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Functional diversity: a review on freshwater fish research

Abstract

Functional diversity is an emergent approach in ecology that has been applied globally to better understand the relationships between organisms and the environment. However, assessing the functional diversity of freshwater fish is a challenge for scientists. Aiming to summarize the evolution of scientific knowledge on fish functional diversity, we performed a systematic review of the literature published from 1945 to 2021 using the Web of Science. Based on the 101 articles reviewed, we found that publications about functional diversity of fishes have increased over time, mainly in Neotropical, Indomalayan and Palearctic regions. Most studies were conducted in lotic ecosystems, especially to assess environmental impacts such as biological invasions and land use. Functional diversity has been assessed mainly by morphological traits that reflect feeding and locomotion dimensions. Functional richness was the most common index used in the studies. Our findings suggest that political neglect and lack of investments may hamper the research development in several places. The missing information about the functional traits of many species may limit the use of the functional approach. We also highlight the need for the incorporation of functional diversity in conservation programs once functional diversity is a key facet of biodiversity to maintain freshwater ecosystem functioning.

Keywords:
Aquatic ecosystems; Biogeographic realms; Functional ecology; Functional traits; Systematic review

Resumo

A diversidade funcional tem sido avaliada principalmente através de traços funcionais morfológicos que refletem as dimensões da alimentação e locomoção. A Riqueza Funcional foi a métrica mais comumente usada nos estudos. Esses resultados sugerem que a negligência política e a falta de investimentos podem dificultar o desenvolvimento de pesquisas em diversas regiões. A falta de informações sobre os traços funcionais de muitas espécies limita o uso da abordagem funcional. Destaca-se também a necessidade de incorporar a diversidade funcional em programas de conservação, uma vez que a diversidade funcional é uma faceta chave da biodiversidade para manter o funcionamento dos ecossistemas de água doce.

Palavras-chave:
Ecossistemas aquáticos; Ecologia funcional; Regiões biogeográficas; Revisão sistemática; Traços funcionais

INTRODUCTION

Functional diversity is a key facet of biodiversity that can be defined as the diversity of functions performed by organisms within ecosystems (Petchey, Gaston, 2006Petchey OL, Gaston KJ. Functional diversity: back to basics and looking forward. Ecol Lett. 2006; 9(3):741–58.https://doi.org/10.1111/j.1461-0248.2006.00924.x
https://doi.org/10.1111/j.1461-0248.2006...
). There is an increasing recognition that functional diversity, rather than species diversity, is a better approach to enhancing our understanding of ecological patterns and processes operating in nature (Gross et al., 2017Gross N, Le Bagousse-Pinguet Y, Liancourt P, Berdugo M, Gotelli NJ, Maestre FT. Functional trait diversity maximizes ecosystem multifunctionality. Nat Ecol Evol. 2017; 132. https://doi.org/10.1038/s41559-017-0132
https://doi.org/10.1038/s41559-017-0132...
). While species diversity studies consider only the taxonomic component (i.e., the number of individuals from different species), functional diversity studies are based on the variability of species’ functional traits (Mason et al., 2005Mason NWH, Mouillot D, Lee WG, Wilson JB. Functional richness, functional evenness and functional divergence: the primary components of functional diversity. Oikos. 2005; 111(1):112–18. https://doi.org/10.1111/j.0030-1299.2005.13886.x
https://doi.org/10.1111/j.0030-1299.2005...
; Cadotte et al., 2011Cadotte MW, Carscadden K, Mirotchnick N. Beyond species: Functional diversity and the maintenance of ecological processes and services. J Appl Ecol. 2011; 48(5):1079–87. https://doi.org/10.1111/j.1365-2664.2011.02048.x
https://doi.org/10.1111/j.1365-2664.2011...
). Functional traits are components of an organism’s phenotype that influence ecosystem-level processes. Traits can be morphological, physiological, reproductive, or behavioral aspects of an organism directly related to an ecological function (Violle et al., 2007Violle C, Navas M-L, Vile D, Kazakou E, Fortunel C, Hummel I et al. Let the concept of trait be functional! Oikos. 2007; 116(5):882–92. https://doi.org/10.1111/j.0030-1299.2007.15559.x
https://doi.org/10.1111/j.0030-1299.2007...
). Thereby, functional traits reveal ecological differentiation between species (i.e., ecological roles of species) instead of their taxonomic identity only. The functional diversity approach helps to explore temporal changes in the functional structure of communities (Cheng et al., 2014Cheng L, Blanchet S, Loot G, Villéger S, Zhang T, Lek S et al. Temporal changes in the taxonomic and functional diversity of fish communities in shallow Chinese lakes: the effects of river–lake connections and aquaculture. Aquat Conserv. 2014; 24(1):23–34. https://doi.org/10.1002/aqc.2418
https://doi.org/10.1002/aqc.2418...
; Fitzgerald et al., 2017Fitzgerald DB, Winemiller KO, Pérez MHS, Sousa LM. Using trophic structure to reveal patterns of trait-based community assembly across niche dimensions. Funct Ecol. 2017; 31(5):1135–44. https://doi.org/10.1111/1365-2435.12838
https://doi.org/10.1111/1365-2435.12838...
; Oliveira et al., 2018Oliveira AG, Baumgartner MT, Gomes LC, Dias RM, Agostinho AA. Long-term effects of flow regulation by dams simplify fish functional diversity. Freshw Biol. 2018; 63(3):293–305. https://doi.org/10.1111/fwb.13064
https://doi.org/10.1111/fwb.13064...
), elucidate responses to environmental impacts (Dala-Corte et al., 2016Dala-Corte RB, Giam X, Olden JD, Becker FG, Guimarães TF, Melo AS. Revealing the pathways by which agricultural land-use affects stream fish communities in South Brazilian grasslands. Freshw Biol. 2016; 61(11):1921–34. https://doi.org/10.1111/fwb.12825
https://doi.org/10.1111/fwb.12825...
; Macnaughton et al., 2016Macnaughton CJ, Senay C, Dolinsek I, Bourque G, Maheu A, Lanthier G et al. Using fish guilds to assess community responses to temperature and flow regimes in unregulated and regulated Canadian rivers. Freshw Biol. 2016; 61(10):1759–72. https://doi.org/10.1111/fwb.12815
https://doi.org/10.1111/fwb.12815...
; Teresa, Casatti, 2017Teresa FB, Casatti L. Trait-based metrics as bioindicators: Responses of stream fish assemblages to a gradient of environmental degradation. Ecol Indic. 2017; 75:249–58. https://doi.org/10.1016/j.ecolind.2016.12.041
https://doi.org/10.1016/j.ecolind.2016.1...
; Dias et al., 2020Dias RM, Ortega JCG, Strictar L, Santos NCL, Gomes LC, Luz-Agostinho KDG et al. Fish trophic guild responses to damming: Variations in abundance and biomass. River Res Appl. 2020; 36(3):430–40. https://doi.org/10.1002/rra.3591
https://doi.org/10.1002/rra.3591...
), predict local extirpations and extinctions (Angermeier, 1995Angermeier PL. Ecological attributes of extinction-prone species: loss of Virginia freshwater fishes. Conserv Biol. 1995; 9(1):143–58. https://www.jstor.org/stable/2386396
https://www.jstor.org/stable/2386396...
; Parent, Schriml, 1995Parent S, Schriml LM. A model for the determination of fish species at risk based upon life-history traits and ecological data. Can J Fish Aquat Sci. 1995; 52(8):1768–81. https://doi.org/10.1139/f95-769
https://doi.org/10.1139/f95-769...
; Olden et al., 2008Olden JD, Poff NL, Bestgen KR. Trait synergisms and the rarity, extirpation, and extinction risk of desert fishes. Ecology. 2008; 89(3):847–56. https://doi.org/10.1890/06-1864.1
https://doi.org/10.1890/06-1864.1...
), and estimate ecosystem functioning (Mouillot et al., 2011Mouillot D, Villéger S, Scherer-Lorenzen M, Mason NWH. Functional structure of biological communities predicts ecosystem multifunctionality. PLoS ONE. 2011; 6(3):e17476. https://doi.org/10.1371/journal.pone.0017476
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, Moore et al., 2017Moore JW, Olden JD. Response diversity, non-native species, and disassembly rules buffer freshwater ecosystem processes from anthropogenic change. Glob Chang Biol. 2017; 23(5):1871–80. https://doi.org/10.1111/gcb.13536
https://doi.org/10.1111/gcb.13536...
; Moi et al., 2021Moi DA, Romero GQ, Jeppesen E, Kratina P, Alves DC, Antiqueira PAP et al. Regime shifts in a shallow lake over 12 years: Consequences for taxonomic and functional diversities, and ecosystem multifunctionality. J Anim Ecol. 2021; 91(3):551–65. https://doi.org/10.1111/1365-2656.13658
https://doi.org/10.1111/1365-2656.13658...
). Hence, it is a valuable tool for improving theoretical knowledge and supporting management plans for conservation.

