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Exotic species invasions undermine regional functional diversity of freshwater fish

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Exotic species invasions undermine regional functional diversity of freshwater fish

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Exotic species invasions often result in native biodiversity loss, i.e. a lower taxonomic diversity, but current knowledge on invasions effects underlined a potential increase of functional diversity. We thus explored the connections between functional diversity and exotic species invasions, while accounting for their environmental drivers, using a fine-resolution large dataset of Mediterranean stream fish communities. While functional diversity of native and exotic species responded similarly to most environmental constraints, we found significant differences in the effects of altitude and in the different ranking of constraints. These differences suggest that invasion dynamics could play a role in overriding some major environmental drivers. Our results also showed that a lower diversity of ecological traits in communities (about half of less disturbed communities) corresponded to a high invasion degree, and that the exotic component of communities had typically less diverse ecological traits than the native one, even when accounting for stream order and species richness. Overall, our results suggest that possible outcomes of severe exotic species invasions could include a reduced functional diversity of invaded communities, but analyzing data with finer ecological, temporal and spatial resolutions would be needed to pinpoint the causal relationship between invasions and functional diversity.
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Exotic species invasions undermine
regional functional diversity of
freshwater sh
Marco Milardi
1,3, Anna Gavioli1*, Janne Soininen2 & Giuseppe Castaldelli1
Exotic species invasions often result in native biodiversity loss, i.e. a lower taxonomic diversity, but
current knowledge on invasions eects underlined a potential increase of functional diversity. We thus
explored the connections between functional diversity and exotic species invasions, while accounting
for their environmental drivers, using a ne-resolution large dataset of Mediterranean stream sh
communities. While functional diversity of native and exotic species responded similarly to most
environmental constraints, we found signicant dierences in the eects of altitude and in the dierent
ranking of constraints. These dierences suggest that invasion dynamics could play a role in overriding
some major environmental drivers. Our results also showed that a lower diversity of ecological traits in
communities (about half of less disturbed communities) corresponded to a high invasion degree, and
that the exotic component of communities had typically less diverse ecological traits than the native
one, even when accounting for stream order and species richness. Overall, our results suggest that
possible outcomes of severe exotic species invasions could include a reduced functional diversity of
invaded communities, but analyzing data with ner ecological, temporal and spatial resolutions would
be needed to pinpoint the causal relationship between invasions and functional diversity.
Biodiversity is a key element of ecosystem functioning and characterizes its resilience to dierent pressures1,
but suers from a general worldwide decline2. Among the causes of global biodiversity loss, exotic invasions are
oen placed at the top3,4, but mechanisms and impact of species invasions might vary in dierent ecosystems,
taxa and spatial scales. While a lot of attention has been devoted to the consequences of exotic invasions on spe-
cies taxonomic diversity at dierent geographical scales5, hardly any regional extinctions have been recorded in
aquatic taxa such as sh (with some notable exceptions, e.g.6,7), but extirpation, species substitution and decrease
of native biomass have all been reported as a local result of exotic invasions811. e detection of exotic invasions‘
eects could thus depend on the spatial and biological detail level of the data used, so that some eects could be
potentially overlooked or misinterpreted if the data is insuciently detailed.
For example, sh introductions could enrich functional diversity at the regional scale, because, from a pres-
ence/absence perspective, they can increase regional species richness and consequently increase the number of
functional traits present in that area12. Functional diversity describes the distinctive assemblage of morphological,
biochemical, physiological, structural, phenological or behavioral traits that characterizes living communities,
and that is highly coupled to environmental conditions13. Ecofunctional diversity is a subset of functional diver-
sity, focusing on the combination of ecological traits in communities14, but is referred to simply as functional
diversity hereaer, because it is a more common term. Ecological traits in a community are usually selected by
factors such as habitat diversity, geography, land use or water chemistry15, but established exotic species are oen
generalists16 and invasion dynamics (e.g. human-aided dispersion) could partly override habitat selectivity.
