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Macroecology of macrophytes in the freshwater realm: patterns,

mechanisms and implications

Janne Alahuhta, Marja Lindholm, Lars Baastrup-Spohr, Jorge

Garcı́a-Girón, Maija Toivanen, Jani Heino, Kevin Murphy

PII: S0304-3770(20)30135-2
DOI: https://doi.org/10.1016/j.aquabot.2020.103325
Reference: AQBOT 103325

To appear in: Aquatic Botany

Received Date: 6 August 2020

Revised Date: 27 October 2020
Accepted Date: 3 November 2020

Please cite this article as: Alahuhta J, Lindholm M, Baastrup-Spohr L, Garcı́a-Girón J,

Toivanen M, Heino J, Murphy K, Macroecology of macrophytes in the freshwater realm:
patterns, mechanisms and implications, Aquatic Botany (2020),
doi: https://doi.org/10.1016/j.aquabot.2020.103325

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MACROECOLOGY OF MACROPHYTES IN THE FRESHWATER REALM: PATTERNS,
MECHANISMS AND IMPLICATIONS

Running title: Macroecology of aquatic macrophytes

Janne Alahuhta1*, Marja Lindholm1, Lars Baastrup-Spohr2, Jorge García-Girón1,3, Maija

Toivanen1, Jani Heino4, Kevin Murphy5

Janne Alahuhta ORCID: 0000-0001-5514-9361

Marja Lindholm ORCID: 0000-0002-0618-474X

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Lars Baastrup-Spohr ORCID: 0000-0001-8382-984X
Jorge García-Girón ORCID: 0000-0003-0512-3088

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Maija Toivanen ORCID: 0000-0002-7665-9018
Jani Heino ORCID: 0000-0003-1235-6613
Kevin Murphy ORCID: 0000-0003-2484-397X -p
1 Geography Research Unit, University of Oulu, P.O. Box. 3000, FI-90014 Oulu, Finland
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2 Freshwater Biological Laboratory, Department of Biology, University of Copenhagen,
Universitetsparken 4 2100 København Ø, Denmark.
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3 Ecology Unit, University of León, Campus de Vegazana S/N 24071, León, Spain
4 Finnish Environment Institute, Freshwater Centre, Paavo Havaksen Tie 3, FI-90570 Oulu,
Finland
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5 University of Glasgow, Glasgow G12 8QQ, Scotland, United Kingdom

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*Correspondence: Janne Alahuhta, Geography Research Unit, University of Oulu, P.O.

Box 3000, 90014 Oulu, Finland. Email: [email protected], GSM: +358294488061
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FUNDING INFORMATION: JA was partly supported by the Academy of Finland (grant

322652). MT acknowledges Maj & Tor Nessling Foundation.

HIGHLIGHTS

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  Few broad-scale patterns are well-studied for aquatic macrophytes.
 Local environmental predictors were important for freshwater plants at broad-
scales
 Several knowledge gaps on macroecology of freshwater plants were identified
 Lack of lotic studies and databases of species traits and phylogeny were found
 Additional macroecological investigations on freshwater plants are clearly
needed

ABSTRACT
Broad-scale studies of species distributions and diversity have contributed to the emergence
of general macroecological rules. These rules are typically founded on research using well-

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known terrestrial taxa as models and it is thus uncertain whether aquatic macrophytes follow
these macroecological rules. Our purpose is to draw together available information from

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broad-scale research on aquatic macrophytes growing in lakes, ponds, wetlands, rivers and
streams. We summarize how different macroecological rules fit the patterns shown by
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freshwater plants at various spatial scales. Finally, we outline future actions which should be
taken to advance macroecological research on freshwater plants. Our review suggested that
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some macroecological patterns are relatively well-evidenced for aquatic macrophytes,
whereas little information exists for others. We found, for example, that the species richness-
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latitude relationship follows a unimodal pattern, and species turnover prevails over species
nestedness, whereas higher nestedness-related richness differences are found in low beta
diversity regions. Contrary to terrestrial plants, climate or history seem not to be dominant
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determinants explaining these broad-scale patterns; instead local explanatory variables (e.g.,
water quality, such as alkalinity and nutrients, and hydromorphology) are often important for
freshwater plants. We identified several knowledge gaps related, for example, to a smaller
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number of studies in lotic habitats, compared with lentic habitats, lack of spatially-adequate
aquatic plant studies, deficiency of comprehensive species traits databases for aquatic
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macrophytes, and absence of a true phylogeny comprising most freshwater plant lineages. We
hope this review will encourage the undertaking of additional macroecological investigations
on freshwater plants across broad spatial and temporal scales.

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KEYWORDS: Aquatic plants, Biogeography, Freshwaters, Hydrophytes, Helophytes, Lakes,
Ponds, Streams, Rivers

1 INTRODUCTION

Macroecology focuses on the relationship between organisms and their environment at broad
spatial and temporal scales. It emphasizes the description and explanation of patterns in
abundance, distribution and diversity (Brown, 1995). In recent decades, there has been an
increasing number of studies using the macroecological approach (Smith et al., 2008). One of
the reasons for the growth in popularity is that this approach has shown its potential in

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combining distinct disciplines like ecology, biogeography, palaeontology and evolutionary
biology in characterizing broad-scale patterns in nature (Brown, 1995; Smith et al., 2008).

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Additionally, the regional, continental and global environmental problems, such as climate
change, have created a need for broad-scale studies on biodiversity (Kerr et al., 2007).

