (eds.). Precipitation partitioning by vegetation. Springer, Cham. p. 133-146. doi: 10.1007/978-3-030-29702-2_9.
https://doi.org/10.1007/978-3-030-29702-... ). Plant-animal interaction studies are more related to myrmecory, making it necessary to investigate possible associations with other organisms, such as bacterias and endemic Amazonian animals (Spicer & Woods 2022Spicer ME, Woods CL. 2022. A case for studying biotic interactions in epiphyte ecology and evolution. Perspectives in Plant Ecology, Evolution and Systematics 54: 125658. doi: 10.1016/j.ppees.2021.125658.
https://doi.org/10.1016/j.ppees.2021.125... ). We can also highlight the need to establish protocols and the need to assess the translocation of epiphytes in pre-exploitation forest concession activities or reduced impact management in Amazonian areas (see Benavides et al. 2023Benavides AM, 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: 834669. doi: 10.3389/ffgc.2023.834669.
https://doi.org/10.3389/ffgc.2023.834669... ).

Some angiosperm families, notably Araceae, Bromeliaceae and Orchidaceae, have received much attention, while studies focusing on other botanical families (e.g. Piperaceae and Clusiaceae) have been less studied. The focus on these families can be explained by their high representativeness in number of species in the Amazon (769 species of Orchidaceae, 456 species of Araceae, and 105 species of Bromeliaceae, according to Cardoso et al. 2017Cardoso AD, Särkinen T, Alexander S et al. 2017. Amazon plant diversity revealed by a taxonomically verified species list. Proceedings of the National Academy of Sciences 114: 10695-10700. doi: 10.1073/pnas.1706756114.
https://doi.org/10.1073/pnas.1706756114... ) and economic importance for ornamental use, with emphasis on the commercialization of flowers (Anacleto et al. 2017Anacleto A, Ramos RAS, Jesus PNF. 2017. Profile and behaviour of orchids consumer in Paraná coast - Brazil. Australian Journal of Basic and Applied Sciences 11: 32-40.; Anacleto & Negrelle 2019Anacleto A, Negrelle RRB. 2019. Bromeliads supply chain of Paraná state - Brazil. International Journal of Advanced Engineering Research and Science 6: 1-12.).

Most studies were published in taxonomic and floristic journals. The approach of most of the studies was within the scope of these journals, confirming that research in these lines has attracted more attention of researchers. Even the anatomical studies were carried out with the objective of contributing to the taxonomic differentiation of species and clarification of the dynamics of geographic distribution of the taxa. More recently, taxonomic and phylogenetic studies began to include more robust analyses to confirm the expansion of the geographic distribution of taxa and evolution of adaptive strategies (Martins et al. 2018Martins AC, Bochorny T, Pérez-Escobar O, Chomicki G, Monteiro SHN, Smidt EC. 2018. From tree tops to the ground: Reversals to terrestrial habit in Galeandra orchids (Epidendroideae: Catasetinae). Molecular Phylogenetics and Evolution 127: 952-960. doi: 10.1016/j.ympev.2018.06.041.
https://doi.org/10.1016/j.ympev.2018.06.... ; Smidt et al. 2021Smidt EC, Brito ALVT, Mauad AVS, Morales NG. 2021. An expanded concept ofMadisoniaincluding miscellaneous species of Pleurothallidinae (Orchidaceae): Evidence from molecular analysis. Phytotaxa 505: 1-28. doi: 10.11646/phytotaxa.505.1.5.
https://doi.org/10.11646/phytotaxa.505.1... ).

As stressed by the researchers cited below, the main limitations recognized in the investigations of epiphytes are: (1) the lack of studies on certain families, preventing the comparison of results obtained in floristic surveys in the Amazon (Quaresma and Jardim 2012Quaresma AC, Jardim MAG. 2012. Diversidade de bromeliáceas epífitas na Área de Proteção Ambiental Ilha do Combu, Belém, Pará, Brasil. Acta Botanica Brasilica 16: 290-294. doi: 10.1590/S0102-33062012000200006.
https://doi.org/10.1590/S0102-3306201200... ); (2) difficulties to visually locate and collect epiphytes in areas with high (≥20 m) and closed forest canopy (Ivanauskas et al. 2004Ivanauskas NM, Monteiro R, Rodrigues RR. 2004. Composição florística de trechos florestais na borda sul-amazônica. Acta Amazonica 34: 339-413. doi: 10.1590/S0044-59672004000300006.
https://doi.org/10.1590/S0044-5967200400... ); and (3) lack of determination of the threat level of species due to the lack of categorization by national and international agencies (Rodrigues et al. 2020Rodrigues PFA, Facundes AS, Pereira LA. 2020. Philodendron Schott (Araceae Juss.) no distrito do Carvão, Mazagão, Amapá, Brasil. Boletim do Museu Paraense Emílio Goeldi 15: 421-431. doi: 10.46357/bcnaturais.v15i2.125.
https://doi.org/10.46357/bcnaturais.v15i... ). In our diagnosis, we also showed that the most productive researchers - precisely 13 researchers who are authors of seven or more articles each - are in Brazil and non-Amazonian countries. This low number authors who continuously publish on the subject suggests that they have unified work teams and access to research funding, especially thos with international collaborations in more developed countries, such as the United States and Germany. In this sense, the need for inclusion and improvement of access is evident, with incentives for grants and financing of research projects with vascular epiphytes aimed at researchers in the Amazonian region, aiming at expanding interdisciplinary and international networks.