Competition with introduced exotic species could act as an additional lter for native species, sometimes
stronger than environmental gradients11. Furthermore, widespread and severe biological invasions could result in
the taxonomic homogenization of invaded communities1719, with few exotic species dominating heavily invaded
areas, a pattern which has been detected at least in plants20. Most likely, taxonomic homogenization would also
aect functional diversity of invaded areas, as it leads to communities with a lower number of species and a lower
variety of traits, but it remains unclear whether this is a signicant element of exotic invasions.
1University of Ferrara, Department of Life Sciences and Biotechnology, via Luigi Borsari 46, 44121, Ferrara, Italy.
2University of Helsinki, Department of Geosciences and Geography, PO Box 64, 34 – 38 Bowen Street, FI-00014,
Helsinki, Finland. 3Present Address: Fisheries New Zealand - Tini a Tangaroa, Ministry for Primary Industries - Manatū
Ahu Matua, 34 – 38 Bowen Street, Wellington, New Zealand. *email: gvlnna@unife.it
OPEN
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Exotic species are a main cause of the loss of biological diversity in the Mediterranean region21,22, particu-
larly in freshwater habitats23. e functional structure of Mediterranean freshwater sh communities is relatively
uncharted, and an ecological trait characterization of native and exotic sh species has only been recently dened
for some areas2426. is nally enables further research on the linkages between biological invasions, functional
diversity and the environment.
We used a spatially-broad yet very detailed dataset, comprising several river basins in northern Italy at a
late invasion stage (i.e. >30 years aer major invasions), as a test case to explore the outcomes of exotic species
invasion in freshwater sh communities and to investigate the relationships between environmental factors, inva-
sions and functional diversity. We used boosted regression tree (BRT) analysis to test the hypothesis (H1) that
functional diversity of exotic and native species would respond dierently to environmental variables, as invasion
dynamics could temporarily override habitat selectivity. We then used spatial and regression analyses to test
whether (H2) the overall functional diversity of communities would be negatively or positively aected by dier-
ent degrees of exotic invasions. Our results would ultimately reveal the connections between functional diversity
and exotic species invasions, on the background of habitat ltering.
Results
BRT analysis showed that environmental variables typically had dierent magnitude and direction of relative
inuence on exotic and native species functional diversity (Fig.1). While altitude was one of the most signicant
variables negatively aecting native species functional diversity (and positively that of exotic ones), high temper-
ature, low salinity or high turbidity were clearly linked to higher exotic species functional diversity (Fig.1). Forest
cover was associated to lower functional diversity of both native and exotic species, while brackish water was
associated to a higher functional diversity of native species (Fig.1).
Several sites showed minimum levels of exotic invasion (invasion degree 10% for 140 sites, 41.9% of the
total) and most of these sites hosted completely native communities (126 sites, 37.6% of the total). However, the
majority of sites were invaded (209 sites, 62.4% of the total) and the invasion degree was relatively severe in most
of them (invasion degree 50% for 134 sites, 40% of the total), including some sites where the community exclu-
sively comprised exotic species (10 sites, 3% of the total). Our spatial analysis underlined that the most severely
invaded sites were mostly located on the lower stretches of most watercourses examined (Fig.2a). Moreover, in
invaded communities, there was a clear spatial overlap between the most invaded areas and the areas where func-
tional diversity was lowest (Fig.2b).
In invaded sites, functional diversity was also clearly negatively linked to the invasion degree (Fig.3). At the
highest invasion degrees, a decrease of nearly 50% of functional diversity, compared with less disturbed commu-
nities, could be observed.