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Macroecology has several predictive approaches, and their validity has been evaluated in
various ecosystems using different biotas. They range, for example, from geographical
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diversity patterns (e.g., relationships of species diversity with latitude, altitude, and depth) to
species-area relationships and species turnover patterns (e.g., assemblage compositional
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changes along environmental and spatial gradients). In addition to studies using solely
taxonomic approaches, an increase in macroecological studies using trait-based and
phylogeny-based approaches has occurred in recent years (Heino et al., 2013; Pacifici et al.,
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2017). However, many of these investigations have been conducted in terrestrial ecosystems,
and much less is known about macroecological patterns in freshwater systems (Heino, 2011;
Heino et al., 2013). Broad-scale studies in inland waters have so far mainly focused on well-
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known and economically valued taxa, such as fish (e.g. Leroy et al., 2019) and
macroinvertebrates (e.g. Heino et al., 2018). As a result, our understanding of
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macroecological patterns in many freshwater taxa that have high ecological importance is
largely missing. One such group is aquatic macrophytes, which play a structurally and
functionally fundamental role in aquatic ecosystems (O’Hare et al., 2018).

Within the freshwater realm (e.g., Beger et al., 2009), aquatic macrophytes are usually
defined as “aquatic photosynthetic organisms, large enough to see with the naked eye, that
actively grow permanently or periodically submerged below, floating on, or up through the
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water surface” of inland freshwater or brackish waterbodies, including a diverse set of both
vascular (clubmosses, ferns and angiosperms) and non-vascular plants (bryophytes and some
macroalgae) (Chambers et al., 2008; Murphy et al., 2019). In this paper, we focus on the
vascular plants of freshwater environments, and hereafter use the term “aquatic
macrophyte(s)” solely in that context. Aquatic macrophytes have important functional and
structural roles in inland waters: they provide habitats and shelter to other organisms, increase
variation in the habitat structure of aquatic environments (Jeppesen et al., 1998), and are an
important food source for a wide variety of other organisms (Jupp and Spence, 1977;
Franceschini et al., 2020a,b). They also play an important role in the carbon and nutrient
cycles (Carpenter and Lodge, 1986), and influence a range of hydrological and sedimentation

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processes in aquatic environments (Sand-Jensen, 1998).

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The main aim of this review is to bring together current advances made in macroecological
research on freshwater macrophytes. Although individual overviews have been undertaken for
aquatic macrophytes (e.g., in relation to local environment and climate gradients: Lacoul and
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Freedman, 2006a; Bornette and Puijalon, 2011), no previous review has explicitly
summarized how general macroecological rules fit the patterns shown by aquatic macrophytes
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at various spatial and temporal scales. Here, we focus on broad-scale patterns related to
species taxonomy, functional traits and phylogenetic relationships, seen for aquatic
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macrophytes in freshwater systems ranging from lakes, reservoirs, ponds and wetlands to
rivers, streams, and artificially-constructed channels such as canals. Finally, we summarize
where we are now in freshwater plant macroecology and address potentially fruitful future
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avenues of research.

Owing to the scarcity of studies for aquatic macrophytes with regard to a number of different
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macroecological phenomena, it is impractical at this point in time to attempt a formal meta-

analysis of previous work on macroecological patterns in these plants. However, our review
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presents a first synthesis of the results to date of work on aquatic macrophytes in a broad-
scale context. Moreover, we are aware that different anthropogenic pressures modify aquatic
macrophyte distributions at local scales (e.g., introduction of alien plant species,
hydromorphological alterations of rivers, eutrophication and construction of dams) but they
are not per se drivers of (classical) general macroecological patterns of species distributions
and including their effects on broad-scale patterns of aquatic macrophytes is thus beyond the
scope of this review.
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2 GENERAL MACROECOLOGICAL PATTERNS AND AQUATIC MACROPHYTES
In this part of the review, we focus on three main general macroecological patterns as shown
by aquatic macrophytes (Fig. 1): geographical gradients in species diversity (2.1), species-
area relationship, (2.2) and community changes along environmental and spatial gradients
(2.3). These main broad-scale patterns are examined with regard to more detailed organism-
environment relationships following commonly used classifications (e.g. Gaston, 2000;
Heino, 2011).

2.1 Geographical gradients in freshwater plant diversity

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2.1.1 Latitudinal gradient in species diversity

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The latitudinal gradient in species diversity is typically considered to decrease relatively
linearly from the Equator towards the Poles (Gaston, 2000; Fig. 1a). Various contemporary
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explanations for this trend have been offered (e.g., less solar energy is available for high
latitude areas compared to the tropics), but the observed trend may also stem from historical
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factors (e.g., variation in glacial coverage during the late Quaternary) and climate variations
(Field et al., 2009). This pattern has primarily been evidenced using well-studied terrestrial
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taxa. However, considerable variation in the species diversity-latitude pattern has been found
for various aquatic and terrestrial taxa at scales ranging from regional to global (Heino, 2002;
Kerswell, 2006; Kindlemann et al., 2007).
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Fig. 1. Examples of different macroecological patterns based on species richness and

community changes for freshwater macrophytes.

To some extent, there have been conflicting results for the diversity-latitude relationship of
aquatic macrophytes at regional, continental and global scales. In a review focused explicitly
on shallow lakes, the authors concluded that no clear pattern exists for plant species richness
and latitude at regional or global scales (Meerhoff et al., 2012). Similarly, Kosten et al.