Since the functional approach has become an important tool in functional ecology research, many indices have been developed to estimate functional diversity. There is extensive published literature that reviews the properties and applicability of each one (Petchey, Gaston, 2006Petchey OL, Gaston KJ. Functional diversity: back to basics and looking forward. Ecol Lett. 2006; 9(3):741–58.https://doi.org/10.1111/j.1461-0248.2006.00924.x
https://doi.org/10.1111/j.1461-0248.2006...
; Cianciaruso et al., 2009Cianciaruso MV, Silva IA, Batalha MA. Diversidades filogenética e funcional: novas abordagens para a Ecologia de comunidades. Biota Neotrop. 2009; 9(3):93–103. https://doi.org/10.1590/S1676-06032009000300008
https://doi.org/10.1590/S1676-0603200900...
; Maire et al., 2015Maire E, Grenouillet G, Brosse S, Villéger S. How many dimensions are needed to accurately assess functional diversity? A pragmatic approach for assessing the quality of functional space. Glo Ecol Biogeogr. 2015; 24(6):728–40. https://doi.org/10.1111/geb.12299
https://doi.org/10.1111/geb.12299...
; Calaça, Grelle, 2016Calaça AM, Grelle CEV. Diversidade functional de comunidades: discussões conceituais e importantes avanços metodológicos. Oecol Aust. 2016; 20(4):401–16.; Teresa et al., 2021Teresa FB, Rodrigues-Filho CAS, Leitão RP. Diversidade funcional de comunidades de peixes de riacho. Oecol Aust. 2021; 25(2):415–32. https://doi.org/10.4257/oeco.2021.2502.12
https://doi.org/10.4257/oeco.2021.2502.1...
). These indices can be based on functional groups, distance matrices, functional dendrograms, and multidimensional functional spaces. However, although the concept of functional diversity is relatively simple to grasp, a plethora of different indices (Mouchet et al., 2010Mouchet MA, Villéger S, Mason NWH, Mouillot D. Functional diversity measures: an overview of their redundancy and their ability to discriminate Community assembly rules. Funct Ecol. 2010; 24(4):867–76. https://doi.org/10.1111/j.1365-2435.2010.01695.x
https://doi.org/10.1111/j.1365-2435.2010...
; Gómez-Ortiz, Moreno, 2017Gómez–Ortiz Y, Moreno CE. La diversidad funcional en comunidades animales: una revisión que hace énfasis en los vertebrados. Anim Biodivers Conserv. 2017; 40(2):165–74. https://doi.org/10.32800/abc.2017.40.0165
https://doi.org/10.32800/abc.2017.40.016...
; Palacio et al., 2021Palacio FX, Callaghan CT, Cardoso P, Hudgins EJ, Jarzyna MA, Ottaviani G et al. A protocol for reproducible functional diversity analysis. Ecography. 2021; 2022(11):e06287. https://doi.org/10.32942/osf.io/yt9sb
https://doi.org/10.32942/osf.io/yt9sb...
) and potencial functional traits for measuring (Winemiller et al., 2015Winemiller KO, Fitzgerald D, Bower LM, Pianka ER. Functional traits, convergent evolution, and periodic tables of niches. Ecol Lett. 2015; 18(8):737–51. https://doi.org/10.1111/ele.12462
https://doi.org/10.1111/ele.12462...
; Villéger et al., 2017Villéger S, Brosse S, Mouchet M, Mouillot D, Vanni MJ. Functional ecology of fish: current approaches and future challenges. Aquat Sci. 2017; 79:783–801. https://doi.org/10.1007/s00027-017-0546-z
https://doi.org/10.1007/s00027-017-0546-...
; Junker et al., 2022Junker RR, Albrecht J, Becker M, Keuth R, Farwig N, Schleuning M. Towards an animal economics spectrum for ecosystem research. Funct Ecol. 2022; 37(1):57–72. https://doi.org/10.1111/1365-2435.14051
https://doi.org/10.1111/1365-2435.14051...
) makes it difficult for researchers to decide the best approach. Then, this would generate a lot of between-study variation in terms of what is being calculated as functional diversity and how, which would make things less comparable to each other.

