Ecological Indicators 81 (2017) 124–131

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Ecological Indicators
journal homepage: www.elsevier.com/locate/ecolind

Review

Using river microalgae as indicators for freshwater biomonitoring: Review MARK

of published research and future directions
⁎
Naicheng Wua,b, , Xuhui Donga,c, Yang Liud,e, Chao Wangf, Annette Baattrup-Pederseng,
Tenna Riisb
a
Aarhus Institute of Advanced Studies, Aarhus University, Høegh-Guldbergs Gade 6B, 8000 Aarhus C, Denmark
b
Department of Bioscience, Aarhus University, Ole Worms Allé 1, 8000 Aarhus C, Denmark
c
Nanjing Institute of Geography and Limnology, Chinese Academy of Sciences, 210008 Nanjing, China
d
Institute for Advanced Studies, Shenzhen University, 518060 Shenzhen, China
e
Key Laboratory of Optoelectronic Devices and Systems of Ministry of Education and Guangdong Province, College of Optoelectronic Engineering, Shenzhen University,
518060 Shenzhen, China
f
Pearl River Fisheries Research Institute, Chinese Academy of Fishery Science, 510380 Guangzhou, China
g
Department of Bioscience, Aarhus University, Vejlsøvej 25, 8600 Silkeborg, Denmark

A R T I C L E I N F O A B S T R A C T

Keywords: Trait-based approaches may give insights into underlying mechanisms of relationships between biological
Riverine microalgae communities and environmental stressors, and are increasingly used in ecological studies, but are only very
Lotic ecosystem functions recently considered for freshwater riverine microalgae. Here, we i) review the research trend in riverine mi-
Trait-based biomonitoring croalgae during the past 26 years in order to conduct a quantitative and qualitative analysis for global trends in
Multiple stressors
the research field, ii) summarize the use of algae traits in riverine biomonitoring and iii) propose future research
Global change
perspectives. The bibliometric analysis showed that the annual number of publications on microalgae increased
significantly from 1991 to 2016, although their proportions to total numbers of scientific articles remained
steady. The studies have become increasingly concerned on issues arisen from global environmental changes
such as “eutrophication”, “pollution”, “land use”, “biomonitoring”, “biodiversity”, “functional group”, etc. The
use of algae traits in biomonitoring has become popular and includes e.g. functional diversity, cell size, guild, life
form, eco-morphology, spore formation as well as algal quality. Here we collate all relevant algal traits, their
different categories and propose their responses to resource supply and disturbance frequency in a conceptual
model, which should be validated in future studies. In order to expand the knowledge and future use of mi-
croalgae in biomonitoring research efforts should also include: i) description of relationships between algal traits
and ecosystem functions (e.g., nutrient uptake, metabolism, energy transfer across the food web) and underlying
mechanisms; ii) selection of robust traits reflecting and disentangling the effects of multiple stressors; iii) water
resource management in an interdisciplinary manner linking risk assessment and management scenarios by an
integrated modelling system using microalgae.

1. Introduction scientific study of algae) as a research field has undergone several

stages. The first stage was from late 18th to late 19th century with
Algae (both eukaryotics and cyanobacteria) occupy nearly every descriptive work of scholars, such as Carl Adolph Agardh (1785–1859),
aquatic environment including fresh and marine waters, moist terres- who firstly emphasized the importance of the reproductive characters
trial habitats, such as soils and rock surfaces, and they also live on of algae and the use of these to distinguish different genera and families
living surfaces such as plants and animals (Hoffmann, 1989; Round (Papenfuss, 1976). The second stage started from the late 19th century,
et al., 1990). While algae were known by the ancient Greeks and Ro- when phycology became a recognized research field of its own. Scholars
mans, records as far back as 3000 BC indicated that algae already at such as Friedrich Traugott Kützing (1807–1893) continued the de-
that time were used by the emperor of China as food (Huisman, 2000; scriptive work with systematic recordings, extensive distribution map-
Porterfield, 1922). Since the late 18th century with the description and ping and the development of identification keys. The third stage was
naming of Ecklonia maxima (Pehr Osbeck) in 1757, phycology (i.e. from the early 20th century up to now. In this stage a rapid progress has

⁎
Corresponding author at: Aarhus Institute of Advanced Studies, Aarhus University, Høegh-Guldbergs Gade 6B, 8000 Aarhus C, Denmark.
E-mail addresses: [email protected], [email protected] (N. Wu).

