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Pteridophytes as ecological indicators: an overview1 1 . Parte do Trabalho de Conclusão de Curso da primeira Autora

Pteridófitas como indicadores ecológicos: uma visão geral

ABSTRACT

The pteridophytes present a great but poorly explored potential as ecological indicators (EIs), shown only in some sparse studies. Therefore, to analyze this potential, we reviewed published articles, websites, or books with pteridophytes as EIs, searching on five scholar databases and also on Google. We selected 134 studies, conducted in all continents (118 in mainland areas and 16 in islands). Brazil is the country with the highest number of studies (N = 33). In general, several species were considered as EIs in a given study, not only a single. The use of Pteridophytes in these works was classified in seven different types: a) classification of vegetation, soils, environments, and ecosystems (N = 65), b) environmental integrity (or quality) (N = 21), c) disturbance (N = 17), d) regeneration/restoration of habitats and/or ecosystems (N = 10), e) climate changes (N = 10), f) contamination of air, soil, or water (N = 14), and g) association with other groups of organisms (N = 12). The vast majority of these studies merely hypothesized the potential use of the Pteridophytes as EIs, with few presenting helpful criteria for the selection of EIs. Although there is an increasing recognition of the potential use of Pteridophytes as EIs, a more in-depth discussion about the criteria for selecting Pteridophytes as indicators and the real uses of such plants is needed.

Keywords:
ferns; lycophytes; types of indication; applied ecology; environmental conservation; plant-environment relationships; bioindicators; plant uses

RESUMO

As pteridófitas apresentam grande potencial como indicadores ecológicos (EIs), mas pouco explorado, mostrado apenas em trabalhos esparsos. Portanto, para analisar esse potencial, revisamos artigos publicados, sites ou livros com pteridófitas como EIs, realizando buscas em cinco bases de dados acadêmicas e no Google. Selecionamos 134 estudos, feitos em todos os continentes (118 em áreas continentais e 16 em ilhas). O Brasil é o país com maior número de estudos (N = 33). Em geral, várias espécies foram consideradas como EIs em cada estudo, não somente uma. O uso das pteridófitas nesses estudos foi classificado em sete tipos de indicação: a) classificação de vegetação, solos, ambientes e ecossistemas (N = 65), b) integridade (ou qualidade) ambiental (N = 21), c) perturbação (N = 17), d) regeneração/restauração de habitats e/ou ecossistemas (N = 10), e) mudanças climáticas (N = 10), f) contaminação de ar, solo ou água (N = 14) e g) associação com outros grupos de organismos (N = 12). A maioria desses estudos apenas hipotetizou o potencial uso das pteridófitas como EIs, com poucos apresentando ou analisando critérios de seleção de EIs. Há crescente reconhecimento do potencial de uso das pteridófitas como EIs, mas faltam discussões sobre a escolha de critérios para selecionar pteridófitas indicadoras e sobre as reais utilizações dessas plantas.

Palavras-chave:
licófitas; samambaias; tipos de indicação; ecologia aplicada; conservação ambiental; relações planta-ambiente; bioindicadores; usos de plantas

Introduction

Ecological indicators (EIs) are useful tools to link empirical results, models, and theories with environmental applications. They are broadly employed in the classification of environments and in the evaluation of natural and/or anthropic disturbance or stress (Niemi & McDonald 2012Niemi, G.J. & McDonald, M.E. 2012. Application of ecological indicators. Annual Review of Ecology, Evolution, and Systematics 35: 89-111., Siddig et al. 2016Siddig, A.A.H., Ellison, A.M., Ochs, A., Villar-Leeman, C. & Lau, M.K. 2016. How do ecologists select and use indicator species to monitor ecological change? Insights from 14 years of publication in Ecological Indicators. Ecological Indicators 60: 223-230.). One definition considers EIs as a species or group of species that readily reflects the abiotic or biotic state of an environment (McGeoch 1998McGeoch, M. 1998. The selection, testing and application of terrestrial insects as bioindicators. Biological Reviews 73: 181-201., Dale & Beyeler 2001Dale, V.H. & Beyeler, S.C. 2001. Challenges in the development and use of ecological indicators. Ecological Indicators 1: 3-10., Heink & Kowarik 2010aHeink, U. & Kowarik, I. 2010a. What are indicators? On the definition of indicators in ecology and environmental planning. Ecological Indicators 10: 584-593.). This definition includes only species and/or group of them, but other taxonomic levels (family, genus) or still ecological attributes (as richness and diversity) could be adopted.

The EIs are often used because they are more easily measurable than other ecological variables of greater interest but difficult measurement (the indicandum, if only one, or the indicanda, if two or more), or when budget and time are restricted (Öster et al. 2008Öster, M., Persson, K. & Eriksson, O. 2008. Validation of plant diversity indicators in semi-natural grasslands. Agriculture, Ecosystems and Environment 125: 65-72.). The use of EIs is multiple as to indicate biotic and abiotic conditions, identify and monitor environmental changes (natural and/or caused by man), identify areas to conserve/restore or more favorable for agriculture, and to predict the distribution of other organisms (Sampson 1939Sampson, A.W. 1939. Plant indicators - concept and status. Botanical Review 5: 155-206., McGeoch 1998McGeoch, M. 1998. The selection, testing and application of terrestrial insects as bioindicators. Biological Reviews 73: 181-201., Niemi & McDonald 2012Niemi, G.J. & McDonald, M.E. 2012. Application of ecological indicators. Annual Review of Ecology, Evolution, and Systematics 35: 89-111.).