Facing the increasing degradation of freshwaters worldwide (Reid et al., 2019Reid AJ, Carlson AK, Creed IF, Eliason EJ, Gell PA, Johnson PTJ et al. Emerging threats and persistent conservation challenges for freshwater biodiversity. Biol Rev. 2019; 94(3):849–73. https://doi.org/10.1111/brv.12480
https://doi.org/10.1111/brv.12480...
), it is necessary to identify and protect species and their functions in the ecosystems. Freshwater ecosystems are home to an extraordinay biodiversity and also they provide essential services for human population. Because the massive alterations of the aquatic ecosystems the biodiversity has dramatically declined and a lot of fish species are facing with extinction (Tickner et al., 2020Tickner D, Opperman JJ, Abell R, Acreman M, Arthington AH, Bunn SE et al. Bending the curve of global freshwater biodiversity loss: An emergency recovery plan. BioScience. 2020; 70(4):330–42. https://doi.org/10.1093/biosci/biaa002
https://doi.org/10.1093/biosci/biaa002...
). In addition, there is a lack of knowledge about species’ traits and their ecological function (Hortal et al., 2015Hortal J, Bello F, Diniz-Filho JAF, Lewinsohn TM, Lobo JM, Ladle RJ. Seven shortfalls that beset large-scale knowledge of biodiversity. Annu Rev Ecol Evol Syst. 2015; 46:523–49. https://doi.org/10.1146/annurev-ecolsys-112414-054400
https://doi.org/10.1146/annurev-ecolsys-...
), which can hinder the selection of conservation priority areas. Thus, it is urgent to understand what we already know and what we can improve in order to assess the functional diversity of freshwater fish.

This concern prompted us to ask a central question: How, where, and why has functional diversity in freshwater fish assemblages been assessed over time? We answered this question by performing a systematic review to identify global trends in studies on the functional diversity of freshwater fish. Specifically, our study focuses on a) exploring how functional diversity has been applied to different biogeographic realms and environments, b) identifying the general background (i.e., the central objective of the study) and the main interest by researchers over time, c) verifying which functional traits and indices have been used to assess functional diversity. To contribute to a theoretical framework on the functional diversity of freshwater fish, we discuss the main gaps found in this study and describe the key perspectives to guide future research. We anticipate that this synthesis will contribute to improving the assessment of functional diversity in freshwater fish assemblages given the relevance of this topic for understanding ecosystem functioning and the current expansion of human effects on aquatic ecosystems.

MATERIAL AND METHODS

In August 2022, we conducted a literature search using the indexed database – the Web of Science (Clarivate Analytics), selecting articles from 1945 up to 2021. This database was used because of the quality of scientific journals encompassing a wide range of publications. For the survey, we used the following Boolean combination of relevant keywords in the “Topic” field: TS = ((fish*) AND (freshwater* OR river* OR stream* OR reservoir* OR aquatic* OR lake* OR lagoon* OR floodplain*) AND (“function* diversit*” OR “function* trait*” OR “environmental trait*” OR “function* richness*” OR “ecological trait*”)). As a result, an initial pool of 1123 articles was retrieved. We screened the titles and abstracts following PRISMA guildelines (Moher et al., 2009Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009; 6(7):e1000097. https://doi.org/10.1371/journal.pmed.1000097
https://doi.org/10.1371/journal.pmed.100...
) to identify whether articles met the criteria for inclusion in this systematic review. To be included in our review, an article must have: i) been a peer reviewed, original research article (no conference abstracts or reviews), and ii) addressed functional diversity of freshwater fish. We excluded Non-English languages studies and articles non related with fish.

We extracted the following information from each article: a) Year of publication; b) Biogeographic realm in which the research was carried out; c) Freshwater environment type; d) General background, i.e., the main objectives of the study; e) Functional traits; f) Functional category; and g) Functional diversity index (Tab. 1). The temporal trend of the number of published articles was investigated using an exponential regression. Since most studies present several objectives, the classification of “general background” reflects the central objective covered by the study and not a specific objective. For example, the studies that addressed the effects of land use on taxonomic and functional structure were classified into “land use” category. Functional traits and functional category were expressed by the total number of traits found in all documents. The total number of articles were used to express the biogeographic realm, freshwater environment type and functional diversity index. Traits occurrence represents the number of times a trait was used in all the articles. Traits with similar nomenclature and meaning were considered only once.

TABLE 1 |
Extracted data from the articles, description of the classification and applcation for each topic analyzed.

RESULTS

We reviewed the full text of 101 articles (Tab. S1). There was an increase in the number of published articles over the years (R2 = 0.91; p < 0.001), mainly after 2013 (Fig. 1). The Neotropical region concentrated the highest number of studies (46 articles), while the Afrotropical region the lowest (1 article) (Fig. 2A). The freshwater ecosystems most assessed in the studies include streams (n = 40 studies) and rivers (n = 28 studies). Reservoirs were the least evaluated environment (n = 4 studies) (Fig. 2B).

FIGURE 1 |
Temporal trend of the number of published articles on the functional diversity of fish in freshwater ecosystems.