http://dx.doi.org/10.1016/j.ecolind.2017.05.066
Received 2 March 2017; Received in revised form 22 May 2017; Accepted 25 May 2017
Available online 03 June 2017
1470-160X/ © 2017 Elsevier Ltd. All rights reserved.
N. Wu et al. Ecological Indicators 81 (2017) 124–131

been made and numerous key books have been published. Two im- traditional taxonomic indices, traits possess many merits: 1) most traits
portant new research areas were also initiated during this last stage need only assignment to different categories and do not need complex
including investigations of freshwater algae (most previous work was algorithm, 2) traits show greater consistency in their responses across
done with marine algae) and the use of algae in bio-assessments, war- temporal and spatial scales (Menezes et al., 2010; Soininen et al.,
ranted by decreased water quality of freshwater ecosystems due to in- 2016), 3) traits can potentially be transferrable across geographic re-
tensive human disturbances. During the last decades the concepts and gions since different geographic regions are likely to contain similar
tools for assessing ecosystem health and diagnosing causes of impair- complements of traits although they might be characterized by distinct
ment in streams and rivers have developed rapidly (Stevenson et al., taxonomic composition (Van den Brink et al., 2011), 4) traits can serve
2010). to tackle with complex mixture of stressors, e.g., disentanglement of
Algae (benthic and pelagic) are increasingly being used as reliable multiple interacting influential factors (Baattrup-Pedersen et al., 2016),
environmental indicators in streams and rivers globally (Lange et al., 5) they can give important insights into the mechanisms driving the
2016; Wu et al., 2012) because they strongly respond to environmental community and ecosystem processes along the gradients of influential
changes (Dong et al., 2016; Stevenson et al., 2010). Especially three factors including responses to global change (Litchman and Klausmeier,
major properties merit their use in ecosystem monitoring (Hötzel and 2008). In fact, functional traits have been used for different purposes in
Croome, 1999): (i) they have a high sensitivity to environmental terrestrial plants (Grime, 1979; Tilman, 1980) and macroinvertebrate
changes, (ii) they are easy to sample, and (iii) most species are cos- (Menezes et al., 2010), but have only very recently been considered for
mopolitan with well-known autecology (Porter, 2008; van Dam et al., freshwater algae (Lange et al., 2016; McGill et al., 2006; Tapolczai
1994). As a consequence, many assessment methods based on micro- et al., 2016), in particular in phytoplankton studies (Colina et al., 2016;
algae (especially diatoms, a key component of stream benthic and pe- Padisák et al., 2009; Reynolds et al., 2002; Thomas et al., 2016), and a
lagic algae) have been developed in several countries and regions growing number of investigations in benthic algae have also adopted a
(Siddig et al., 2016). Generally, the assessment methods build on one of trait-based approach. A broadly accepted trait nowadays is guilds (i.e.,
three different approaches. The first approach is based on community low profile, high profile, motile) of diatoms (Berthon et al., 2011; Dong
composition and the ecological preferences and/or tolerances of species et al., 2016; Lange et al., 2011; Soininen et al., 2016; Tang et al., 2013),
or taxa within the community (Kolkwitz and Marsson, 1908), for in- which can reflect not only the difference of dispersal ability, but also
stance, the Pollution Sensitivity Index (PSI) (Kelly et al., 1995), the the environmental adaptability (Passy, 2007). Meanwhile, other bio-
Trophic Diatom Index (TDI) (Kelly and Whitton, 1995), the Pollution logical traits based on cell sizes, life history, physiology, behaviour and
Tolerance Index (PTI) (Kentucky Department for Environmental morphology have been proposed recently (Lange et al., 2016).
Protection Division, 2002), the Q index (Borics et al., 2007) and the In this paper we describe research trends in past years, and by
Trophic Index of Potamoplankton (TIP) (Mischke and Behrendt, 2007). collecting the latest trait-based approaches and existing attempts, we
The second approach relies on algal diversity as a general indicator of aim to identify future research gaps in order to progress the use of algal