6
(2011) found a lack of latitudinal gradient in the species richness of submerged plants in
shallow lakes across South America. On the other hand, Chambers et al. (2008) concluded in
their global descriptive exercise that the highest number of vascular aquatic macrophytes is
found in the Neotropics (see also Murphy et al., 2019). Chappuis et al. (2012) found evidence
that aquatic vascular macrophyte richness peaked between 40°N and 50°N across Europe and
North Africa. There was a unimodal pattern, as species richness was lower at higher and
lower latitudes. Interestingly, the proportion of hydrophytes increased linearly from North
Africa towards the North Pole (Chappuis et al., 2012). A recent study, also indicating a
unimodal pattern in species richness-latitude relationship, suggested that the highest number
of aquatic macrophyte species is found around 50-55°N in Europe and ~40°N in North

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America (Alahuhta et al., 2020a). Crow (1993) found limited evidence to suggest that aquatic
macrophyte species richness was higher in temperate than in tropical regions. Perhaps most

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importantly, Murphy et al. (2019) showed in their global analysis that freshwater macrophyte
species richness is highest in sub-tropical to low tropical latitudes (20-30°). Despite different
study scales, the evidence clearly suggests that species richness of aquatic macrophytes does
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not linearly decrease from the Equator towards the Poles, but follows a unimodal latitudinal
pattern.
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For other biodiversity measures, the diversity-latitude relationship is more complicated. In a
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global analysis Alahuhta et al. (2017a) found a weak positive linear pattern between
lacustrine plant beta diversity (i.e., the spatial variation of species composition among sites
across space, Anderson et al., 2011) and latitude. This finding suggested that freshwater plant
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beta diversity increases towards the high latitudes. Latitudinal climatic effects had some effect
on beta diversity of lake plants across 16 regions worldwide, but their contributions were
overshadowed by altitude (Alahuhta et al., 2018). Using the same set of lake plants in 16
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regions, Garcia-Giron et al. (2020a) discovered that multiple beta diversity facets clearly
decreased with increasing latitude. Unfortunately, no similar studies exist for plants in lotic
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habitats.

The correlates which have been found to explain the species diversity-latitude relationship
stem not only from different spatial scales, but also from geographical variations in climate,
geology and soil, water body and drainage characteristics, and land use. It is challenging to
compare studies focused at different spatial scales (i.e., both resolution and extent), but the
species richness-latitude pattern is relatively similar regardless of spatial resolution. In
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general, important drivers (such as climate, land use and area of inland water) of plant
biodiversity are not equally distributed across the earth (Murphy et al., 2019; Alahuhta et al.,
2020a).

2.1.2 Altitude influences freshwater plant diversity

Species richness often decreases with increasing altitude (Gaston, 2000; Fig. 1b). Similar to
latitude, altitude mirrors different current and historical environmental factors, as well as
geographical, biotic and stochastic forces (Rahbek, 1995). At broad scales, the general trend
is that freshwater macrophyte species richness decreases with altitude when a strong

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elevational gradient exists (e.g. Lacoul and Freedman, 2006a; 2006b). Studies focusing purely
on altitudinal gradient effects on aquatic macrophytes are sparse and mainly done in

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mountainous areas, such as the Pyrenees (Chappuis et al., 2011; Pulido et al., 2014) or
Himalaya (Lacoul and Freedman, 2006b). Yet, altitude has been shown to be a strong
predictor of aquatic macrophyte diversity irrespective of geographical location (Tapia
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Grimaldo et al., 2016; Alahuhta et al., 2018). However, due to altitude’s potential as a
surrogate for many abiotic characteristics (e.g. climate or physico-chemistry), it is unlikely to
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be the only important driver of aquatic macrophyte richness unless the study area has a wide
elevational range (Jones et al., 2003; Chappuis et al., 2012; Fernández-Aláez et al., 2018).
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From a conservation viewpoint, studying altitudinal gradients is interesting especially in

terms of climate change, because there are large climatic differences over short geographical
distances. For example, endemic high-altitude species are particularly vulnerable to climate
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change (Chambers et al., 2008). In a wider context, altitude can be included in overall abiotic
diversity measures, such as geodiversity indices (Toivanen et al., 2019).
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Altitude has also been used to divide a given study area into spatial and ecological units with
similar natural characteristics (Baláži and Hrivnák, 2015) or to classify study sites into
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lowland and upland groups (Sun et al., 2019). The importance of different factors (e.g., land
use) in promoting the establishment or hindering the maintenance of freshwater plant species
and communities is likely to vary across elevational gradients (Sun et al., 2019). For example,
land use can be a more important predictor at lower altitudes, whereas natural variation in
nutrient concentrations or soil properties becomes more important at higher elevations
(Fernández-Aláez et al., 2018).

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Aquatic macrophytes have varying altitudinal ranges, with some covering a wide altitudinal
gradient (e.g., Callitriche palustris) and others being extremely restricted (e.g., Isoëtes
bolanderi) (Chambers et al., 2008; Fernández-Aláez et al., 2018). This makes determining
aquatic macrophyte diversity across altitudinal gradients a complex endeavour, and it could
be complemented by studies utilising information on species traits. For example, altitude has
been observed to affect leaf trait variation in terrestrial plants, whereas biotic drivers were
more important at low altitude and abiotic drivers at high altitude (Hulshof et al., 2013). At
broad spatial scales, it has been suggested that the general trend in the freshwater realm is that
abiotic geo-climatic factors (such as altitude and temperature) dominate over human impact
factors (Feld et al., 2009). However, at coarse spatial resolution (10 × 10° latitude x

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longitude), in a global analysis of plant diversity (Murphy et al., 2019), altitude was
overridden by the effect of latitude, land use and area of waterbodies, all of which are directly

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or indirectly related to climate (Dodds et al., 2019). Thus, even though altitude is widely used
as a surrogate for many abiotic characteristics, it is also important to be able to separate the
effects of different abiotic factors driving freshwater plant diversity.