The choice of EIs is directly related to the purpose(s) of indication. For the selection of suitable and effective EIs, many criteria were proposed to minimize chances of spending time and resources studying taxa that are unlikely to be good indicators (McGeoch 1998McGeoch, M. 1998. The selection, testing and application of terrestrial insects as bioindicators. Biological Reviews 73: 181-201., Heink & Kowarik 2010bHeink, U. & Kowarik, I. 2010b. What criteria should be used to select biodiversity indicators? Biodiversity and Conservation 19: 3769-3797.). We summarize criteria suggested by different studies in table 1 to check how they are or could be used for pteridophytes.

Table 1
Criteria suggested by different authors for the selection of ecological indicators (EIs).

To select a good EI, four sets of these criteria must be evaluated. First, the economic and logistical suitability (including financial cost, time efficiency, and personnel requirements); followed by the analysis and interpretation efficiency (including the accurate correlation between indicator and indicandum, the capacity of be understandable, self-explanatory, and simplify the information); then the availability of ecological information (including distributional, reliability, representation, physical tolerance, response in function of natural or anthropogenic stress and enemies); and finally, the taxonomic knowledge (including ease of field identification to avoid collecting taxa that do not belong to the indicator group, and that inexperienced or non-experts can be trained quickly to support the studies).

In addition to establishing criteria, some further steps can be followed to select EIs. McGeoch (1998McGeoch, M. 1998. The selection, testing and application of terrestrial insects as bioindicators. Biological Reviews 73: 181-201.) proposes nine of them that, regardless of the objective of the indicator, might be considered (table 2). Throughout the selection process, one must have clarity about the objectives to use the EI, and of its temporal and spatial scales. The scale of indication is essential, since a local and transitory disturbance might not be able to be evaluated using regional or global scales. Thus, the objective of this selection is to identify an organism, or group of organisms, that reflects a particular abiotic or biotic characteristic on the interest scale. The sampling methods should be planned to identify relationships between the EIs and environmental or biotic variables of interest, as strong (significant) relations provide greater predictive values.

Table 2
Steps for establishing an ecological indicator (EI) (adapted from McGeoch 1998McGeoch, M. 1998. The selection, testing and application of terrestrial insects as bioindicators. Biological Reviews 73: 181-201.).

Pteridophytes are vascular plants without seeds currently with about 12,000 known species. They are from two phylogenetically distinct groups: the lycophytes (less than 1500 species) and the ferns (some 10,500 species) (PPG I 2016PPG I. 2016. A community-derived classification for extant lycophytes and ferns. Journal of Systematics and Evolution 54: 563-603.). They are widely distributed, from the tundra to tropical forests, being more diverse in the equatorial region (Tryon 1972Tryon, R.M. 1972. Endemic areas and geographic speciation in tropical American ferns. Biotropica 4: 121-131., Tryon & Tryon 1982, Moran 2008Moran, R.C. 2008. Neotropical genera of ferns and lycophytes: a guide for students. New York Botanical Garden, New York.). Although lycophytes and ferns reach high frequency and abundance in humid forests, they also occur in dry environments, where some genera can be quite species-rich (Moran 2008). Locally pteridophytes are not randomly distributed, as their presence or absence reflects microhabitat characteristics, such as soil texture and fertility, atmospheric temperature and humidity, precipitation, and light intensity (Nóbrega et al. 2011Nóbrega, G.A., Eisenlohr, P. V., Paciencia, M.L.B., Prado, J. & Aidar, M.P.M. 2011. A composição florística e a diversidade de pteridófitas diferem entre a floresta de restinga e a floresta ombrófila densa das terras baixas do Núcleo Picinguaba/PESM, Ubatuba/SP? Biota Neotropica 11: 153-164., Patil et al. 2016Patil, S., Lavate, R., Rawat, V. & Dongare, M. 2016. Diversity and distribution of pteridophytes from Satara District, Maharashtra (India). Plant Science Today 3: 149-156.). Hence the distribution of pteridophytes being strongly related with abiotic variables, this group presents a great potential as EI. In addition, a large number of genera or species are easily recognized in the field (Tuomisto & Ruokolainen 1993Tuomisto, H. & Ruokolainen, K. 1993. Distribution of Pteridophyta and Melastomataceae along an edaphic gradient in an Amazonian rain forest. Journal of Vegetation Science 5: 25-34., Salovaara et al. 2004Salovaara, K.J., Cárdenas, G.G. & Tuomisto, H. 2004. Forest classification in an Amazonian rainforest landscape using pteridophytes as indicator species. Ecography 27: 689-700.).

Considering the great potential of lycophytes and ferns as EIs, the main objectives of this article are: (1) to compile available literature that mentions lycophytes and ferns as EIs, (2) to provide an overview of the current state of research and use of pteridophytes as EIs, (3) to identify the main research areas, criteria, methods, and target groups, and (4) to highlight needful prospects in the study and use of indicator pteridophytes.

Material and Methods

The bibliographic review was mainly concentrated on the search for scientific articles, but also scholar books, thesis, and websites treating the pteridophytes as EIs were included.