Low-order streams (in the uplands) showed lower values of species richness and functional diversity than
high-order streams (in the lowlands) (Fig.4a,b). Species richness was low in upland streams, but these habitats
showed a larger variation in functional diversity than lowland streams. Canals, in the lowlands, had lower rich-
ness and functional diversity values than natural rivers in the same area (Fig.4a,b). e dierence between native
and exotic functional diversity was consistently lower than what suggested by their relative richness (Fig.4c,d),
with native species usually showing higher values of functional diversity relative to their richness. Exotic species
Figure 1. Boosted Regression Tree (BRT) summary showing the relative inuence of geographical variables
(in orange), water physico-chemical variables (in blue) and land use (in green) on freshwater sh functional
diversity (calculated through the functional dispersion, FDis metric, applied to the ecological traits of species)
for native (le panel) and exotic (right panel) species. e variable abbreviations stand for: Long – longitude,
Lat – latitude, Alt – altitude, NH4+ – ammonia, BOD – biological oxygen demand, TSS – total suspended solids,
T – water temperature, NO3 – nitrate nitrogen, COD – chemical oxygen demand, EC – electrical conductivity,
TP – total phosphorus, Agric – agricultural, Other nat – other natural area, Freshw – freshwater, Forest – forest,
Urban – urban and Brackishw – brackish water.
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showed lower functional diversity values than native species in all natural rivers, which was most evident in
higher order streams, but the pattern was reversed in canals (Fig.4d).
Both native and exotic functional diversity in communities were linked to species richness and tended to sat-
urate with growing richness (Fig.5), albeit with dierent rates and asymptotes. However, accounting for species
richness, community functional diversity for exotic species was generally lower than that of native ones (Fig.5).
Discussion
Functional diversity of native and exotic species, as expressed by the FDis metric, responded similarly to most
environmental constraints. However, conrming our rst hypothesis (H1), we found signicant dierences in
the eects of altitude (positive eect for native and negative eect for exotic species) and in the dierent ranking
of constraints. is suggests that invasion dynamics could play a role in overriding some major environmental
drivers of functional diversity. Our results also showed that a high invasion degree corresponded to a lower
functional diversity of sh communities, conrming our second hypothesis (H2). Exotic species typically had a
lower functional diversity than native species, even when accounting for stream order and species richness, which
Figure 2. (a) Invasion degree in freshwater sh communities of northern Italy, and (b) spatial distribution
of functional diversity (calculated through the FDis metric applied to the ecological traits of species) in the
invaded sites, obtained by linear kriging. Dots represent the sampling sites used in each analysis. Colors
represent the severity of invasion (% of exotic species abundance in a community) and the functional diversity
of communities, respectively.
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could be at the root of the observed lower functional diversity of highly invaded communities. Our results thus
suggest that possible outcomes of severe exotic species invasions could include a reduced functional diversity
of freshwater sh communities, and that analyzing data with ner ecological and spatial resolutions could help
further investigate these eects.
e dierent ranking of environmental drivers for exotic and native species might indicate that there are some
dierences in the relevance of factors shaping their respective functional diversity patterns. For example, our
BRT analysis highlighted the role of native marine species entering brackish habitats in contributing to the sh
Figure 3. Italian freshwater sh communities’ functional diversity (calculated through the FDis metric applied
to the ecological traits of species), along the invasion gradient. Circles represent values of overall functional
diversity for each invaded site, while the line represents the best-tting non-linear regression line (see
Supplementary Table3 for best t regression evaluation).
Figure 4. (a) Distribution of species richness and (b) functional diversity (calculated through the FDis metric
applied to the ecological traits of species) by stream order classes, calculated on the whole sh community. e
same patterns for species richness (c) and functional diversity (d) are also represented for exotic and native sh
species separately. e horizontal bars in the boxes represent the median, the boxes’ hinges represent the rst
and third quartile, and the notches represent the 95% condence interval of the median.