2.2 Species-area relationship

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Species richness-area relationship (SAR) have deep roots in classical ecological theories
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(Arrhenius, 1921), predicting that species richness should increase with increasing island area
(Lawton, 1999; Fig. 1c). In the freshwater realm, evaluation of SAR is especially suitable in
lentic systems, which can be viewed as aquatic islands in an uninhabitable matrix of terrestrial
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landscapes (Hortal et al., 2014). Similar to lakes and ponds, rivers and streams can also be
viewed as “islands”. Aquatic ecologists early on grasped this topic, making SAR one of the
most investigated ecological rules in macroecological studies of aquatic macrophytes.
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An increasing number of freshwater plant species with increasing ecosystem size has been
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demonstrated in several studies (Møller and Rørdam, 1985; Rørslett, 1991; Vestergaard and
Sand-Jensen, 2000; Jones, Li and Maberly, 2003; Søndergaard, Jeppesen and Jensen, 2005;
Alahuhta et al., 2017b). The positive effect of patch size on species richness can be attributed
to the separate, but not mutually exclusive, effects of increased area per se and habitat
diversity (Kohn and Walsh, 1994; Ricklefs and Lovette, 1999). Commonly, habitat diversity
and area are strongly correlated because more habitats and microhabitats appear when area
size increases. These two variables can thus be hard to tease apart. So far, direct attempts to
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quantify the relative roles of habitat diversity and area for the species richness of aquatic
macrophytes have been scarce. Vestergaard and Sand-Jensen (2000) suggested that increased
water transparency, allowing for more vertical habitat variation with increasing depth, had
larger effects on species richness than lake area. Fernández-Aláez et al. (2020) also suggested
that species richness is higher in more heterogeneous ponds, caused by longer hydroperiod,
but a similar pattern may not hold in lakes. These findings thus suggest that habitat diversity
likely plays an important role for aquatic macrophyte species richness. The pure area effect
has been attributed to the lowered extinction rates caused by large local population sizes
(MacArthur and Wilson, 1967), but also to a positive effect of area on the immigration rate
known as ‘the target area effect’ (Lomolino, 1990). For lakes, this latter effect is supported by

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a larger initial colonization rate into large re-established lakes (Baastrup-Spohr et al., 2016)
compared to smaller ones (Søndergaard et al., 2018; Sø et al., 2020).

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The species richness of aquatic macrophytes does not always correlate strongly or at all with
water body size (Vestergaard and Sand-Jensen, 2000; Chappuis, Gacia and Ballesteros, 2014;
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Nolby et al., 2015). Such deviations from the expected relationship have generally been
attributed to overriding local environmental effects, variable degree of disturbance on water
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bodies and the difference between water body size and vegetated area within it. In lakes, the
entire bottom is rarely covered with vegetation, because light limits the distribution of plants
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in deeper sites and wave action limits plant growth in exposed sites (Jupp and Spence, 1977).
For instance, Vestergaard and Sand-Jensen (2000) found no significant effect of lake surface
area on species richness, but when using estimates of vegetated area, they found a strong
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relationship between area and species richness. This idea is supported by the findings of
Møller and Rørdam (1985), showing that species richness was more closely related to area of
the littoral zone than the entire surface area of ponds.
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Theoretically, larger lakes, irrespective of vegetated area, should receive more propagules
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compared to smaller ones due to the target area effect. This effect is not only caused by a
higher passive immigration rate to larger sites, but also by a more directed dispersal in the
form of zoochorous dispersal due to larger populations of dispersal vectors, such as waterfowl
(Brochet et al., 2009; Lovas-Kiss et al., 2019). Larger lakes also tend to have more inflows,
therefore increasing probability of immigrations via hydrochory (Jones et al., 2003). These
effects of area on immigration rate, and subsequently on species richness, have not been
investigated to date for aquatic macrophytes.
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The species richness-area relationship can also be modified or interfered with by natural
environmental conditions, such as bicarbonate concentration, shaping the pool of species
potentially able to inhabit individual locations (Vestergaard and Sand-Jensen, 2000; Iversen et
al., 2019). In areas of northwestern Europe, for example, where the species pool is larger in
bicarbonate-rich waters, a steeper relationship between species richness and area should be
expected for bicarbonate rich lakes compared with areas having more species-poor low-
bicarbonate systems. Likewise, an increase in the slope of the species area relationship should
be expected with increasing regional species richness (Qian et al., 2007). For aquatic
macrophytes, this implies steeper SARs at lower latitudes, particularly in the Neotropics,

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where regional species richness is highest (Murphy et al., 2019). In sum, there is evidence for
positive SARs for plants in lentic systems but details about their shape, causes and underlying

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mechanisms are still relatively unknown.

For river plants, much less is known about SARs, although patterns similar to those seen in
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lentic systems could be expected in lotic ecosystems. For other aquatic organisms, an effect of
stream area on species richness has been observed (e.g., Brönmark et al., 1984), but this
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pattern has been little-explored for river plants. However, when looking at single river
stretches, Szoszkiewicz et al. (2014) found a significant effect of river width and water depth
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on species richness of aquatic macrophytes. In temperate small and intermediate-sized

lowland streams, channel width also strongly affected plant species richness (Hachol et al.,
2019). Modelling river plants, Gillard et al. (2020) also found that river width was one of the
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main drivers of the distributions of different species. Yet, river plant diversity and
distributions are often related less to stream width and water depth than to current velocity
and flood-pulse factors, which further stem, for example, from a variable degree of
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precipitation (e.g., Chambers et al., 1991; Davidson et al., 2012; Varandas Martins et al.,
2013). However, all of these variables are usually both closely interrelated and associated
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strongly with stream order, which indicates the level of branching in a river system (e.g.,
Neiff et al, 2014; Morandeira and Kandus, 2015). For example, in a study of tropical rivers in
Zambia, Kennedy et al. (2015) found that stream order was a major correlate of macrophyte
richness and community composition. The general paucity of studies clearly illustrates that
the SAR remains relatively unexplored for river plants and even basic patterns need to be
better described, not to mention the underlying mechanisms.

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2.3 Community changes along environmental and spatial gradients

2.3.1 The effects of environmental and spatial gradients on species composition

A highly popular approach for examination of whether environmental factors and biotic
interactions or spatial processes (e.g., dispersal limitation and historical factors) structure
biological communities is to partition the variation in community composition into
environmental, spatial, and their joint effects (Fig. 1d). Spatial variables have often been
derived from spatial eigenfunction analysis (e.g., Moran’s eigenvector maps) or from simple
polynomials of geographical coordinates (Dray et al., 2012). Here, we discuss whether niche-

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based or spatial processes are the dominant forces driving freshwater plant assemblages at
different spatial scales.