Search and selection strategy - The bibliographic research was carried out from October 2015 to July 2017, in five scientific search engines: Scopus, ScienceDirect, PubMed, SciELO, and Google Scholar. The keywords used in the searches were: ferns, pteridophytes, and ecological indicator (in English, Portuguese, and Spanish). The results of these searches were checked for the title, and subsequently for the abstract and keywords. We selected and analyzed the papers that presented the following criteria:

Be published in peer-reviewed scientific journal, book, or thesis.

Be written in English, Portuguese, or Spanish (other languages as Chinese, French, and German were excluded).

Report species or ecological attributes of pteridophytes as EIs.

Be published as from 1980.

In addition, the references of the selected studies were verified, with potentially eligible papers also searched and analyzed, if they had the inclusion criteria and were electronically available for us. Searches were not limited to these databases. Using Google, we also checked websites, books, and monographs available online, using the same keywords. Thus, we selected a total of 122 articles, four websites, four monographs, and four book chapters, totaling 134 studies.

Data extraction and analyses - For each study selected, we extracted the following information: (a) country or countries where the study was carried out, (b) taxa or ecological attributes considered as EIs, (c) methodology and criteria utilized, and (d) results obtained.

As pteridophytes were tested or employed as EIs in a wide variety of objectives, we classified the studies with a similar purpose in different types of indication. The type of indication refers to the indicandum of an indicator, its usefulness, function, purpose of selection, and the possible use of the EI.

We consider the spatial scale of indication, at two levels of amplitude: regional or global. At the regional level, EIs hypothesized or were employed to indicate events (situations) with more restricted geographic distribution (city(ies), state(s), country(ies), and/or group of these). At the global level, they were applied to indicate events (situations) of wider distribution (continents or globe).

We checked if studies included (or not) sampling and data collection in the field. For this, we classify them into two categories: as empirical (with their own data analyses) or as revisive. Empirical studies included data from fieldwork, or collected data from others and discussed the indication potential of the taxa. Revisive studies only cited results/information from previous studies without hypothesizing, arguing, or concluding about the use of certain taxa as EIs.

We examined if each study presented criteria of selection of EIs (such as those in table 1) and if its main objective was to establish/use pteridophytes as EIs. We also checked if there was a relationship between the indicator and the indicandum, and if there was a logical proposition of this relation. Finally, we verified if the studies used statistical tests, separating them into two groups: those that tested statistically the correlation of indicator and indicandum, and those which did not.

Conspectus of the selected studies - A total of 134 studies were published from 1980 to 2018 (table 3). Until the year 2000, an average of one paper with pteridophytes as EIs was published yearly. From then, there was an increase, especially this last decade to reach 16 papers in 2016 (figure 1). These studies were published in a wide variety of journals, but mostly in Ecological Indicators (N = 9), Biodiversity and Conservation (N = 7), and Biological Conservation (N = 6). Articles with pteridophytes as EIs were not found in other important conservation biology journals, such as Conservation Biology or Conservation Letters.

Table 3
Information of the analyzed studies citing pteridophytes as EIs. Types of indication: A. Classification of vegetation, soils, environments, and ecosystems. B. Environmental integrity (or quality). C. Disturbance. D. Regeneration/restoration of habitats and/or ecosystems. E. Climate changes. F. Contamination of air, soil, or water. G. Association with other groups of organisms. The column “Main goal?” answers if the main objective of the study was to establish pteridophytes as EIs. With * the studies that presented the word ‘conservation’ in the title or keywords, or included small citations in the text on the use of EIs for biodiversity conservation.

Figure 1
Temporal variation of the number of studies published with Pteridophytes as EIs from 1981 to 2016.

Studies with pteridophytes as EIs covered all continents but not equally: Africa (N = 9), America (N = 79), Asia (N = 17), Europe (N = 17), Oceania (N = 7), and Antarctica (N = 1); there are four studies without a defined region; 16 studies included islands sampling, and the remainder was carried out exclusively in mainland areas. Within America, North America had less than half of articles (N = 22) compared to South and Central America (N = 57, two of these in Central America), and had fewer studies than the Amazon region (N = 23). Brazil had most of the studies (N = 33), followed by Peru (N = 19), Ecuador (N = 9), the United States of America and Mexico (N = 8), and Colombia and Canada (N = 7). India was the country with most studies outside the Americas (N = 6).

The fact that our review included articles in Portuguese and the largest repository of studies produced in Brazil (SciELO) might have contributed to the number of papers found in this country. On the other hand, the large number of studies in the Amazon can be explained by the existence of a group of researchers studying ferns and Melastomataceae as EIs in this region, with most of the studies in this region being published by its members. Surprisingly, more scientifically developed English-speaking countries had few studies of indicator pteridophytes inside their territories (N = 19).

The majority of the studies (N = 83, or 62% of them) aimed to establish pteridophytes as EIs. Selection of EIs was secondary for the others, where the main goal was, for example, to analyze species distribution along an elevation gradient, to compare species distribution between two areas, or to determine the influence of abiotic variables in the distribution of species (see table 3).

Several taxonomic levels were used as EIs, with most studies (57%) adopting indicator species. The remainder preferred higher levels (mainly genus or family). EIs at higher taxonomic levels may be advantageous, because they include a broader range of functional relationships, and can be more easily identified than species. Nevertheless, we should take into account the objectives and purposes of the study for choosing a species or group of species as EIs.