FIGURE 2 |
A. World map showing the distribution of research effort among biogeographic realms; B. Pie charts represent the number of studies in each type of aquatic environment per realm. *Global: studies that evaluated more than one biogeographic realm.

We recorded 14 general backgrounds linked to the functional diversity of fish. Among these, biological invasion, land use, and environmental filtering covered 50% of the studies reviewed (Fig. S2). There was an increase in published articles addressing land use and biological invasion after 2015 (Fig. 3A). Biological invasion was the most recorded approach in the Indomalayan region, while land use was addressed mainly in the Neotropical region (Fig. 3B). The other topics showed relatively homogeneous distributions with few studies in each biogeographic realm (Fig. 3B).

Morphological traits were the most applied type of traits (n = 167), while ecological traits were the least used (73 traits) (Fig. 4A; Tab. S3). Feeding and locomotion were the most common categories of traits (Fig. 4B; Tab. S3).

FIGURE 3 |
A. Distribution of the general backgrounds in studies on the functional diversity of freshwater fish over time; B. Distribution of the central objectives in studies in each biogeographic realm.

FIGURE 4 |
A. Total number functional traits types found in our review; B. Total number of functional traits in each category. (Feed = Feeding, Locom = Locomotion, Hab.U = Habitat use, Lif.H = Life history, Phys = Phsysiology) (see Tab. S3).

We identified the use of 16 functional diversity indices in the studies reviewed. The most applied indices were Functional Richness (63% of studies), Functional Evenness (45% of studies), Functional Divergence (33% of studies), and Functional Dispersion (33% of studies) (Tab. 2).

TABLE 2 |
List of functional diversity indices in the reviewed studies, number of studies that used the index and a brief description of each index. *The number of studies does not correspond to the total number of studies reviewed, but the number of studies that used functional indices to measure the functional diversity.

DISCUSSION

Functional diversity is an emergent tool in functional ecology that researchers have been applied over the last decades to address a wide range of issues encompassing at least 14 general backgrounds in studies of freshwater fish worldwide. Our literature search recorded the oldest publication in 2005 (Mouillot et al., 2005Mouillot D, Mason NWH, Dumay O, Wilson JB. Functional regularity: a neglected aspect of functional diversity. Oecologia. 2005; 142:353–59. https://doi.org/10.1007/s00442-004-1744-7
https://doi.org/10.1007/s00442-004-1744-...
), a seminal methodological article in which the authors proposed a new functional diversity index. After 2015, we observed an increased number of publications covering community structure, environmental impacts, and conservation. Functional approach has helped to better understand communities’ responses to environmental disturbances in order to propose more efficient conservation actions in aquatic ecosystems.

Despite the increasing number of publications on the functional diversity of freshwater fish assemblages, the distribution of studies is not homogeneous around the globe. Most of the studies were concentrated in the Neotropical region. This pattern could be due to a large number of water bodies, encompassing a high biodiversity of freshwater fish in this region (~ 4.000 species) (Toussaint et al., 2016Toussaint A, Charpin N, Brosse S, Villéger S. Global functional diversity of freshwater fish is concentrated in the Neotropics while functional vulnerability is widespread. Sci Rep. 2016; 6:22125. https://doi.org/10.1038/srep22125
https://doi.org/10.1038/srep22125...
; Tonella et al., 2022Tonella LH, Ruaro R, Daga VS et al. Neotropical freshwater fishes: A dataset of occurrence and abundance of freshwater fishes in the Neotropics. Ecology. 2022; 104(4):e3713. https://doi.org/10.1002/ecy.3713
https://doi.org/10.1002/ecy.3713...
) and because of the political, economic and social issues at local or regional scales (Pelicice, 2019Pelicice FM. Weak democracies, failed policies, and the demise of ecosystems in poor and developing nations. Trop Conserv Sci. 2019; 12. https://doi.org/10.1177/1940082919839902
https://doi.org/10.1177/1940082919839902...
). In the Neotropical region, Brazil presents a strong role in the studies advance of freshwater fish. The government investments in the early 2000s in Brazil lead the country to play an important role in Latin-American and global science. In addition, the regional scientific collaboration, as well as the development of the Sociedade Brasileira de Ictiologia and the creation of the journal Neotropical Ichthyology has contributed to the progress of scientific knowledge and innovations. In contrast, we recorded only one study in the Afrotropical realm, which also harbor a large number of fishes (~2,000 species). Several countries in the tropical regions need a better governance capacity and more research investments. A combination of limited infrastructure, weak institutions, and poor funding poses challenges to biodiversity research (Barlow et al., 2018Barlow J, França F, Gardner TA, Hicks CC, Lennox GD, Berenguer E et al. The future of hyperdiverse tropical ecosystems. Nature. 2018; 559:517–26. https://doi.org/10.1038/s41586-018-0301-1
https://doi.org/10.1038/s41586-018-0301-...
; Pelicice, 2019Pelicice FM. Weak democracies, failed policies, and the demise of ecosystems in poor and developing nations. Trop Conserv Sci. 2019; 12. https://doi.org/10.1177/1940082919839902
https://doi.org/10.1177/1940082919839902...
).

Another problem in several regions is the lack of investment in collecting and cataloging species. Describing new species, for instance, must be a collaborative global effort, with researchers accessing resources and specimens in many museums and collections, however this is not a simple task once the knowledge of the actual number of species on Earth is unknown. Therefore, without basic research on species and their characteristics, we cannot understand local ecosystems’ biological composition or ecological function, which limits our understanding of other biodiversity topics like species’ life history and functional ecology (Hortal et al., 2015Hortal J, Bello F, Diniz-Filho JAF, Lewinsohn TM, Lobo JM, Ladle RJ. Seven shortfalls that beset large-scale knowledge of biodiversity. Annu Rev Ecol Evol Syst. 2015; 46:523–49. https://doi.org/10.1146/annurev-ecolsys-112414-054400
https://doi.org/10.1146/annurev-ecolsys-...
) and our ability to conserve biodiversity (Barber et al., 2014Barber PH, Ablan-Lagman MCA, Ambariyanto, Berlinck RGS, Cahyani ED, Ravago-Gotanco R et al. Advancing biodiversity research in developing countries: the need for changing paradigms. Bull Mar Sci. 2014; 90(1):187–210. https://doi.org/10.5343/bms.2012.1108
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).