river health (i.e. ecological integrity). The third approach can be seen as traits in biomonitoring. Specifically, the goals of this review are to 1)
a mixture of the previous two approaches combining the different in- describe research trends of river microalgae in the past 26 years by
dices in multimetric indices, like for instance the Index of Biotic In- conducting a bibliometric analysis, 2) summarize the current algal
tegrity (IBI) (Karr, 1981). The third approach is preferred by more and traits used in riverine biomonitoring, and 3) propose future research
more researchers for purposes of risk assessment and management of directions and applications.
freshwater ecosystems and has been developed for different types of
impairments in various regions (Bae et al., 2010; Birk et al., 2012; Dong 2. Methods
et al., 2015; Zalack et al., 2010; Zhu and Chang, 2008).
Despite the increasing popularity of using these three approaches, 2.1. Terminology of river microalgae
some studies have shown that the first two approaches have not always
been successful (Tang et al., 2006). For instance, nonlinear relationship River microalgae can be divided into two main categories: pelagic
between anthropogenic impacts and response of indices (Allan, 2004) algae and benthic algae. Pelagic algae are algae suspended in the water
resulted in potential bias for assessment. Moreover, if we look at the column and most previous studies have been carried out in lowland
most used indices, summarized in a previous review (Wu et al., 2014), rivers or streams with long retention time and low flow current (Abonyi
in research papers (Dong et al., 2015; Tang et al., 2006; van Dam et al., et al., 2014; Basu and Pick, 1996; Piirsoo et al., 2008; Sabater et al.,
1994; Wang et al., 2005) and in books (Mischke and Behrendt, 2007; 2008). In the literature, more popularly used terms are “phyto-
Stevenson et al., 2010), it becomes obvious that the algorithm of many plankton”, “potamoplankton”, “phytoseston” or “riverine algae”. In
of these (e.g., TDI, PSI, PTI, TIP) is highly complex with a low degree of contrast to the pelagic algae, benthic algae grow on the surfaces of
transparency. Furthermore, these approaches largely ignore that bottom sediments and are most commonly filamentous or colonial
freshwater environments are exposed to a complex mixture of stressors forms, but may also be microscopic single celled organisms. Former
arising from global change including water abstraction, intensive investigations have been conducted mostly in mountainous streams
farming land use and climate change (Dudgeon et al., 2006; Hering with short retention time and high flow velocity (Birk et al., 2012;
et al., 2015; Vörösmarty et al., 2010). Consequently, the use of indices Soininen et al., 2016; Wang et al., 2005). Except for “benthic algae”,
developed to target single stressors is inadequate and new approaches other widely used terms are “periphyton”, “benthic diatom”, “diatom”,
are needed to deal with this complexity. “eplithic algae/diatom”, “epiphytic algae/diatom”, “epipelic algae/
Recent studies have shown the advantages of applying traits for diatom”, etc. In this study, however, to unify the terminology, we
biomonitoring of freshwater ecosystems and for biodiversity con- confine to either “pelagic algae” or “benthic algae” (but for the pub-
servation (Di Battista et al., 2016; Lange et al., 2011; Litchman and lication searching, we used all keywords referred above).
Klausmeier, 2008; McGill et al., 2006; Menezes et al., 2010; Soininen
et al., 2016). A trait is defined as a characteristic that reflects a species 2.2. Data sources, methods and results
adaption to its environment (Menezes et al., 2010). Usually traits are
divided into two types: ecological traits (related to habitat preferences, We used a bibliometric analysis similar to a previous study (Wang
like pH, oxygen and temperature tolerance, tolerance to organic pol- et al., 2015) with a minor modification of the keywords used. All ar-
lution, etc.) and biological traits (e.g., life history, physiological, be- ticles containing the keyword “river microalgae”; “pelagic algae”;
havioural and morphological characteristics, such as reproductive “phytoplankton”; “potamoplankton”; “phytoseston”; “benthic algae”;
strategies, motility, cell size, life form, etc.). In comparison with “periphyton”; “benthic diatom”; “diatom”; “eplithic algae”; “eplithic