Within the studies that considered indicator species, 13% presented a single species; the others suggested more species. Use of a large number of indicator species seen here was also highlighted in others reviews about EIs (Jørgensen et al. 2013Jørgensen, S.E., Burkhard, B. & Müller, F. 2013. Twenty volumes of Ecological Indicators - An accounting short review. Ecological Indicators 28: 4-9., Gao et al. 2015Gao, T., Nielsen, A.B. & Hedblom, M. 2015. Reviewing the strength of evidence of biodiversity indicators for forest ecosystems in Europe. Ecological Indicators 57: 420-434.). Some studies considered an individual (the plant as a whole) as an indicator; and in 12 studies only part of a plant (such as spores, fossil or not) was considered.

Most studies (51%) evaluated not only the indication potential of pteridophytes but also included taxa from other groups, as angiosperms (mainly monocotyledons and Melastomataceae), while five (4%) also included animals, such as birds and insects. In all these articles, pteridophytes were studied simultaneously with other groups but without the objective of representing them, different from the seventh type of indication (next section and table 4) in which the pteridophytes reflect the richness, frequency, or abundance of other groups.

Table 4
Studies included in each type of indication.

The methodologies in the studies were similar; the majority (N = 92) used standardized sampling, although sample size varied, with presence or absence of a particular species, its abundance and/or frequency of individuals, or richness and/or diversity in the studied areas as the most important aims.

As expected, proposed EIs were of regional or local spatial scale. Few studies established indicators with a wider scale (global), with ten studies proposing indicators for climate changes.

About 90% of the studies were classified as empirical, and few were reviews of previous works, or in some cases presented only a logical inference without field data to support the hypothesis of the type of relationship between the indicator and indicandum. Most of the studies (78%) presented statistical analyses using indexes (or values) of indication, richness, diversity, and/or correlation between species and abiotic variables. Those which did not present a correlation of indicandum and indicator were based only in the logic. Finally, some articles (Snyder 2009Snyder, M. 2009. What are Indicator Plants? Available at http://northernwoodlands.org/articles/article/what_are_indicator_plants (access in 23-V-2017).
http://northernwoodlands.org/articles/ar...
, Gassner et al. 2012Gassner, P., Mostacero, J. & Weiss, M. 2012. Establishing suitable bio-indicators for cloud forest management. Available at http://www.biodiversityscience.com/2012/09/26/bioindicators-cloud-forest-management/ (access in 23-V-2017).
http://www.biodiversityscience.com/2012/...
) aimed at scientific dissemination only.

Surprisingly, only a few studies (as Tuomisto & Ruokolainen 1998Tuomisto, H. & Ruokolainen, K. 1998. Uso de especies indicadoras para determinar características del bosque y de la tierra. In: R. Kalliola & S.F. Paitán (eds.). Geoecología y desarrollo amazónico. Estudio integrado en la zona de Iquitos, Perú. Turun Yliopisto, Turku. pp. 81-491., Kessler & Bach 1999Kessler, M. & Bach, K. 1999. Using indicator families for vegetation classification in species-rich Neotropical forests. Phytocoenologia 29: 485-502.) presented criteria for the selection of EIs, such as those listed in table 1. Not taking into account these criteria, time and resources might be spent studying species that will not be good EIs. Taxa that in a study are highly correlated with abiotic (or even biotic) variables, but which are hardly identified by people with low taxonomic and ecological knowledge, would have a low potential for indication. This shows the importance of using selection criteria of EIs, and we emphasize this aspect as one of the main contributions of this review.

As for the existence of an association between indicator and indicandum, we can conclude that all studies presented a logical association. For all types of objectives that the pteridophytes were studied as EIs, their relationship with the indicandum made sense. The majority of the studies (N = 121) only hypothesized that pteridophytes would be good EIs, while only two (Goforth 2006Goforth, T. 2006. Crow dog native ferns and gardens. Available at http://www.crowdognativeferns.com/ (access in 23-V-2017).
http://www.crowdognativeferns.com...
, Halme & Bodmer 2007Halme, K.J. & Bodmer, R.E. 2007. Correspondence between scientific and traditional ecological knowledge: Rain forest classification by the non-indigenous riberenos in Peruvian Amazonia. Biodiversity and Conservation 16: 1785-1801.) used them as EIs. Moreover, 11 studies only cited the indication potential of pteridophytes, not falling under the previous alternatives.

Types of indication - The selected studies tested the pteridophytes as EIs with different purposes (indicanda), which here we grouped into seven types (see table 4 for the references, and figure 2 for their proportions). Taking into consideration that some studies suggested more than one type of indication, the number of indications exceeds 134 (and the percentages also exceed 100%).

Figure 2
Proportion of each type of indication (N = 149).

  • a) Classification of vegetation, soils, environments, and ecosystems (N = 65 studies, 48% of them): the presence, abundance, frequency, and diversity of pteridophytes are directly correlated with abiotic conditions, such as humidity, texture, pH and soil nutrients, air humidity, luminosity, precipitation, altitude, topography, and atmospheric temperature. Pteridophytes are well known to have soil preferences and adaptations that allow them to survive on different types of soils (Young & León 1989Young, K.R. & Léon, B. 1989. Pteridophytes species in the central Peruvian Amazon: Importance of edaphic specialization. Brittonia 41: 388-395., Tuomisto & Ruokolainen 1993Tuomisto, H. & Ruokolainen, K. 1993. Distribution of Pteridophyta and Melastomataceae along an edaphic gradient in an Amazonian rain forest. Journal of Vegetation Science 5: 25-34., Tuomisto & Poulsen 2000). Different soils usually harbor different vegetation types. Thus, besides EIs be used to support the classification of soil types, they can be employed for vegetation too (when clearly defined by soil type).