Among the great heterogeneity of freshwater ecosystems, lotic environments were the most assessed. Historically, research on fishes in lotic systems has focused mainly on streams probably because it is easier to sample fishes in small than in large aquatic systems (Johnson et al., 1995Johnson BL, Richardson WB, Naimo TJ. Past, present, and future concepts in large river ecology: How rivers function and how human activies influence river processes. BioScience. 1995; 45(3):134–41. https://doi.org/10.2307/1312552
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; Flotemersch et al., 2006Flotemersch JE, Stribling JB, Paul MJ. Concepts and approaches for the bioassessment of non-wadeable streams and rivers. Washington, DC: US EPA; 2006.) and because the number of streams is greater than that of other water bodies (Teresa et al., 2021Teresa FB, Rodrigues-Filho CAS, Leitão RP. Diversidade funcional de comunidades de peixes de riacho. Oecol Aust. 2021; 25(2):415–32. https://doi.org/10.4257/oeco.2021.2502.12
https://doi.org/10.4257/oeco.2021.2502.1...
). Furthermore, several stream fishes are extremely sensitive to environmental changes and respond markedly to human pressures on aquatic ecosystems, which makes it possible to understand the alterations in fish communities in a short period (Cruz, Pompeu, 2020Cruz LC, Pompeu PS. Drivers of fish assemblage structures in a Neotropical urban watershed. Urban Ecosyst. 2020; 23:819–29. https://doi.org/10.1007/s11252-020-00968-6
https://doi.org/10.1007/s11252-020-00968...
; Silva et al., 2020Silva ALL, Lemes WP, Andriotti J, Petrucio MM, Feio MJ. Recent land-use changes affect stream ecosystem processes in a subtropical island in Brazil. Austral Ecol. 2020; 45(5):644–58. https://doi.org/10.1111/aec.12879
https://doi.org/10.1111/aec.12879...
; Tirupathi, Shashidhar, 2020Tirupathi C, Shashidhar T. Investigating the impact of climate and land-use land cover changes on hydrological predictions over the Krishna river basin under present and future scenarios. Sci Total Environ. 2020; 721:137736. https://doi.org/10.1016/j.scitotenv.2020.137736
https://doi.org/10.1016/j.scitotenv.2020...
). Conversely, large rivers are more challenging to sample compared to streams. Both environments are under intense human activity, especially by industrial pollution, urbanization, and fragmentation (Dias et al., 2020Dias RM, Ortega JCG, Strictar L, Santos NCL, Gomes LC, Luz-Agostinho KDG et al. Fish trophic guild responses to damming: Variations in abundance and biomass. River Res Appl. 2020; 36(3):430–40. https://doi.org/10.1002/rra.3591
https://doi.org/10.1002/rra.3591...
; Kundu et al., 2021Kundu S, Pal S, Talukdar S, Manda I. Impact of wetland fragmentation due to damming on the linkages between water richness and ecosystem services. Environ Sci Pollut Res 2021; 28:50266–85. https://doi.org/10.1007/s11356-021-14123-x
https://doi.org/10.1007/s11356-021-14123...
). The extensive and ever-increasing urbanization creates new landscapes, alters habitats, and causes the loss of natural vegetation cover, which triggers a series of changes in several processes in the aquatic environment (Cerqueira et al., 2020Cerqueira TC, Mendonça RL, Gomes RL, Jesus RM, Silva DML. Effects of urbanization on water quality in a watershed in northeastern Brazil. Environ Monit Assess. 2020; 192(65). https://doi.org/10.1007/s10661-019-8020-0
https://doi.org/10.1007/s10661-019-8020-...
). River impoundments affect a variety of abiotic conditions (Zuluaga-Gómez et al., 2016Zuluaga-Gómez MA, Fitzgerald DB, Giarrizzo T, Winemiller KO. Morphologic and trophic diversity of fish assemblages in rapids of the Xingu River, a major Amazon tributary and region of endemism. Environ Biol Fish. 2016; 99:647–58. https://doi.org/10.1007/s10641-016-0506-9
https://doi.org/10.1007/s10641-016-0506-...
), alter natural flow regimes (Barbarossa et al., 2020Barbarossa V, Schmitt RJP, Huijbregts MAJ, Zarfl C, King H, Schipper AM. Impacts of current and future large dams on the geographic range connectivity of freshwater fish worldwide. Proc Natl Acad Sci USA. 2020; 117(7):3648–55. https://doi.org/10.1073/pnas.1912776117
https://doi.org/10.1073/pnas.1912776117...
), cause shifts in species composition (Arantes et al., 2019Arantes CC, Fitzgerald DB, Hoeinghaus DJ, Winemiller KO. Impacts of hydroelectric dams on fishes and fisheries in tropical rivers through the lens of functional traits. Curr Opin Environ Sustain. 2019; 37:28–40. https://doi.org/10.1016/j.cosust.2019.04.009
https://doi.org/10.1016/j.cosust.2019.04...
), and facilitate the introduction of non-native species (Vitule et al., 2012Vitule JRS, Skóra F, Abilhoa V. Homogenization of freshwater fish faunas after the elimination of a natural barrier by a dam in Neotropics. Divers Distrib. 2012; 18(2):111–20. https://doi.org/10.1111/j.1472-4642.2011.00821.x
https://doi.org/10.1111/j.1472-4642.2011...
). These examples of specific impacts on the lotic ecosystems and their consequences to communities may explain the higher number of studies in these environments.