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functional diversity in these areas. Our analysis results also suggested that geographical factors like altitude could
play a major role to control invasion dynamics, as altitude appeared to be the main factor of divergence for native
and exotic functional diversity. In addition to temperature, altitude is linked to a number of other factors, includ-
ing habitat fragmentation but also habitat quality. Mountain streams typically have lower habitat complexity and
resources availability but higher habitat quality than rivers in the lowlands27,28. However, upland streams can be
more fragmented due to the presence of dispersal barriers29,30.
e high degree of invasion in the lower stretches of all basins also implies that lowland areas constitute a mas-
sive reservoir of exotic species, which could exert a signicant propagule pressure towards higher altitudes31,32.
is pressure is held in check, at least in some cases, by impassable barriers to migration and by unfavorable
ecological conditions in upstream areas33. Habitat fragmentation and other consequences of water abstraction
for human use are a worldwide issue oen deeply interlinked with exotic species invasions34,35, freshwater com-
munities functional diversity36, and homogenization processes37. Unfortunately, habitat connectivity restoration
near heavily invaded areas may not be sucient to restore native biodiversity, as it could favor exotic invasions in
upstream areas. Furthermore, some sh species can colonize upstream areas through human-mediated transport
even if migration barriers are not removed38,39. Our analysis did not show sharp regional invasion gradients in
several non-fragmented rivers, albeit the spatial resolution of our data should have been sucient to underline
habitat fragmentation at that scale. Overall, exotic species invasion was still halted in upland areas, and we can
only speculate that this could be attributed to natural gradients (e.g. temperature and habitat factors).
Perhaps the most immediate outcome of our work is a visualization of the degree of exotic freshwater sh
invasion on a broad geographical scale, which highlighted the alarming decline in native species richness and
abundance at most sites in the lowlands of our focus area. A high degree of invasion corresponded also to a
lower functional diversity of invaded communities. Canals were among the most heavily invaded areas and a
good example of this mechanism, with lower overall functional diversity than rivers in the same geographical
area. is could be the result of simplied habitats, but also of the native species extinctions in this area, where
only few natives remained at the time of sampling911, but still showing higher functional diversity for the few
remaining native species than for the more abundant exotic ones. Lowland rivers with high-stream order class
had generally more heterogeneous habitats than canals, oering more spatial and trophic niche options to species
and thus presumably allowing for a higher overall functional diversity, yet showed a similar functional diversity
to that detected in canals. is pattern could potentially be caused by the presence of exotic species, which have
led to local homogenizations of the sh fauna in lowland rivers and canals that are connected to them. Conversely,
stream order 2 sites had a very low invasion degree (at the extreme le of Fig.3), yet the functional diversity of
these communities was not much higher than more invaded sites. is perhaps indicates that invasion in these
areas is not at the initial stages, and has caused a very moderate decline (if any) of native species, thus resulting
in communities where the moderate loss is compensated by a corresponding increase in functional diversity
provided by exotic species. Invasion in these areas probably did not progress further because of environmental
constraints (e.g. water temperature or habitat) or competition with native species11.
Although there are only few documented cases of extinctions in freshwater sh68, previous studies in this area
have highlighted how freshwater sh invasions could substitute native with exotic species, resulting in a decrease
of native taxonomic diversity at the local level, especially when abundances are taken into account9,10. Taxonomic
and functional substitutions have been previously advocated as non-detrimental or even benecial for the envi-
ronment and biodiversity40,41. However, from a functional perspective, our data show that exotic species generally
had a lower functional diversity than native species across similar habitats, which was evident in higher order
streams and in canals. As a consequence, substitution of native species with exotic ones could decrease the overall
functional diversity of the community.
It has been previously suggested that the availability of habitat and trophic niches in the environment might
be the ultimate factor that denes a limit to the possible expression of functional diversity. In this framework, if
Figure 5. Native (blue circles) and exotic (red circles) functional diversity (calculated through the FDis metric
applied to the ecological traits of species), in sh communities along a species richness gradient. Black lines
represent best tting non-linear regression lines for each distribution (see Supplementary Table3 for best t
regression evaluation).