  • b) Environmental integrity (or quality) (N = 21 studies, 16%): evergreen forests with good canopy cover have reduced solar radiation in the understory, and tropical ones also have usually high humidity. Species adapted to the understory are, most of the time, sensitive to changes in these two conditions (Padmawathe et al. 2004Padmawathe, R., Qureshi, Q. & Rawat, G.S. 2004. Effects of selective logging on vascular epiphyte diversity in a moist lowland forest of Eastern Himalaya, India. Biological Conservation 119: 81-92., Silva et al. 2018Silva, V.L., Mehltreter, K. & Schmitt, J.L. 2018. Ferns as potential ecological indicators of edge in two types of Mexican forests. Ecological Indicators 93: 669-676.). Therefore, such species could be considered as good initial candidates for EIs (but other criteria must also be checked at table 1). Most pteridophytes respond quickly to changes in these conditions, being much affected by canopy opening and linked alterations in environmental variables and vegetation composition (Romero et al. 2008Romero, L.R., Pacheco, L. & Zavala Hurtado, J.A. 2008. Pteridofitas indicadoras de alteración ambiental en el bosque templado de San Jerónimo Amanalco, Texcoco, México. Revista de Biología Tropical 56: 641-656., Bergeron & Pellerin 2014Bergeron, A. & Pellerin, S. 2014. Pteridophytes as indicators of urban forest integrity. Ecological Indicators 38: 40-49.). Usually, species richness and abundance of pteridophytes are greater in intact or well-preserved habitats. Also, species richness and abundance of pteridophytes are greater in shady forests than in more open ones or in open vegetation types because there are more shade tolerant species (umbrophiles) of pteridophytes than pioneers/heliophiles (Tryon & Tryon 1982Tryon, R.M. & Tryon, A.F. 1982. Ferns and allied plants, with special reference to tropical America. Springer, New York., Della 2016Della, A.P. 2016. Pteridófitas como indicadores ecológicos: revisão geral e aplicações em Santa Catarina. Trabalho de Conclusão de Curso, Universidade Federal de Santa Catarina, Florianópolis.).

  • c) Disturbance (N = 17 studies, 13%): disturbance of a given natural area generally promotes a simplification of its community structure at first; this is usually reflected by reduction of species richness and diversity of pteridophytes and other groups (Watson & Cameron 2002Watson, L.H. & Cameron, M.J. 2002. Forest tree and fern species as indicators of an unnatural fire event in a southern Cape mountain forest. South African Journal of Botany 68: 357-361., Tejeda-Cruz et al. 2008Tejeda-Cruz, C., Mehltreter, K. & Sosa, V.J. 2008. Indicadores ecológicos multi-taxonómicos. In: R.H. Manson, V. Hernández-Ortiz, S. Gallina & K. Mehltreter (eds.). Agroecosistemas cafetaleros de Veracruz. Biodiversidad, manejo y conservación. Instituto de Ecología A.C., Xalapa, & Instituto Nacional de Ecología, México, pp. 271-278., Reeb et al. 2012Reeb, C., Ranarijaona, H.L. & Dubuisson, J.Y. 2012. Ecological survey of the lycophytes and ferns of the Vohimana Reserve, Madagascar. Scripta Botanica Belgica 50: 73-81.). Species that are more sensitive to changes in soil moisture and luminosity are the greatly affected; reduction of their frequency and abundance can lead to local extinction (at least temporarily). On the other hand, species that are more tolerant to sunny and dry environments might be favored in these disturbed areas, sometimes becoming dominant. Thus, disturbance can lead to many and quick changes in this group that can be easily measured and monitored.

  • d) Regeneration/restoration of habitats and/or ecosystems (N = 10 studies, 7%): as seen above, species composition and density of pteridophytes are different in disturbed areas and pristine natural environments, with primary and late secondary forests among the most important communities for these plants. Therefore, changes in the composition (or substitution) of ecological groups of pteridophytes might be used as an ecological indication.

  • e) Climate changes (N = 10 studies, 7%): observed and predicted changes in climate due to anthropogenic activities are a growing research field. It is expected that, in some regions, changes in existing climatic conditions might lead to dramatic changes in the ecosystems, including expansion or retraction of climate-sensitive pteridophytes, but also species extinction (Bässler et al. 2010Bässler, C., Müller, J., Hothorn, T., Kneib, T., Badeck, F. & Dziock, F. 2010. Estimation of the extinction risk for high-montane species as a consequence of global warming and assessment of their suitability as cross-taxon indicators. Ecological Indicators 10: 341-352., Higa et al. 2013Higa, M., Nakao, K., Tsuyama, I., Nakazono, E., Yasuda, M., Matsui, T. & Tanaka, N. 2013. Indicator plant species selection for monitoring the impact of climate change based on prediction uncertainty. Ecological Indicators 29: 307-315.). Sensitive species can be considered good EIs for monitoring such temporal and spatial changes.