In general, freshwater ecosystems are among the most threatened environments, and it has concerned researchers due to the rapid biodiversity loss worldwide. Unsurprisingly, biological invasion and land use have been imminent concerns of ecologists for decades. However, we noticed that only over the last five years has functional diversity been applied as an approach to evaluate the effects of such disturbances in local communities. Studies have reported alterations in fish functional diversity due to the introduction of non-native species (Shuai et al., 2018Shuai F, Lek S, Li X, Zhao T. Biological invasions undermine the functional diversity of fish community in a large subtropical river. Biol Invasions. 2018; 20:2981–96. https://doi.org/10.1007/s10530-018-1751-y
https://doi.org/10.1007/s10530-018-1751-...
; Millardi et al., 2019Millardi M, Gavioli A, Soininen J, Castaldelli G. Exotic species invasions undermine regional functional diversity of freshwater fish. Sci Rep. 2019; 9:17921. https://doi.org/10.1038/s41598-019-54210-1
https://doi.org/10.1038/s41598-019-54210...
; Rojas et al., 2020Rojas P, Castro SA, Vila I, Jaksic FM. Exotic species modify the functional diversity patterns of freshwater fish assemblages in continental Chile: Examining historical and geographical patterns. Glob Ecol Cons. 2020; 24:e01355. https://doi.org/10.1016/j.gecco.2020.e01355
https://doi.org/10.1016/j.gecco.2020.e01...
) and because of the effects of land use alterations (Leitão et al., 2018Leitão RP, Zuanon J, Mouillot D, Leal CG, Hughes RM, Kaufmann PR et al. Disentangling the pathways of land use impacts on the functional structure of fish assemblages in Amazon streams. Ecography. 2018; 41(1):219–32. https://doi.org/10.1111/ecog.02845
https://doi.org/10.1111/ecog.02845...
; Alvarenga et al., 2021Alvarenga LRP, Pompeu PS, Leal CG, Hughes RM, Fagundes DC, Leitão RP. Land-use changes affect the functional structure of stream fish assemblages in the Brazilian Savanna. Neotrop Ichthyol. 2021; 19(3):e210035. https://doi.org/10.1590/1982-0224-2021-0035
https://doi.org/10.1590/1982-0224-2021-0...
; Larentis et al., 2022Larentis C, Pavanelli CS, Delariva RL. Do environmental conditions modulated by land use drive fish functional diversity in streams? Hydrobiologia. 2022; 849:4465–83. https://doi.org/10.1007/s10750-021-04756-x
https://doi.org/10.1007/s10750-021-04756...
). Consequently, changes in functional diversity imply changes in the dynamic and stability of communities. For example, introducing non-native species can promote biotic homogenization, decreasing the functional diversity of fish communities in the long term. We also highlight the greater number of studies addressing the impacts of land use in the Neotropical region. These studies are important because the Neotropical region faces intense agricultural and livestock production, accelerating habitat loss and fragmentation. Furthermore, political neglect in many South American countries has increased deforestation rates over the last years, justifying the concerns of the academic community about the effects of land use on the ichthyofauna (Casatti et al., 2015Casatti L, Teresa FB, Zeni JO, Ribeiro MD, Brejão GL, Ceneviva-Bastos M. More of the same: High functional redundancy in stream fish assemblages from tropical agroecosystems. Environ Manage. 2015; 55:1300–14. https://doi.org/10.1007/s00267-015-0461-9
https://doi.org/10.1007/s00267-015-0461-...
; Zeni et al., 2017Zeni JO, Hoeinghaus DJ, Casatti L. Effects of pasture conversion to sugarcane for biofuel production on stream fish assemblages in tropical agroecosystems. Freshw Biol. 2017; 62(12):2026–38. https://doi.org/10.1111/fwb.13047
https://doi.org/10.1111/fwb.13047...
; Leitão et al., 2018Leitão RP, Zuanon J, Mouillot D, Leal CG, Hughes RM, Kaufmann PR et al. Disentangling the pathways of land use impacts on the functional structure of fish assemblages in Amazon streams. Ecography. 2018; 41(1):219–32. https://doi.org/10.1111/ecog.02845
https://doi.org/10.1111/ecog.02845...
; Larentis et al., 2022Larentis C, Pavanelli CS, Delariva RL. Do environmental conditions modulated by land use drive fish functional diversity in streams? Hydrobiologia. 2022; 849:4465–83. https://doi.org/10.1007/s10750-021-04756-x
https://doi.org/10.1007/s10750-021-04756...
).

