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.


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, 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., 2017).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., 2005;Cadotte et al., 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., 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., 2014;Fitzgerald et al., 2017;Oliveira et al., 2018), elucidate responses to environmental impacts (Dala-Corte et al., 2016;Macnaughton et al., 2016;Teresa, Casatti, 2017;Dias et al., 2020), predict local extirpations and extinctions (Angermeier, 1995;Parent, Schriml, 1995;Olden et al., 2008), and estimate ecosystem functioning (Mouillot et al., 2011, Moore et al., 2017;Moi et al., 2021).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, 2006;Cianciaruso et al., 2009;Maire et al., 2015;Calaça, Grelle, 2016;Teresa et al., 2021).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., 2010;Gómez-Ortiz, Moreno, 2017;Palacio et al., 2021) and potencial functional traits for measuring (Winemiller et al., 2015;Villéger et al., 2017;Junker et al., 2022) 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., 2019), 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, 2020).In addition, there is a lack of knowledge about species' traits and their ecological function (Hortal et al., 2015), 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* Functional diversity of freshwater fish 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., 2009) 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.

RESULTS
We reviewed the full text of 101 articles (Tab.S1).There was an increase in the number of published articles over the years (R 2 = 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).
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).
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).Functional diversity of freshwater fish

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., 2005), 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., 2016;Tonella et al., 2022) and because of the political, economic and social issues at local or regional scales (Pelicice, 2019).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., 2018;Pelicice, 2019).
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., 2015) and our ability to conserve biodiversity (Barber et al., 2014).
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., 1995;Flotemersch et al., 2006) and because the number of streams is greater than that of other water bodies (Teresa et al., 2021).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, 2020;Silva et al., 2020;Tirupathi, Shashidhar, 2020) (Dias et al., 2020;Kundu et al., 2020).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., 2020).River impoundments affect a variety of abiotic conditions (Zuluaga-Gómez et al., 2016), alter natural flow regimes (Barbarossa et al., 2020), cause shifts in species composition (Arantes et al., 2019), and facilitate the introduction of non-native species (Vitule et al., 2012).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., 2018;Millardi et al., 2019;Rojas et al., 2020) and because of the effects of land use alterations (Leitão et al., 2018;Alvarenga et al., 2021;Larentis et al., 2021).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., 2015;Zeni et al., 2017;Leitão et al., 2018;Larentis et al., 2021).
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., 2017), especially from databases such as FishMorph (Brosse et al., 2021) and Fishbase (Froese, Pauly, 2023), 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., 2017).The fishes present a wide range of traits (Nelson, 2006) that can be linked to several niche dimensions (Villéger et al., 2017).However, many of the traits related to the autecology of species (i.e., reproduction, growth, development, tolerance) remain unknown (Matthews, 2012;Teresa et al., 2021).Studies on the basic ecology of fish have typically concentrated on larger species or species of commercial importance (Honji et al., 2008;Normando et al., 2009;Bailly et al., 2011;Cook-Hildreth et al., 2016).As mentioned, the technical difficulties in selecting and measuring some functional traits bound researchers to use a small set of traits (Gómez-Ortiz, Moreno, 2017).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, 2015a,b;Vitorino Júnior et al., 2016).As a result, only a subset of the functional diversity would be assessed (Vitule et al., 2017;Silva et al., 2019).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., 2014).As an example, Frimpong, Angermeier (2009) 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 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., 2017), which supports the application of these categories in niche width.The number of traits to describe food acquisition is high, including morphoanatomical 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., 2017).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., 2005;Villéger et al., 2008) et al., 2013).For example, Tucker et al. (2017) 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.

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

FIGURE 3 |
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.

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