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which would be valid for both pelagic and benthic algae (Table 1), as
complementary to traditional taxonomic based indices that have been
summarized previously (Mischke and Behrendt, 2007; Wu et al., 2014).
A total of 12 algal traits, which belong to 79 categories (for details see
Table 1) have been widely used recently (Berthon et al., 2011; Centis
et al., 2010; Ferragut and Campos Bicudo, 2010; Guo et al., 2016a;
Passy, 2007; Rimet and Bouchez, 2012), but some obvious and con-
cerning constrains exist:
(i) Trait categories are continuously being updated and taxa as-
signments to different categories are still controversial and a more
complete and reliable assignment system for all algal taxa is therefore
of high priority to advance the use of trait-based approaches in the
future. Classification of diatom guilds, for instance, has mostly been
based on the study of Passy (2007) with three guilds (i.e., low profile,
high profile and motile taxa), but Rimet and Bouchez (2012) proposed
modifications by adding a fourth ecological guild (i.e., planktonic taxa)
Fig. 1. Temporal trend of the research articles and its proportion in total databases from and furthermore suggested some revisions. For example, planktonic
1991 to 2016. species were excluded from the low profile guild (e.g., Cyclotella spp.,
Stephanodiscus spp., Supplementary Table S1) and all taxa presenting
diatom”; “epiphytic algae”; “epiphytic diatom”; “epipelic algae” and the largest size class (> 1500 μm3, e.g., Cymbella lanceolata, Eucocconeis
“epipelic diatom” in the title published between 1991 and 2016; were flexella, Achnanthes brevipes, etc.) were moved from the low profile guild
queried from all citation indexes on Web of Science (Thomson Reuters). to the high profile guild (Rimet and Bouchez, 2012). Nevertheless, the
An XML file containing titles; keywords; abstracts; year of publication; assignment of Frustulia spp. was still unclear: some regarded it as high
authors’ names and authors’ affiliations; cited times and cited reference profile guild (Passy, 2007; Rimet and Bouchez, 2012) while others re-
counts was generated. The search query was constructed as: TI = (river garded it as a motile taxa (Dong et al., 2016; Passy and Larson, 2011;
OR stream) AND TI = (microalgae OR pelagic algae OR algae OR algal Stenger-Kovács et al., 2013; Tang et al., 2013). These updates and
OR phytoplankton OR potamoplankton OR phytoseston OR benthic modifications will improve the precision of assignments into distinct
algae OR periphyton OR benthic diatom OR diatom OR epilithic algae trait categories, but at the same time restrict the comparisons with
OR epilithic diatom OR epiphytic algae OR epiphytic diatom OR epi- other studies applying different assignment systems.
pelic algae OR epipelic diatom). (ii) Responses of different traits to environmental stressors are still
A total of 1907 articles were found based on the keywords defined, debated and some studies have concluded contradictory responses to a
and the annual numbers of publication demonstrated a linear increasing single stressor. For example, both positive (B-Béres et al., 2014; Lange
tendency (p < 0.001) from 1991 to 2016 (Fig. 1), although the pro- et al., 2016; Passy, 2007B-Béres et al., 2014) and negative (Stenger-
portion to the total numbers of scientific articles remained steady Kovács et al., 2013) relationships between motile taxa and nitrogen
(around 0.005%). concentrations have been found. Besides, most previous studies have
Then, we extracted the keywords following the procedures of Wang focused on single or a few traits and were conducted in mesocosms (Hill
et al. (2015) and top 30 keywords were visualized (Fig. 2). First, the et al., 2011; Lange et al., 2011; Piggott et al., 2012; Piggott et al., 2015)
yearly percentages of occurrence of each keyword was calculated as the or in the field (Berthon et al., 2011; Guo et al., 2016a; Passy, 2007;
yearly frequency divided by total frequency during a specified period of Soininen et al., 2016; Thomas et al., 2016). Very few have investigated
time, and then adjusted (divided) by the numbers of yearly total pub- the combined effects of multiple, simultaneously operating stressors on
lications to compensate for the general increase of total amount of a comprehensive set of algal traits (Lange et al., 2016; Piggott et al.,
publications. Second, Mann–Kendal (MK) trend test, by a self-composed 2012), although it is quite clear that multiple stressors often interact on
R code, was performed thereafter on each keyword in order to test the algal community (i.e., synergism or antagonism) (Guo et al., 2016a;
whether the temporal change (from 1991 to 2016) is significant (in- Hill et al., 2011; Lange et al., 2011; Lange et al., 2016; Piggott et al.,
creasing or decreasing). Third, we show 30 keywords with significant 2012).
increasing trend from 1991 to 2016 in Fig. 2. (iii) Trait distribution has been investigated at a comparatively
The temporal trends of the top 30 keywords showed an obvious small scale and their underlying environmental and historical drivers at
increasing trend from 1991 to 2016 (Fig. 2). The popular keywords larger scales are still poorly understood (Soininen et al., 2016). Fur-
used were algae terms (e.g., “diatom”, “phytoplankton”, “periphyton”, thermore, most of the previous studies have been conducted on a spatial
“algae”, “benthic algae”, “benthic diatom” “biofilm”, “cyanobacteria”, scale (Berthon et al., 2011; Dong et al., 2016; Passy, 2007, 2009;
“bacillariophyceae” etc.) in relation to abiotic factors (e.g., “nutrient”, Soininen et al., 2016) while studies based on a temporal scale are rare
“phosphorus”, “nitrogen”, “nutrient limit”, etc.) and biotic interaction (B-Béres et al., 2014; Stenger-Kovács et al., 2013B-Béres et al., 2014).
(i.e., “macroinvertebrate”) at different research locations (e.g.,
“stream”, “river”). Water problem related keywords (e.g., “eu- 4. Conceptual framework of algal traits in relation to resources
trophication”, “pollution”, “land use”) and its related fields (e.g., and disturbance
“monitoring”, “biomonitoring”, “indicator”, “bioindicator”, “biodi-
versity”, “diversity”, etc.) also showed an increasing trend. Im- Based on the existing knowledge, we here propose a number of
pressively, new keywords as “functional group” and “framework di- conceptual models to describe the responses of different algae traits to
rective” were also included in more studies. resource supply (mainly nutrient enrichment) and disturbance intensity
(e.g., flow regulation and grazing) (Fig. 3). Six response patterns (A-F)
3. Traits used in river microalgae biomonitoring are shown in Fig. 3. Most traits are co-regulated by disturbance in-
tensity and resource supply (e.g., Fig. 3A–D). For example large cell
In addition to species composition, ecologists have recently started size, high profile and functional diversity decrease with increasing
investigating trait composition since it reflects the functional responses disturbance frequency and decreasing resource supply. On the contrary
of communities to environmental gradients (McGill et al., 2006). In this small cell size and low profile species are expected to increase from
section, we summarize the latest proposed traits of river microalgae, high resource and low disturbance towards low resources and high