To assess the functional diversity of fish, researchers have used more morphological traits than ecological traits, probably owing to the facility to obtain these morphological measures (Villéger et al., 2017Villéger S, Brosse S, Mouchet M, Mouillot D, Vanni MJ. Functional ecology of fish: current approaches and future challenges. Aquat Sci. 2017; 79:783–801. https://doi.org/10.1007/s00027-017-0546-z
https://doi.org/10.1007/s00027-017-0546-...
), especially from databases such as FishMorph (Brosse et al., 2021Brosse S, Charpin N, Su G, Toussaint A, Herrera-R GA, Tedesco PA et al. FISHMORPH: A global database on morphological traits of freshwater fish. Glob Ecol Biogeogr. 2021; 30(12):2330–36. https://doi.org/10.1111/geb.13395
https://doi.org/10.1111/geb.13395...
) and Fishbase (Froese, Pauly, 2023Froese R, Pauly D. FishBase. 2023. World Wide Web electronic publication. 2023. Available from: www.fishbase.org), which provides several ecomorphological traits for many fish species. Conversely, ecological traits are less representative because it is more difficult or expensive to measure (Vitule et al., 2017Vitule JRS, Agostinho AA, Azevedo-Santos VM, Daga VS, Darwall WRT, Fitzgerald DB et al. We need a better understanding about functional diversity and vulnerability of tropical freshwater fishes. Biodivers Conserv. 2017; 26:757–62. https://doi.org/10.1007/s10531-016-1258-8
https://doi.org/10.1007/s10531-016-1258-...
). The fishes present a wide range of traits (Nelson, 2006Nelson JS. Fishes of the world. Wiley, Hoboken; 2006.) that can be linked to several niche dimensions (Villéger et al., 2017Villéger S, Brosse S, Mouchet M, Mouillot D, Vanni MJ. Functional ecology of fish: current approaches and future challenges. Aquat Sci. 2017; 79:783–801. https://doi.org/10.1007/s00027-017-0546-z
https://doi.org/10.1007/s00027-017-0546-...
). However, many of the traits related to the autecology of species (i.e., reproduction, growth, development, tolerance) remain unknown (Matthews, 2012Matthews WJ. Patterns in freshwater fish ecology. Chapman & Hall; 2012.; Teresa et al., 2021Teresa FB, Rodrigues-Filho CAS, Leitão RP. Diversidade funcional de comunidades de peixes de riacho. Oecol Aust. 2021; 25(2):415–32. https://doi.org/10.4257/oeco.2021.2502.12
https://doi.org/10.4257/oeco.2021.2502.1...
). Studies on the basic ecology of fish have typically concentrated on larger species or species of commercial importance (Honji et al., 2008Honji RM, Narcizo AM, Borella MI, Romagosa E, Moreira RG. Pattens of oocyte development in natural habitat and captive Salminus hilarii Valenciennes, 1850 (Teleostei: Characidae). Fish Physiol Biochem. 2008; 35:109–23. https://doi.org/10.1007/s10695-008-9239-9
https://doi.org/10.1007/s10695-008-9239-...
; Normando et al., 2009Normando FT, Arantes FP, Luz RK, Thomé RG, Rizzo E, Sato Y et al. Reproduction and fecundity of tucunaré, Cichla kelberi (Perciformes: Cichlidae), an exotic species in Três Marias Reservoir, Southeastern Brazil. J App Ichthyol. 2009; 25(3):299–305. https://doi.org/10.1111/j.1439-0426.2008.01174.x
https://doi.org/10.1111/j.1439-0426.2008...
; Bailly et al., 2011Bailly D, Batista-Silva VF, Abelha MCF, Kashiwaqui EAL, Fernandes CA Carvalho ED. Relative abundance and reproductive tactics of a Loricariidae species at Saraiva Lagoon, Ilha Grande National Park, MS-PR, Brazil. Biota Neotrop. 2011; 11(3):171–78. http://dx.doi.org/10.1590/S1676-06032011000300014
http://dx.doi.org/10.1590/S1676-06032011...
; Cook-Hildreth et al., 2016Cook-Hildreth SL, Bonner TH, Huffman DG. Female reproductive biology of an exotic suckermouth armored catfish (Loricariidae) in the San Marcos River, Hays Co., Texas, with observations on environmental triggers. BioInvasions Rec. 2016; 5(3):173–83. http://dx.doi.org/10.3391/bir.2016.5.3.09
http://dx.doi.org/10.3391/bir.2016.5.3.0...
). As mentioned, the technical difficulties in selecting and measuring some functional traits bound researchers to use a small set of traits (Gómez-Ortiz, Moreno, 2017Gómez–Ortiz Y, Moreno CE. La diversidad funcional en comunidades animales: una revisión que hace énfasis en los vertebrados. Anim Biodivers Conserv. 2017; 40(2):165–74. https://doi.org/10.32800/abc.2017.40.0165
https://doi.org/10.32800/abc.2017.40.016...
). For instance, when a functional trait is unavailable for one species, researchers have extrapolated some information to genus or family level (e.g., trophic guild) (Carvalho, Tejerina-Garro, 2015aCarvalho RA, Tejerina-Garro FL. Environmental and spatial processes: what controls the functional structure of fish assemblages in tropical rivers and headwater streams? Ecol Freshw Fish. 2015a; 24(2):317–28. https://doi.org/10.1111/eff.12152
https://doi.org/10.1111/eff.12152...
,bCarvalho RA, Tejerina-Garro FL. Relationships between taxonomic and functional components of diversity: implications for conservation of tropical freshwater fishes. Freshw Biol. 2015b; 60(9):1854–62. https://doi.org/10.1111/fwb.12616
https://doi.org/10.1111/fwb.12616...
; Vitorino Júnior et al., 2016Vitorino Júnior OB, Fernandes R, Agostinho CS, Pelicice FM. Riverine networks constrain b-diversity patterns among fish assemblages in a large Neotropical river. Freshw Biol. 2016; 61(10):1733–45. https://doi.org/10.1111/fwb.12813
https://doi.org/10.1111/fwb.12813...
). As a result, only a subset of the functional diversity would be assessed (Vitule et al., 2017Vitule JRS, Agostinho AA, Azevedo-Santos VM, Daga VS, Darwall WRT, Fitzgerald DB et al. We need a better understanding about functional diversity and vulnerability of tropical freshwater fishes. Biodivers Conserv. 2017; 26:757–62. https://doi.org/10.1007/s10531-016-1258-8
https://doi.org/10.1007/s10531-016-1258-...
; Silva et al., 2020Silva ALL, Lemes WP, Andriotti J, Petrucio MM, Feio MJ. Recent land-use changes affect stream ecosystem processes in a subtropical island in Brazil. Austral Ecol. 2020; 45(5):644–58. https://doi.org/10.1111/aec.12879
https://doi.org/10.1111/aec.12879...
).

We suggest that a starting point to contribute to this issue could be the creation of functional traits databases, on a regional scale to address more local biodiversity knowledge shortfalls and minimize geographic variation in species traits. It would allow us to compare more efficiently different datasets taking account the local role of species, which is essential to identify priority areas for conservation (Mouillot et al., 2014Mouillot D, Villeger S, Parravicini V, Kulbicki M, Arias-Gonzáles JE, Bender M et al. Functional over-redundancy and high-functional vulnerability in global fish faunas on tropical reefs. Proc Natl Acad Sci USA. 2014; 111(38):13757–62. https://doi.org/10.1073/pnas.1317625111
https://doi.org/10.1073/pnas.1317625111...
). As an example, Frimpong, Angermeier, (2009)Frimpong EA, Angermeier PL. Fish traits: A database of ecological and life-history traits of freshwater fishes of the United States. Fish Res. 2009; 34(10):487–95. https://doi.org/10.1577/1548-8446-34.10.487
https://doi.org/10.1577/1548-8446-34.10....
compiled over 100 traits for 809 fish species from freshwaters in the United States. However, creating a database may be challenging for ecologists as it depends on experimental and observational studies, so the effort should be a joint work of the scientific community interested in this field. The Societies such as Sociedade Brasileira de Ictiologia, has the mission of becoming an international forum for the dissemination and discussion of original research on the diversity of Neotropical marine, estuarine and freshwater fish, which has helped to expand knowledge about the diverse Neotropical ichthyofauna. Thus, we suggest that the challenges, limitations and solutions for creating the datasets would be a good point to discuss by scientists in further events.