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The variation partitioning approach to investigate the effects of environmental and spatial
factors on plant communities has been more popular for lakes than rivers. In lakes,
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environmental filtering is typically more important than spatial processes in explaining plant
community variation, especially in glacial-originated lakes. This has been shown, for
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example, for aquatic macrophyte communities in hundreds of US lakes (Capers et al., 2010;
Mikulyuk et al., 2011; Alahuhta and Heino, 2013), for Fennoscandian and Siberian lakes
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(Alahuhta et al., 2013; Alahuhta et al., 2020b), and for plant species richness variation in
European lakes (Alahuhta et al., 2013; Viana et al., 2014). However, joint effects of
environment and space often override pure environmental effects due to strong geographical
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structuring of key water quality and hydromorphology variables, or because spatially-explicit

environmental variables were missing from the studies (Mikulyuk et al., 2011; O’Hare et al.,
2012; Alahuhta et al., 2020b). In addition, spatial factors have often explained significant
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variation in lake macrophyte communities (Capers et al., 2010; Mikulyuk et al., 2011). For
example, De Bie et al. (2012) found that spatial factors dominated over environmental factors
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across Belgium farmland ponds.

So far, the most comprehensive assessments of environment vs. space were undertaken by
Alahuhta et al. (2018) and García-Girón et al. (2020a) using the same set of lake plants in 16
regions across the world. They reported that environmental factors were typically more
important than spatial effects in structuring plant community composition, but spatial
variables were also associated with lake plant community variation in some regions, and joint
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effects were often high. It seems that spatial processes play an essential role in structuring
freshwater plant communities especially in highly human-affected environments.
Furthermore, spatial processes have been a dominant force explaining variation in plant
communities in environmentally more unstable floodplain lakes (Padial et al., 2014; Alahuhta
et al., 2018), Mediterranean lakes (García-Girón et al., 2020a), and semi-lentic environments
(Hajek et al., 2011). These results suggest that environmental filtering is more important than
spatial processes for lake plants not influenced strongly by human activities, but spatial
processes may become increasingly important in more-fluctuating and human-influenced
lentic systems.

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For river plants, the importance of environmental filtering and spatial processes seems to be
more dependent on the studied region, making it challenging to draw uniform conclusions

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about these gradients. Tapia Grimaldo et al. (2016) found that spatial variables and spatially-
structured environmental variables contributed more than pure environment in explaining
plant species richness and community composition in calcareous rivers of the UK and
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Zambia. On the other hand, environmental variables solely or mainly structured community
composition of river plants in Finland (Alahuhta et al., 2015) and in Canada (Bourgeois et al.,
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2016). Variation in lowland river plant communities was similarly explained by only local
environment, whereas both the environment and space contributed to variation in headwater
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river plant communities in Denmark (Göthe et al., 2017). These few and rather contradictory
findings highlight the need for further research to examine the relative roles of environmental
filtering and spatial processes on river plant communities.
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Understanding of the influence of spatial scale in structuring freshwater plant communities is

also poor. The importance of spatial processes should increase with increasing scale (Leibold
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et al., 2004). There has been some indication that the importance of spatial processes
increases with increasing spatial scale for both lake (Alahuhta and Heino, 2013) and river
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(Tapia Grimaldo et al., 2016) plants. However, no other investigations exist in which multiple
spatial scales were studied simultaneously for freshwater plant communities in this context.

2.3.2 Distance decay

How community similarity decreases with spatial or environmental distance has been a
popular research question since the turn of the millennium (Nekola and White, 1999; Fig. 1e).
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The correlation of similarity against distance incorporates several ecological mechanisms,
thus providing a suitable perspective for investigating the spatial turnover across regions
(Soininen et al., 2007). In general, steeper slopes of distance decay suggest higher beta
diversity. When it comes to underlying mechanisms, this pattern suggests more restricted
dispersal and/or stronger relation to local environmental conditions. Thus, distance-decay
relationships may indicate how communities are structured by niche-based and neutral
processes because community similarity often decreases with increasing environmental and
spatial distance, respectively (Nekola and White, 1999; Soininen et al., 2007).

Only a few studies of distance decay of freshwater plant communities exist. For example, in

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tropical Australia, Warfe et al. (2012) discovered no evidence for dispersal limitation (i.e.,
spatial distance-decay as a proxy) in connected river sites, and little dispersal limitation was

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reported in disconnected sites along a 480 km length of river. Community similarity
decreased significantly with both geographical and environmental distance in four isolated
Chinese wetlands with different agricultural drainage ditch densities (Lu et al., 2009). This
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finding suggests that distance decay rate decreases with increasing disturbance intensity.
However, the lack of studies on distance decay of freshwater plant communities hinders the
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possibilities of further discussing the topic, let alone comparing any patterns found for aquatic
macrophytes with other freshwater taxa. Moreover, future studies should consider whether
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observed patterns of distance decay are not only a result of drier areas having greater
distances between aquatic habitats. These water bodies of drier areas are also often more
turbid and have greater salinity, further affecting aquatic macrophyte distributions.
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2.3.3 Partitioning of beta diversity into distinct components

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Beta diversity refers to the variation in species composition among communities across space
or time (Anderson et al., 2011), and it is fundamentally related to two processes (Legendre,
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2014): species turnover or replacement (i.e. one species replaces another with no change in
richness), and species richness difference (i.e. one community may include a larger number of
species than another) or nestedness (a special case of species richness difference: nestedness-
related species richness differences being due to species gain or loss). Mechanisms
responsible for species turnover/replacement may originate from environmental filtering,
competition and historical events (Anderson et al., 2011). In contrast, species richness
differences originate from species thinning or from other ecological processes (Baselga, 2010;
14
Legendre, 2014), such as physical barriers or human disturbance. Beta diversity has been
reported to decrease with latitude and increase with elevation and biome area (Anderson et
al., 2011; Soininen et al., 2018). However, increasing evidence suggests that patterns in beta
diversity depend on the studied ecosystem, organisms, geographical location and spatial
extent (Legendre, 2014; Soininen et al., 2018).