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Fig. 2. The yearly percentages of occurrence of top 30

keywords with significant increasing trend in the arti-
cles found from 1991 to 2016. The significance was
tested by Mann–Kendal (MK) trend test (see text for
details). ALGA = algae, EUTROPH = eutrophication,
DIVERS = diversity, POLLUT = pollution, DIOINDIC -
= bioindicator, INDIC = indicator, ECOLOG = -
ecology.

disturbance frequency. Some traits are supposed to respond to solely a the role of benthic and pelagic microalgae in nutrient removal in
single stressor (Fig. 3E, F) and may be suitable to disentangle the effects streams is therefore particularly important for managing stream eco-
of multiple stressors (e.g., nitrogen fixation to detect nutrient enrich- systems given the fact that anthropogenic point and diffuse sources
ment, attachment to substrate to detect hydrological disturbance). have increased nitrogen and phosphorus loads to river ecosystem
Nevertheless, the relationship between traits and the complex mixture globally (Guse et al., 2015; Hering et al., 2015; Seitzinger et al., 2005).
of stressors existing in freshwater habitats is still poorly documented Experiments, reviews and meta-analyses have shown that biological
and understood. We thus advocate that 1) further sampling of trait data traits, which can inform the contributions of species to ecosystem
to build up an updated database, 2) linkages between traits and en- function through differences in nutrient use and storage (Cadotte et al.,
vironmental stressors should be further studied, and 3) validations of 2011), are one of the best predictors of ecosystem function available
the hypotheses over larger spatial and temporal scale in the future (Griffin et al., 2009; Hooper et al., 2005; Petchey and Gaston, 2006).
studies, which may greatly benefit the trait-based environmental as- However, to our knowledge, the role of different functional traits in
sessment, biodiversity conservation and integrated water resource maintaining stream ecosystem function is still not well documented.
management. Therefore, the relationships between algal traits and ecosystem func-
tions (e.g., nutrient uptake, metabolism) and their underlying me-
5. Future research directions and applications chanisms along stream size gradients are greatly needed. In addition,
the majority of previous studies have focused only on algal traits
5.1. The role of microalgae in ecosystem functions lacking investigations of interaction with higher consumers (e.g., zoo-
plankton, macroinvertebrates and fish) and energy transfer in eco-
There is an increasing interest in ecology to understand linkages system functions. Thus, impacts of human mediated stressors on algal
between microalgae community composition and ecosystem functions traits and their consequent effect in stream food webs warrant further
(Reisinger et al., 2015; Reiss et al., 2009; Taylor et al., 2002), especially scientific attentions.
across the longitudinal gradient. Streams and rivers regulate resource
(such as nutrients, sediments, organic matters, etc.) transport from 5.2. Trait-based approach for biomonitoring under multiple stressors
terrestrial to marine ecosystems making them extremely important for
understanding and protecting downstream ecosystems (Alexander As mentioned above, freshwater resources are globally affected by
et al., 2008; Reisinger et al., 2015). Nutrients entering the streams are multiple stressors such as water abstraction, intensive farming land use
partially used by benthic and pelagic biota (e.g., assimilation, dissim- and climate change (Dudgeon et al., 2006; Hering et al., 2015;
ilation, sorption, etc.) with a portion being removed permanently via Vörösmarty et al., 2010), and the importance of assessing the potential
denitrification or deposited at the bottom, and the rest is transported to risks on stream ecosystems is becoming ever more urgent. The tradi-
downstream waters. Assimilatory uptake by biota in streams has proved tional taxonomic based indices, however, do not fully meet these urgent
to constitute the majority of nutrient removal from the water column demands and new approaches for biomonitoring purposes are required
(Mulholland et al., 2008), however, the ultimate fate of assimilated (see details above). Although the developments of the algal trait ap-
nutrients still remains unknown (Reisinger et al., 2015). Understanding proach in biomonitoring are promising, one issue arises: how to select