In addition, we also highlight the importance of the authors making data available for compilation. We noticed that most studies did not provide the species lists and their functional traits. Therefore, we could be creating a more collaborative culture of providing our data and, when using someone else’s dataset just asking them to collaborate in any product. Even if the functional approach is independent of taxonomic identity, providing species lists would describe local patterns and guide new research. For example, using datasets to predict changes or losses of functional diversity facing climate change, river fragmentation, biological invasions. In short, we need to know to conserve, we need to share our knowledge and our data to protect biodiversity.

Regarding the category of functional traits, our results indicate that traits related to feeding and locomotion were the most applied. Indeed, this result is associated with our findings regarding the type of traits since most morphological traits were linked with these two fundamental niche dimensions of species (Tab. S3). Furthermore, it has been suggested that feeding and locomotion traits are good descriptors of species’ function (Villéger et al., 2017Villéger S, Brosse S, Mouchet M, Mouillot D, Vanni MJ. Functional ecology of fish: current approaches and future challenges. Aquat Sci. 2017; 79:783–801. https://doi.org/10.1007/s00027-017-0546-z
https://doi.org/10.1007/s00027-017-0546-...
), which supports the application of these categories in niche width. The number of traits to describe food acquisition is high, including morpho-anatomical traits representing each step of the food acquisition process and a qualitative classification that may be based on categories describing trophic level (Villéger et al., 2017Villéger S, Brosse S, Mouchet M, Mouillot D, Vanni MJ. Functional ecology of fish: current approaches and future challenges. Aquat Sci. 2017; 79:783–801. https://doi.org/10.1007/s00027-017-0546-z
https://doi.org/10.1007/s00027-017-0546-...
). However, the low number of traits representing the other categories may be associated with the type of functional trait that represents each category. For instance, life history is another fundamental niche dimension less explored because it includes poorly known traits such as fecundity, egg diameter, and spawning substrate. Finally, the low usage of some trait categories might be related to them not being directly tied to the studies’ central question.

With the advance in functional ecology, numerous functional indices have been developed to assess functional diversity and obtain conclusions about community responses to environmental changes and ecosystem functioning. Functional Richness (FRic) appears to be the most widely used functional diversity index, mainly coupled with Functional Evenness (FEve) and Functional Divergence (FDiv). These indices are one of the first indices developed to assess functional diversity (Mason et al., 2005Mason NWH, Mouillot D, Lee WG, Wilson JB. Functional richness, functional evenness and functional divergence: the primary components of functional diversity. Oikos. 2005; 111(1):112–18. https://doi.org/10.1111/j.0030-1299.2005.13886.x
https://doi.org/10.1111/j.0030-1299.2005...
; Villéger et al., 2008Villéger S, Mason NWH, Mouillot D. New multidimensional functional diversity indices for a multifaceted framework in functional ecology. Ecology. 2008; 89(8):2290–301. https://www.jstor.org/stable/27650754
https://www.jstor.org/stable/27650754...
) and allow the understanding of complementary facets of functional diversity (Mouillot et al., 2013Mouillot D, Graham NAJ, Villéger S, Mason NWH, Bellwood DR. A functional approach reveals community responses to disturbances. Trends Ecol Evol. 2013; 28(3):167–77. https://doi.org/10.1016/j.tree.2012.10.004
https://doi.org/10.1016/j.tree.2012.10.0...
). For example, Tucker et al., (2017)Tucker CM, Cadotte MW, Carvalho SB, Davies TJ, Ferrier S, Fritz SA et al. A guide to phylogenetic metrics for conservation, community ecology and macroecology. Biol Rev. 2017; 92(2):698–715. https://doi.org/10.1111/brv.12252
https://doi.org/10.1111/brv.12252...
suggest that the intuitive, unifying framework of the phylogenetic dimensions – richness, divergence, and regularity of traits – is very useful, since it applies to biological questions at multiple ecological scales, for single or multiple groups of species, and across fields.

Our findings reveal that fish functional diversity has been globally assessed for several purposes. The main concerns addressed by scientists were the effects of biological invasions and land use on fish assemblages. The main shortfall that hampers the applicability of the functional approach is the shortage of information on the autecology of fishes. Describing basic information about species ecology is a challenge for researchers since the rapid alterations of freshwater ecosystems accelerate species loss even before knowing them. Therefore, we emphasize the need for more research related to the basic ecology of freshwater fish to improve the use of the functional approach. We also reinforce the need to incorporate the functional facet in conservation plans once the studies have reported losses on fish functional diversity in freshwater ecosystems.

ACKNOWLEDGEMENTS

The Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) provided LCG with a doctoral scholarship and RMD with research fellowships. We are grateful to Job D. R. Borges for his contribution to the search of the articles and Prof. Fabricio Teresa for his suggestions and contribution to the manuscript.

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ADDITIONAL NOTES

  • HOW TO CITE THIS ARTICLE

    Gomes LC, Dias RM, Ruaro R, Benedito E. Functional diversity: a review on freshwater fish research. Neotrop Ichthyol. 2023; 21(2):e230022. https://doi.org/10.1590/1982-0224-2023-0022

Edited-by

Lilian Casatti

Publication Dates

  • Publication in this collection
    10 July 2023
  • Date of issue
    2023

History

  • Received
    6 May 2022
  • Accepted
    29 May 2023
Sociedade Brasileira de Ictiologia Neotropical Ichthyology, Núcleo de Pesquisas em Limnologia, Ictiologia e Aquicultura, Universidade Estadual de Maringá., Av. Colombo, 5790, 87020-900, Phone number: +55 44-3011-4632 - Maringá - PR - Brazil
E-mail: neoichth@nupelia.uem.br