  • f) Contamination of air, soil, or water (N = 14 studies, 10%): pteridophytes are utilized for indicating contamination or pollution caused by heavy metals (antimony, arsenic, lead, chromium, gold, etc.), in aquatic or terrestrial environments. The concentration of heavy metals in plant organs measures the degree of contamination or pollution (Repula et al. 2012Repula, C.M.M., Quináia, S.P., De Campos, B.K., Ganzarolli, E.M. & Lopes, M.C. 2012. Accumulation of chromium and lead in bryophytes and pteridophytes in a stream affected by tannery waste water. Bulletin of Environmental Contamination and Toxicology 88: 84-88., Wolff et al. 2012Wolff, G., Pereira, G.C., Castro, E.M., Louzada, J. & Coelho, F.F. 2012. The use of Salvinia auriculata as a bioindicator in aquatic ecosystems: biomass and structure dependent on the cadmium concentration. Brazilian Journal of Biology 72: 71-77.), and other variables would estimate the species survival capacity or degree of injuries (mainly foliar necrosis), but determine sensitive species that might not survive in these conditions. This type of indication is linked to the ability to absorb and accumulate heavy metals (in rhizomes and/or fronds) that some pteridophytes have.

  • g) Association with other groups of organisms (N = 12 studies, 9%): pteridophytes can be employed to indicate the presence of other species in a given site. It is assumed that there is a “strict relationship” or association between these species, or that some pteridophytes (e.g. tree ferns, litter basket ferns, etc) are keystone species in a certain ecosystem. Thus, a particular taxon can be used as a measure (or estimation) of diversity (such as richness, abundance, and frequency) of other associated taxon or taxa in a habitat or set of habitats.

Some studies presented more than one type of indication. Bergeron & Pellerin (2014Bergeron, A. & Pellerin, S. 2014. Pteridophytes as indicators of urban forest integrity. Ecological Indicators 38: 40-49.), Paciencia & Prado (2005Paciencia, M.L.B. & Prado, J. 2005. Distribuição espacial da assembléia de pteridófitas em uma paisagem fragmentada de Mata Atlântica no sul da Bahia, Brasil. Hoehnea 32: 103-117.), and Romero et al. (2008Romero, L.R., Pacheco, L. & Zavala Hurtado, J.A. 2008. Pteridofitas indicadoras de alteración ambiental en el bosque templado de San Jerónimo Amanalco, Texcoco, México. Revista de Biología Tropical 56: 641-656.) encompassed pteridophytes as EIs of the environmental integrity, as well as of regeneration/restoration of habitats. Gehrig-Downie et al. (2012Gehrig-Downie, C., Marquardt, J., Obregón, A., Bendix, J. & Gradstein, S.R. 2012. Diversity and vertical distribution of filmy ferns as a tool for identifying the novel forest type “tropical lowland cloud forest”. Ecotropica 18: 35-44.) applied pteridophytes to classify vegetation and indicate environmental integrity. Carvajal-Hernández et al. (2017Carvajal-Hernández, C.I., Krömer, T., López-Acosta, J.C., Gómez-Díaz, J.A. & Kessler, M. 2017. Conservation value of disturbed and secondary forests for ferns and lycophytes along an elevational gradient in Mexico. Applied Vegetation Science 20: 662-672.) suggested pteridophytes to classify vegetation, but also to indicate disturbance. Liira et al. (2008Liira, J., Schmidt, T., Aavik, T., Arens, P., Augenstein, I., Bailey, D., Billeter, R., Bukáček, R., Burel, F., De Blust, G., De Cock, R., Dirksen, J., Edwards, P.J., Hamerský, R., Herzog, F., Klotz, S., Kühn, I., Le Coeur, D., Miklová, P., Roubalova, M., Schweiger, O., Smulders, M.J.M., van Wingerden, W.K.R.E., Bugter, R. & Zobel, M. 2008. Plant functional group composition and large-scale species richness in European agricultural landscapes. Journal of Vegetation Science 19: 3-14.), Silva & Schmitt (2015Silva, V.L. & Schmitt, J.L. 2015. The effects of fragmentation on Araucaria forest: analysis of the fern and lycophyte communities at sites subject to different edge conditions. Acta Botanica Brasilica 29: 223-230.), Silva et al. (2017, 2018), and Travassos et al. (2014Travassos, C.C., Jardim, M.A.G. & Maciel, S. 2014. Florística e ecologia de samambaias e licófitas como indicadores de conservação ambiental. Biota Amazônia 4: 40-44.) hypothesized pteridophytes for environmental integrity, as well as for disturbance, and the last study also for regeneration/restoration. Della (2016Della, A.P. 2016. Pteridófitas como indicadores ecológicos: revisão geral e aplicações em Santa Catarina. Trabalho de Conclusão de Curso, Universidade Federal de Santa Catarina, Florianópolis.) discussed pteridophytes to classify vegetation and to evaluate the integrity of environments and regeneration/restoration. Ceschin et al. (2010Ceschin, S., Zuccarello, V. & Caneva, G. 2010. Role of macrophyte communities as bioindicators of water quality: Application on the Tiber river basin (Italy). Plant Biosystems 144: 528-536.) studied pteridophytes to indicate contamination/pollution, but also to associate them with other groups of organisms.