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Table 1
Algal indices, traits, their descriptions, and expected responses to different environmental stressors e.g., nutrient enrichment, light, flow regulation and grazing.

Traits Categories Abbreviations Expected responses to stressors

Resource Disturbance

1. Functional diversity (Bruno et al., 2016; Functional richness FRic Disturbances will reduce while high resource supply will increase functional
Cadotte et al., 2011; Schleuter et al., Functional evenness FEve diversity
2010) Functional divergence FDiv
Functional attribute FAD
diversity
Functional dispersion FDis
Functional redundancy FRed

2. Cell size (Berthon et al., 2011; Rimet and Nano (5–100 μm3) BioVol_c1 Smaller cells have higher nutrient uptake rates and growth rates that allow
Bouchez, 2012) Micro (100–300 μm3) BioVol_c2 greater resilience to disturbance making them advantage under nutrient-limiting
Meso (300–600 μm3) BioVol_c3 and high disturbance conditions; Larger cells show converse trend
Macro (600–1500 μm3) BioVol_c4
Very large (> 1500 μm3) BioVol_c5

3. Diatom guild (Passy, 2007; Rimet and Low profile LowPro Advantage at lower resources and high disturbance;
Bouchez, 2012) High profile HigPro Favor higher resources and low disturbance;
Motile taxa MotTax Advantage in resource gathering and low-flow depositional condition (MotTax
Planktonic taxa PlaTax and PlaTax)

4. Life form (Ferragut and Campos Bicudo, Colonial LifFor_col LifFor_fil has advantage in resource gathering but susceptible to high disturbance
2010) Filamentous LifFor_fil regimes
Flagellate LifFor_fla LifFor_uni has advantage in under depositional and high resource conditions
Unicellular LifFor_uni

5. Eco-morphology (B-Béres et al., 2016) Guild +Cell sizea – Combination between diatom guilds and cell size classes
Life form +Cell sizeb – Combination between life forms and cell size classes

6. Nitrogen fixation (Stancheva et al., 2013) Yes (1) or no (0) NitFix_1 N-fixer algae has advantage under nutrient-limiting condition but their relation
to disturbances varies

7. Attachment to substratum (Biggs et al., Non attached AttSub_non Algae with stronger attachment are more likely to retain under high disturbance
1998) Medium attached AttSub_med condition
Tightly attached AttSub_hig

8. Motility Motile attached Motile_att Actively motile algae have advantage in resource gathering and low-flow
(Round, 1984) Motile gliding Motile_gli depositional condition
Motile drift Motile_dri

9. Reproductive strategies (Biggs et al., Fission RepStr_fis RepStr_fis has advantage for dispersal and recolonization after disturbance
1998) Fragmentation RepStr_fra