For freshwater plants, new insights into their beta diversity patterns have accumulated from
various regions and scales. Based on these studies, it is evident that freshwater plant
communities are primarily structured by species turnover (Alahuhta et al., 2017a; Murphy et
al., 2020; Fig. 1e). Regarding temporal beta diversity patterns, Boschilia et al. (2016) studied

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changes in plant communities in a Brazilian reservoir and found high values of beta diversity
with the prevalence of species turnover over the course of a decade. For the spatial beta

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diversity patterns, species turnover prevailed for lake plants across five regions in Europe
(Viana et al., 2016) and between permanent and temporal agricultural ponds (Fernández-
Aláez et al., 2020). Murphy et al. (2020) found evidence for the existence of a latitudinal beta
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diversity gradient, which was only poorly explained by nestedness for the global distribution
of range-sizes of 1083 freshwater plant species, suggesting that species turnover made a
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higher contribution to beta diversity. In a global analysis of freshwater plant beta diversity
across 21 regions, Alahuhta et al. (2017a) showed that species turnover overrode nestedness
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in shaping aquatic macrophyte communities. This was most evident in regions with high
overall beta diversity, whereas nestedness was highest, but still lower than species turnover,
in regions with low beta diversity.
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3 FUNCTIONAL AND PHYLOGENETIC PERSPECTIVES

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The widespread appreciation that the interaction between an organism and its environment is
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primarily determined by biological traits, rather than taxonomic position (McGill et al.,
2006), has led to a rapid growth of the applications of the functional dimension in
macroecology. Consequently, macroecological research has recently started to improve
understanding of the mechanistic basis behind broad-scale patterns in biodiversity through
focusing on the relationships between species traits and their distributions (Heino et al.,
2013). In this regard, species traits have shown their advantages in studies of several
biological groups and different environments, for example, in climate change (e.g., Pacifici et
15
al., 2017), ecosystem functioning (Petchey and Gaston, 2006), and range shift contexts
(Estrada et al., 2016).

Whereas the traditional taxonomic approach requires only information on the geographical
distributions of species, functional analyses require an additional suite of trait measurements
for each species. Traditionally, studies with aquatic macrophytes have dealt with this
functional dimension of biodiversity using different types of categorical divisions derived
mainly from the growth form and the life form concepts (Vermaat et al., 2000; Willby et al.,
2000). However, some studies have utilized a broader range of morphological and
physiological traits to characterize aquatic macrophyte species and communities in functional

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terms (Hills et al., 1994; Hills and Murphy, 1996; Garbey et al., 2004). Of the categorical
divisions, the functional groups based on life form have probably been the most used (e.g.,

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Chappuis et al., 2012; Mormul et al., 2015; García-Girón et al., 2018). More recently, species
traits have been utilized in broad-scale studies without categorical divisions of trait
composition, but instead using continuous or experimentally quantified values (e.g., Göthe et
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al., 2017; Iversen et al., 2019). Over the last few decades, research has focused on several
morphological, physiological and life-history traits that are related to plant morphology and
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hydrology, perennation (i.e., a species growing for a single or several years), use of carbon,
photosynthetic efficiency, and dispersal vectors (e.g., De Wilde et al., 2014; Fu et al., 2014;
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García-Girón et al., 2019a,b, 2020a,b; Iversen et al., 2019; Lindholm et al., 2020a,b). This
shift of focus has given new insights into patterns and processes of species distributions and
community assembly that otherwise would be missed, or even misrepresented, from the
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standard taxonomic viewpoint. For example, Lukács et al. (2017) showed the importance of
traits related to competitive ability (e.g., growth rate and leaf economics spectrum) during
aquatic macrophyte invasions in Europe, while García-Girón et al. (2019b) showed that a
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trait-based approach could help explain the abundance structure of Mediterranean pond plant
metacommunities, using dispersal vectors (i.e., wind- vs water-dispersed species) and trait-
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environment relationships at different spatial scales. At global scale, Iversen et al. (2019)
showed that functional composition (bicarbonate users vs CO2 users) of plant communities
was structured by environmental bicarbonate concentrations. Despite these rather few new
studies, the general shortage of studies at broad scales still hinders our ability to test and
validate macroecological hypotheses, and consequently also affects our ability to answer
questions about how the trait composition of aquatic macrophyte communities varies along
geographical gradients and environmental gradients (see also Dalla Vecchia et al., 2020). For
16
the most part, this is due to the fact that very few studies (but see García-Girón et al., 2020a)
have yet used the same analytical methods to examine community variation based on multiple
traits in various geographical regions at global scale.