These seven types of indication form two larger groups: one that would indicate biotic or abiotic conditions of communities/habitats (the first six types), and the other that would indicate the presence of other species in a given site (the seventh type). EIs are far more used as a tool for the first group.

Indicator taxa - Most of the taxa cited as EIs are ferns (Polypodiopsida), representatives of all subclasses (Equisetidae, Ophioglossidae, Marattiidae, and especially Polypodiidae). The families of Polypodiopsida most cited were Aspleniaceae (Asplenium), Blechnaceae (Blechnum), Cyatheaceae (Cyathea), Dennstaedtiaceae (Pteridium), Dryopteridaceae (Elaphoglossum), Equisetaceae (Equisetum), Gleicheniaceae (Dicranopteris and Sticherus), Hymenophyllaceae (Hymenophyllum and Trichomanes), Polypodiaceae (Campyloneurum and Polypodium), Pteridaceae (Adiantum and Pteris), and Thelypteridaceae (Thelypteris). Most studies adopted the traditional circumscriptions of families or genera instead of the many recent proposed changes (PPG I 2016PPG I. 2016. A community-derived classification for extant lycophytes and ferns. Journal of Systematics and Evolution 54: 563-603. and references therein).

Few lycophytes were considered as EIs, among them species of Huperzia, Isoetes, Lycopodiella, Lycopodium, and Selaginella. This difference of lycophytes and ferns cited as EIs could be due to the smaller number of species in the first group, as well as because the lycophytes are perhaps more taxonomically problematic when compared to the ferns, or even because they are sometimes considered as neglected in some context.

Although hundreds of species were studied or analyzed as EIs, only a few appeared more than once (e.g. Athyrium filix-femina, Azolla filiculoides, Equisetum hyemale, E. sylvaticum, E. telmateia, Lomagramma guianensis, Pteridium aquilinum, etc), but none was used or cited many times.

The scientific interest in developing and applying EIs - has increased substantially in the last 40 years (Niemi & McDonald 2012Niemi, G.J. & McDonald, M.E. 2012. Application of ecological indicators. Annual Review of Ecology, Evolution, and Systematics 35: 89-111. and table 3), as evidenced by the growing number of articles (Jørgensen et al. 2013Jørgensen, S.E., Burkhard, B. & Müller, F. 2013. Twenty volumes of Ecological Indicators - An accounting short review. Ecological Indicators 28: 4-9., Siddig et al. 2016Siddig, A.A.H., Ellison, A.M., Ochs, A., Villar-Leeman, C. & Lau, M.K. 2016. How do ecologists select and use indicator species to monitor ecological change? Insights from 14 years of publication in Ecological Indicators. Ecological Indicators 60: 223-230., and figure 1) and books (Niemi & McDonald 2012). EIs were suggested for different objectives and purposes, as discussed in the previous sections. In spite of this, the use of EIs outside the scientific community seems restricted. The lack of broader application of these EIs may be related to slow or difficult translations of scientific information (concepts, terms, and methodologies) into the practitioners community (Jørgensen et al. 2013), or that latter does not tend to publish in scientific journals. This contributes to a knowledge gap between the public and the academics, making it difficult to measure if EIs are or not more widely utilized. However, in cases where the pteridophytes are employed as EIs by practitioners or by researchers, this use tends to be limited, given the relatively large number of purposes that exist. Thus, in addition to the possible gap between science, politics, and population, although pteridophytes are a group with lower species richness (when compared to angiosperms and insects, which are the groups most commonly employed as EIs), they are not so used as indicators. Another explanation might be their perceived ‘secondary importance’ in ecosystems generally dominated by angiosperms, and their usually low economic value.

The acceleration of the scientific interest in the use of EIs is partly due to the increased need to evaluate biodiversity, ecological and conservation needs in decision-making (Niemi & McDonald 2012Niemi, G.J. & McDonald, M.E. 2012. Application of ecological indicators. Annual Review of Ecology, Evolution, and Systematics 35: 89-111.). Thus, EIs can be considered important tools and standards for connecting, maintaining, and improving environmental quality with policy measures (Turnhout et al. 2007Turnhout, E., Hisschemöller, M. & Eijsackers, H. 2007. Ecological indicators: Between the two fires of science and policy. Ecological Indicators 7: 215-228.).

Indeed, there has been an increase in the number of indicator taxa considered in international agreements. One example is the Montreal Process, an agreement established between 12 countries in 1994 that determines indicator species for the conservation of temperate and boreal forests (Niemi & McDonald 2012Niemi, G.J. & McDonald, M.E. 2012. Application of ecological indicators. Annual Review of Ecology, Evolution, and Systematics 35: 89-111.). Indicators are also being used locally as the case of the Brazilian Environment Ministry (which has the function of conserving and managing plant formations in the country and is also responsible for environmental licensing), which have some resolutions under the Brazilian Council for the Environment (CONAMA - Conselho Nacional do Meio Ambiente), as resolutions 04/1994, 261/1999, and 423/2010, which use indicator species (including pteridophytes) to characterize the successional stages of different vegetation types (see Della 2016Della, A.P. 2016. Pteridófitas como indicadores ecológicos: revisão geral e aplicações em Santa Catarina. Trabalho de Conclusão de Curso, Universidade Federal de Santa Catarina, Florianópolis.).