10. Spore formation (Agrawal, 2009; Lange No spore formation SpoFor_non SpoFor_aki and SpoFor_oos.zyg have advantage in unfavourable conditions
et al., 2016) Zoospores SpoFor_zoo
Akinetes SpoFor_aki
Oospores and zygospores SpoFor_oos.zyg

11.Temperature traits (Thomas et al., 2016) Optimum temperature for Topt Topt Tmax Tmin decline with latitude increasing
growth
Maximum persistence Tmax
temperature
Minimum persistence Tmin
temperature

12. Algal quality (Guo et al., 2016a,b; Hill Saturated fatty acids SAFA Nutrient enrichment, low light and low temperature increases PUFA%, which in
et al., 2011) Monounsaturated fatty acids MUFA turn affect growth and PUFA composition in stream grazers
Polyunsaturated fatty acids FUFA
Highly unsaturated fatty HUFA
acid

Note: Resource acquisition includes nutrient enrichment (e.g., global land use change) and light (global warming); disturbance includes flow regulation and grazing. Seven traits (i.e., cell
size, life form, nitrogen fixation, attachment to substratum, motility, reproductive strategies and spore formation) were adapted from Lange et al. (2016). Although some traits are
overlapped, we retained them in order to gather all potential traits. Except for temperature traits, which are ecological traits, all these traits are biological traits (for definitions see
Supplementary Table S2).
a
A simple combination between 4 guilds and 5 cell size classes, resulting in 20 combinations (B-Béres et al., 2016).
b
A simple combination between 4 life forms and 5 cell size classes, resulting in 20 combinations.

robust traits that can disentangle the effects of multiple stressors in a 2006). Further field surveys and manipulative studies are needed to
catchment? address how algal traits vary across gradients of environmental vari-
One of the main objectives of the trait-based research approach is ables in streams and their consequent impacts on ecosystem functions.
relating traits to environmental factors (McGill et al., 2006). Although In fact, trade-offs and trait syndromes are two major challenges during
the relationships between environmental conditions (e.g., resources, the trait selection. A standard approach to diminish these two problems
disturbances, grazing, etc.) and many aspects of river microalgae is to relate traits to each other by regression (McGill et al., 2006). One
community structure and dynamics are well known, trait − environ- example was relating nutrient uptake rates and growth rates to cell size
ment linkages are still poorly documented. Robust (unlinked, un- (Biggs et al., 1998; Lange et al., 2016; Litchman and Klausmeier, 2008).
correlated) traits should supply a quick assessment of the stressor and Similarly, Menezes et al. (2010) also suggested a formal analysis ac-
provide insight into the environmental gradients in question (Poff et al., counting for phylogenetic relationships and potential confounding

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Fig. 3. Conceptual models showing six response patterns of different traits to resource supply and disturbance frequency. Traits categories are designated to different response patterns
and given below the diagrams. Some of these patterns have been validated (bold) and others remain to be tested (italic). The pattern E and F show the potential traits, which relate solely
to a single stressor and may be suitable for disentangling the effects of multiple stressors (e.g., nitrogen fixation to detect nutrient enrichment, attachment to substrate to detect
hydrological disturbance). Temperature traits, which are supposed to relate solely to temperature changes, and eco-morphology traits were not shown here. Abbreviations are as in
Table 1.

Fig. 4. A conceptual framework following a rigorous

step-by-step process (S1-S3). S1 is risk assessment of
different stressors and identifying robust traits of
microalgae; S2 is predicting the future global change
scenarios (including global land use and climate
change) and developing management strategies with
regard to global change and socio-economic devel-
opment; S3 is the implementation and evaluation of
distinct management scenarios in integrated model-
ling system. Definitions of different terms are shown
at Supplementary Table S2.

effects on trait measures, which will be used to provide information on potential applications of trait-based approaches is to improve our
future trait selection for biomonitoring purposes. ability to predict community composition, dynamics and ecosystem
functions under rapidly environmental changes or management sce-
narios. To develop adaptive strategies and manage water resources in a
5.3. Trait-based approach for water resource management in an
sustainable way, we suggest to develop an integrated interdisciplinary
interdisciplinary manner
approach with a sound understanding of potential risks, catchment
processes and feedback mechanisms of stream organisms. Models could
Apart from biomonitoring and risk assessment, one of the great

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