Lack of comprehensive species trait information on aquatic macrophytes has also created
further challenges (see Supporting Information for more discussion). In the absence of
species-specific multi-trait data, plant researchers have tried to test the validity of predicting
traits from congeneric or confamilial species, as has been recently done at regional (García-
Girón et al., 2019a) and continental scales (Alahuhta et al., 2017a; García-Girón et al.,
2020a). These evaluations are based on assessing the `phylogenetic niche conservatism´ (e.g.,

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Blomberg et al., 2003) of the traits under study. This approach aims to determine whether
similarity in the biological or ecological characteristics of the species is influenced by the

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effect of ancestor-descendant relationships (Roquet et al., 2013). For the moment, their
outcomes have been somewhat contradictory, finding evidence of either some level of species
niche conservatism (Alahuhta et al., 2017b) but also often low phylogenetic signal in traits
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(García-Girón et al., 2019a; García-Girón et al., 2020a). This hinders our ability to establish a
general picture of whether traits are conserved or not in aquatic macrophytes, and to compare
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patterns found with other organisms. A likely reason is that the rather phylogenetically-distant
nature of aquatic macrophytes causes difficulties for phylogenetic studies (Hu et al., 2017), as
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these plants are evolutionarily highly dispersed across the Tree of Life (Du et al., 2016), with
at least 50 independent origins from their closest terrestrial relatives (Cook, 1990).
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To further understand how evolutionary history shapes the geographical distribution of

aquatic macrophytes, we need accurate information on the phylogenetic relationships between
plant species. To date, this has been performed using several methods of varying complexity
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and reliability, but the implementation of this new era of `ecophylogenetics´ (Mouquet et al.,
2012) to the macroecology of aquatic macrophytes is still facing a number of methodological
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challenges (Hu et al., 2017). As a first step, some studies have used taxonomic classification
as a surrogate for evolutionary relatedness, as implemented recently by Alahuhta et al.
(2017c) and García-Girón et al. (2019c), in order to develop proxies for aquatic macrophyte
phylogenetic diversity. However, such an approach is rather unrealistic since it assumes that
topological relationships (i.e., intrageneric relatedness) are equal for all genera (Roquet et al.,
2013). In other published works, phylogenetic inferences have been done by incorporating the
topological information from published phylogenies. For example, De Wilde et al. (2014)
17
used the released compilation of angiosperm phylogeny based on Angiosperm Phylogeny
Group III (2009) to determine whether phylogenetic position at family level controls the
effects of dewatering on aquatic macrophyte performance. Although appealing, such an
approach provides no estimates of branch lengths, i.e., quantitative evolutionary relationships
of species.

The super matrix approach (Roquet et al., 2013) has been recently proposed as an alternative
method to simultaneously analyze large DNA sequence datasets from either nuclear,
ribosomal or plastid regions, and thus estimate meaningful branch length values (see Hu et
al., 2017 for instructions). However, when it comes to aquatic macrophytes, this super matrix

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approach has only been used in systematic studies (e.g., Cai et al., 2010 for Ranunculaceae;
Chen et al., 2012 for Alismataceae; and Bernardini and Lucchese 2018 for Hydrocharitaceae),

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meaning that no accurate species-level phylogenetic tree exists for the diverse group of
freshwater plants, thus imposing significant constraints upon current macroecological
research. This is unfortunate considering the constant increase of available molecular data in
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GenBank, the growing number of algorithms for alignment, optimization and depuration (e.g.,
Tamura et al., 2011), and the recent improvements in freely available software (e.g., MEGA;
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GARLI; RAxML) able to handle extremely large data sets within a moderate amount of time.
Recently, García-Girón et al. (2020a) advanced our understanding of the phylogenetic
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relatedness of freshwater plants by building the very first genus-level DNA-based phylogeny
(i.e. the maximum likelihood on sequences from two chloroplast DNA regions) comprising
most plant lineages (from Lycopodiopsida to Eudicotyledoneae). However, more accurate,
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fully resolved phylogenies are still needed to reduce possible artefacts due to data patchiness
and improve historical inferences from current macroecological patterns of aquatic
macrophytes.
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Globally, our review reveals that the basic functional and evolutionary biology of freshwater
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plants has been mostly ignored, highlighting the need for greater efforts to collect multi-trait
and phylogenetic data and to make them available in a standard format using existing portals
(e.g., TRY and GenBank) and digital repositories (e.g., Dryad and Figshare).

4 WHERE TO GO FROM HERE?

18
Freshwater macrophyte research has lagged behind that for many other terrestrial, marine and
freshwater groups with regard to investigation of different macroecological patterns. This
derives from several reasons related to research community size, field surveys and research
perspectives (Table 1). (i) The number of scientists working with aquatic macrophytes is
small compared with terrestrial plants and most other freshwater groups, such as fish and
macroinvertebrates. This means that fewer aquatic macrophyte ecologists are interested in
macroecological research questions. (ii) Previous freshwater plant studies have often been
conducted by botanists with completely different study aims compared to those of ecologists
and biogeographers. The focus in many of these previous botany-related plant studies has
been on local patterns and processes using data at fine scales and with a limited number of

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surveyed water bodies. (iii) A notable proportion of freshwater plant studies has focused on
specific genera and/or invasive species. As a result, community composition of aquatic

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macrophytes has not always been surveyed, hindering our possibilities to investigate aquatic
vegetation in a macroecological context. Fortunately, there has been an awakening in
macroecological freshwater plant studies during recent years due to the improved quality and
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quantity of available data (both field and atlas data), GIS-programs and computer efficiency.
However, we still need more aquatic macrophyte surveys to be carried out in geographically
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less-studied regions (e.g., Africa, Asia, Russia, North America [for river plants], South
America and Oceania, in addition to the highest or lowest latitudes) in order to advance
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macroecological research on freshwater plants.

In addition to these field survey and botanical research perspectives, our review revealed that
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most macroecological studies on plants have been done in lentic ecosystems (e.g., Alahuhta et
al., 2018). Nevertheless, there are a few examples of moderately broad-scale river plant
studies in this context, for both tropical (e.g., Kennedy et al., 2015) and temperate areas (e.g.,
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Janauer et al., 2018). Recent studies suggest that lake and river plants may not respond
similarly to the same ecological gradients. For example, alkalinity was found to be a highly
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important driver of plant distributions in lakes but less so in rivers (Iversen et al., 2019), and
even the distributions of the same plant species can be explained by different environmental
gradients in lakes and rivers (Gillard et al., 2020). Recent compilation of a global lake plant
dataset has permitted an increase in macroecological studies on lentic plants, and we clearly
need a similar worldwide database on river plants. This problem is more challenging to
overcome with atlas data, where lentic and lotic ecosystems are rarely distinguished. More
efforts to build a grid cell-based freshwater plant database, distinguishing also different water
19
body types, should be made. Current biodiversity databases (e.g., GBIF) can form the basis
for this work and further promote finer-scale global databases of freshwater plants.