However, despite the existence of indicators in these agreements and resolutions, their use to implement policies is still incipient, because of two main points. Some believe that this type of instrument oversimplifies the natural environment, leading to much uncertainty in understanding the complexity of ecosystems (although this claim is an inherent difficulty for the use of any indicator). The other is that the application of these instruments for the development of appropriate indicators for the purpose of the study, monitoring, or evaluating at hand, implies a process of selection, interaction, and aggregation of criteria and parameters that are, sometimes, not too easy to establish (Turnhout et al. 2007Turnhout, E., Hisschemöller, M. & Eijsackers, H. 2007. Ecological indicators: Between the two fires of science and policy. Ecological Indicators 7: 215-228.). In addition, transfer and translation of scientific knowledge into policy is often difficult because of common misconceptions of use of EIs, lobby (e.g. denial of anthropogenic climate changes, etc), disconnect between the progress of scientific studies and communication with those responsible for drafting laws, apart from other simpler problems as nomenclature errors or use of synonyms (Della 2016Della, A.P. 2016. Pteridófitas como indicadores ecológicos: revisão geral e aplicações em Santa Catarina. Trabalho de Conclusão de Curso, Universidade Federal de Santa Catarina, Florianópolis.). This is somehow clear in this review that found a large number of species suggested as EIs compared to the few listed in the CONAMA resolutions (Della 2016).

The use of EIs should be made more relevant (Jørgensen et al. 2013Jørgensen, S.E., Burkhard, B. & Müller, F. 2013. Twenty volumes of Ecological Indicators - An accounting short review. Ecological Indicators 28: 4-9., Rapport & Hildén 2013Rapport, D.J. & Hildén, M. 2013. An evolving role for ecological indicators: From documenting ecological conditions to monitoring drivers and policy responses. Ecological Indicators 28: 10-15.) to connect the science-policy interface (Turnhout et al. 2007Turnhout, E., Hisschemöller, M. & Eijsackers, H. 2007. Ecological indicators: Between the two fires of science and policy. Ecological Indicators 7: 215-228.).

EIs are not only having low use to help support policies, but they also have a limited use in some fields of Nature research as conservation biology. For the pteridophytes, all seven types of indication considered here could be directly or indirectly applied in this field, especially those dealing with integrity (or quality) of environments, disturbance, regeneration/restoration of habitats and/or ecosystems, climate changes, and contamination (pollution). Those studies with * in table 3 (N = 38, or 28%) had the word ‘conservation’ in the title or keywords, or included use of EIs for biodiversity conservation. Nevertheless, this aspect tended to be treated somehow superficially and might have been included to try to reach a larger audience, and not because it was part of the main study objectives.

Directions for future research - An important step in the selection of EIs is the establishment of criteria since the application of them minimizes the chance of carrying out studies with species and/or group of species that are not suitable indicators (McGeoch 1998McGeoch, M. 1998. The selection, testing and application of terrestrial insects as bioindicators. Biological Reviews 73: 181-201., Heink & Kowarik 2010bHeink, U. & Kowarik, I. 2010b. What criteria should be used to select biodiversity indicators? Biodiversity and Conservation 19: 3769-3797.), thus saving time and resources. However, as seen here, few studies have established criteria, and most of these studies did not discuss sufficiently such criteria. Therefore, there is a need to research into creation and use of criteria for EIs, as these indicators are becoming important tools in the context of worldwide decreasing resources for scientific research combined with stricter environment resolutions for carrying out development projects.

13% of the studies adopted single species as EI, instead of a group of species or other taxonomic or functional groups. However, use of more than one species with similar traits may provide better resolution of the indicandum and would be more likely to be applicable on a larger scale. Use of groups of a broader range of taxonomic and functional entities would cover a larger habitat diversity, as well as, more types of environmental responses (McGeoch 1998McGeoch, M. 1998. The selection, testing and application of terrestrial insects as bioindicators. Biological Reviews 73: 181-201.). Thus, whenever possible, use of groups of similar species (little adopted in the studies selected here dealing with several or many species) may be a more advisable procedure than an isolated species as EI. However, selection of criteria must also be clearly spelled out in this case.

This overview also shows other priorities for the use of pteridophytes as EIs. There is a need for more studies to check broader deficiencies of some selected EIs, and to verify if the proposed use is the only or if the EI could be applied for another type (s) of indication. Related, it is also important to evaluate the use of these EIs outside research studies (e.g. impact assessment, monitoring, etc), to understand and reduce the difficulties in this use, and how to increase their adoption in technical policy documents.

Conclusions

Use of pteridophytes as EIs is becoming more conventional, but studies are having many different objectives, leading to a wide variety of indication types. In one hand, this shows a great potential of this group as EIs, which is also supported by many studies employing similar methodologies, leading to a large number of species, genera, and families to be suggested as EIs. However, there is a lack of studies demonstrating their practical application and which criteria were adopted to choose the/these EIs.

Acknowledgements

We are grateful to Regina Hirai, Maria Leonor D’El Rei Souza, Tania Tarabini Castellani, and Pedro Fiaschi, for comments on previous versions of the study, and to Associate Editor, Claudia Baider, and the anonymous reviewers, for corrections and suggestions on this article.

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  • 1
    . Parte do Trabalho de Conclusão de Curso da primeira Autora

Publication Dates

  • Publication in this collection
    2019

History

  • Received
    25 May 2018
  • Accepted
    10 Oct 2018
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