We recommend that future studies on the epiphytic synusia include topics neglected in recent years, such as ecological studies (e.g. interactions with animals and mycorrhizal fungi), floral and reproductive biology, biochemistry, phytochemistry, anatomy, and physiology. The importance of biotic interactions and the medicinal use of vascular epiphytes have already been well documented in other continental-scale reviews (Nugraha et al. 2020Nugraha AS, Triatmoko B, Wangchuk P, Keller PA. 2020. Vascular epiphytic medicinal plants as sources of therapeutic agents: Their ethnopharmacological uses, chemical composition, and biological activities. Biomolecules 10: 181. doi: 10.3390/biom10020181.
https://doi.org/10.3390/biom10020181... ; Spicer & Woods 2022Spicer ME, Woods CL. 2022. A case for studying biotic interactions in epiphyte ecology and evolution. Perspectives in Plant Ecology, Evolution and Systematics 54: 125658. doi: 10.1016/j.ppees.2021.125658.
https://doi.org/10.1016/j.ppees.2021.125... ), demonstrating the need for these assessments in the Amazon. We also reinforce that future research should consider the impacts of climate change on the diversity of vascular epiphytes (Gomes et al. 2019Gomes VHF, Vieira ICG, Salomão RP, Teer Steege H. 2019. Amazonian tree species threatened by deforestation and climate change. Nature Climate Change 9: 547-553. doi: 10.1038/s41558-019-0500-2.
https://doi.org/10.1038/s41558-019-0500-... ; Chang et al. 2022Chang K, Tao J, Fang C et al. 2022. Evolution of research topics on the Tibetan Plateau environment and ecology from 2000 to 2020: A paper mining. Environmental Science and Pollution Research 29: 12933-12947. doi:10.1007/s11356-021-17149-3.
https://doi.org/10.1007/s11356-021-17149... ), mainly in the Amazon, taking into account current trends in deforestation, environmental changes, and expansion of the deforestation arc (Gomes et al. 2019Gomes VHF, Vieira ICG, Salomão RP, Teer Steege H. 2019. Amazonian tree species threatened by deforestation and climate change. Nature Climate Change 9: 547-553. doi: 10.1038/s41558-019-0500-2.
https://doi.org/10.1038/s41558-019-0500-... ). Long-term studies and studies of the population dynamics of epiphytes in the face of climate and land use changes are also essential for understanding the interactions and potential vulnerability of these plants (Richards 2020Richards JH. 2020. Assessing the strength of climate and land-use influences on montane epiphyte communities. Conservation Biology 35: 1496-1506. doi: 10.1111/cobi.13679.
https://doi.org/10.1111/cobi.13679... ).

Conclusion

We found that vascular epiphytes in the Amazon have attracted the interest of researchers in the last two decades. In the scientific literature, there is a clear predominance of studies on the richness, spatial, vertical, horizontal and geographic distribution, and taxonomy of vascular epiphytes and researchers associated with Brazilian institutions actively participate in research carried out in the Amazon. However, there are still poorly studied regions and knowledge gaps.

Our study presented a comprehensive and cross-sectional approach on studies of vascular epiphytes carried out in the Amazon. However, we found some limitations. The exhaustive search for articles that characterize the state of the art of research on epiphytes in the Amazon resulted in publications with a low frequency of citations. Still, these studies are important and indicate that research is being conducted. As the main lessons resulting from this systematic review, we can state that there is a need to expand the network of researchers through continuous and long-term studies, strengthening institutional collaborations and interactions in the scientific community to produce knowledge on this theme.

Acknowledgments

We thank the Federal Rural University of the Amazon, the Emílio Goeldi Museum of Pará, the Federal University of Pará, and the Nucleus for Research in Epiphytes (NUPÉFITA) for the infrastructure and facilities provided during the preparation of this study; and Lisi Alvarenga for revising the English. ALSL thanks Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for the support provided through a fellowship grant.

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