Biases in studied macroecological questions were clear based on our overview. For example,
latitudinal, altitudinal and area-related patterns in species diversity were relatively well
studied, whereas only a few investigations had examined distance-decay relationships. The
better scientific coverage of these well-investigated patterns partly stems from a longer
tradition of studying such ecological phenomena. More research is required not only for less-
studied macroecological phenomena but also for better-recognized patterns in order to
improve our knowledge of the causal mechanisms underlying these patterns in freshwater

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plants.

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Temporal studies in macroecological context are also mostly lacking for aquatic macrophytes
(but see Sand-Jensen et al., 2000; Baastrup-Spohr et al., 2013). This shortage is mostly due to
unavailable historical data. So far most temporal exercises have focused on single water
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bodies (e.g., Varandas Martins et al., 2013; Ceschin et al., 2009, 2010; Sand-Jensen et al.,
2017), or are based on palaeolimnological approaches (e.g., Dieffenbacher-Krall and
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Jacobson, 2001; Sawada et al., 2003) but spatially-explicit temporal data founded on
historical field surveys is needed for broad-scale studies (Lindholm et al., 2020a,b and
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references therein). Temporal macroecological investigations are especially important

nowadays because of threats posed by global change to highly vulnerable and biodiversity-
rich freshwater ecosystems (Heino et al., 2020).
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Biotic interactions in individual water bodies have been intensively investigated at small
spatial scales for decades. However, there is very little evidence about how biotic interactions
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affect communities among freshwater systems. For example, a high proportion of unexplained
variation is often detected when variation partitioning analysis has been applied to freshwater
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plant communities (e.g. Alahuhta & Heino, 2013; Sun et al., 2019). This may be due to the
lack of inquiry for biotic interactions in the study designs. In fact, García-Girón et al. (2020c)
recently discovered that potential biotic interactions among pond plant species clearly
overrode the environmental effects in explaining variation in Mediterranean pond
communities. This finding may be very important considering not only the high ecological
relevance of plants in the freshwater realm (O’Hare et al., 2018; Law et al., 2019), but also
the degradative nature of certain invasive aquatic macrophyte species (Hussner, 2012;
20
Ceschin et al., 2020). However, further evaluations in different regions and different types of
inland ecosystems are certainly needed.

Finally, future research should consider the integration of functional traits with phylogenetic
analyses for the extraction of well-curated aquatic macrophyte data among different
geographical entities, including drainage basins, ecoregions and biogeographical realms. To
achieve this, freshwater plant researchers will need to combine large trait databases, species-
level field and laboratory measurements, regional floras and botanical checklists with deep
sequencing and comparative phylogenetics. By doing so, we should be able to build high-
quality functional and phylogenetic datasets for hypothesis testing, thereby permitting the

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validation and extension of macroecological patterns and understanding of underlying
processes. We hope that our review will stimulate more macroecological research on

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freshwater plant across different geographical areas, scales and ecosystems.

Table 1. Summary of known research gaps and suggestions for possible future research
directions for macroecology of freshwater plants.
Research gap
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Suggestion for future study direction
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Lack of spatially adequate First, combining and harmonization of existing surveys (e.g.,
freshwater plant surveys collected for ecological quality assessments and/or existing
in different databases). Second, more complementary
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surveys with macroecological study focus should be carried

out.
Geographical biases in Europe and North America (the latter continent only for
freshwater plant studies lakes though) are intensively surveyed. More studies are
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needed from, for example, Africa, different parts of Asia,

Central and South America as well as Oceania.
Investigations from both highest and lowest latitudes are also
required.
Scarcity of river plant studies Lentic ecosystems are predominantly represented in
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macroecological plant studies and more information about

how river plants respond to ecological gradients at broad
scales is required. In addition, species growing in lentic and
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lotic systems may respond differently to macroecological

gradients, highlighting the need for further river studies.
Bias in certain Certain phenomena are relatively well-studied (e.g., species
macroecological phenomena diversity-latitude, diversity-altitude and diversity-area
relationships, and environmental vs. spatial effects on
community composition), but our knowledge is deficient for
many others (e.g., patterns of abundance, functional
diversity and phylogenetic diversity). More research is
needed for understanding these less well-studied
macroecological phenomena.

21
Lack of temporal studies with Majority of temporal investigations on aquatic macrophytes
macroecological perspectives have focused on single (or few) water bodies but
macroecological gradients cannot be studied with such a
small number of lakes or rivers. More comprehensive
temporal data is needed to better understand temporal
macroecological patterns in aquatic macrophytes.
Omission of biotic Information on biotic interactions between pairs of
interactions in a spatial freshwater plant species at among-water bodies scales is
context missing. A high amount of unexplained variation in
community composition analyses can originate from species
interactions, but this needs to be further addressed.
Suitable species traits for Terrestrial plants dominate in many existing species trait
macroecological studies databases, and the information therein is not often
ecologically relevant for freshwater plants. Thus, new
species trait measurements are needed from different

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regions. In addition, the high level of intraspecific variation
in species traits should be accounted for in these
measurements.

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Shortage of true phylogeny Efforts to construct true and comprehensive aquatic
macrophyte phylogeny need to be undertaken.

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Declaration of interests
The authors declare that they have no known competing financial interests or personal
relationships that could have appeared to influence the work reported in this paper.
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Declaration of interests

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☒ The authors declare that they have no known competing financial interests or personal
relationships that could have appeared to influence the work reported in this paper.
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