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more species are added to the system functional diversity should not be positively aected, but rather show an
asymptotic saturation of the available functional space42. While our results clearly show this asymptotic satura-
tion, they also show that, in invaded communities, the functional diversity of exotic species was generally lower
than native ones, perhaps because fewer exotic species with a limited number of traits are introduced. is could
be at the root of the decrease observed in overall functional diversity of the highly invaded communities (>50%
invasion degree), as the exotic component becomes predominant and drives the overall functional diversity of the
community. is also suggests that a relatively smaller number of species with similar traits could be leading the
invasion in the lowlands, and that high degrees of invasion might coincide with higher faunal homogenization
i.e. Figure3 of the present work,11,19,43. Our view is also supported by the relatively higher functional diversity of
native species in the lowlands, despite their richness not being higher than exotic ones44. A possible explanation
is the longer evolution history in the area, which allowed natives to be more functionally diverse and match the
ecological niches in their native environment more closely45, albeit no studies have dealt with this aspect in sh
communities, so far. us, our results clearly indicate that the overall functional diversity of highly invaded com-
munities might be diminished, resulting in an overall heavier loss of diversity and adding a new dimension to the
eects of exotic invasions, which should be of great interest to conservation science and management but needs to
be further investigated. Our results disagree with the outcomes of the study by12, conducted at the macro-regional
scale. is dierence could stem from our dierent approach to the same problem: we analyzed a set of sites at
a late-invasion stage rather than using a pre/post invasion approach, but also used species abundance measures
and a ner spatial scale, which were advocated by12. e divergence in our outcomes indicates that dierent spa-
tial and biological resolutions, and dierent study setups, deeply aect the results of the analysis (see e.g.46). It is
also possible that the number and quality of functional traits investigated could further modulate the ultimate
outcome of the analysis, suggesting that the role of these factors in aecting the results would need to be tested
by future studies.
Given our results, we encourage further studies that deal with functional diversity and, more in general, a
wider use of functional approaches before a consensus is formed on the ultimate eects of exotic invasions on
diversity. Spatially- and temporally-detailed measures of species abundances would be crucial in these studies, as
subtler changes in abundances could be detected before regional extinctions occur. Future studies should investi-
gate in further detail whether a true functional loss has occurred, using a wider geographical scale and comparing
areas with dierent invasion degrees (or theoretical reference communities). Furthermore, large-scale patterns
of community diversity could be explored using measures of relative functional diversity, to express the amount
of functional diversity expressed by an average species unit. We also encourage studies that explore these mecha-
nisms in dierent taxa and, whenever possible, compare results across taxa. Ultimately, other aspects of functional
diversity should also be investigated, as they might provide useful insights on the nal outcomes of exotic and
native species interactions. ese are all necessary elements to fully understand the ecological consequences of
functional diversity loss and its signicance for ecosystem functioning at large.
Materials and Methods
Study area. Northern Italy is a dwelling area for more than 17 million humans, with consequent agricul-
tural activities and livestock farming. is area has a Mediterranean continental climate, with an annual average
precipitation of 1036 mm and a mean temperature of 12 °C. e largest river basin in Italy, the Po River basin
(71,000 km2), is included in this area and we focused our investigation on the Po River itself (in all its course), the
Oglio River (one of the most important hydrographic le tributaries of the Po River) and the hydrographic right
tributaries in the Emilia-Romagna region. We also analyzed two additional groups of rivers outside of this basin:
the Brenta River (north-east of the Po River basin) and the Romagna rivers basin (south of the Po River basin).
Overall, a total of 335 sampling sites in 105 watercourses were included in this study, covering a wide range of
freshwater habitats, dierent altitudinal zones and environmental conditions (see Supplementary Fig.1).
Organic material originating from villages, small towns and livestock farms is the main source of river pol-
lution for rivers in the uplands. Conversely, urbanization and intensive agriculture, causing high nutrient loads
and consequent eutrophication, are the main factors aecting lowland rivers10. A network of drainage canals was
established in the lowlands to support agricultural irrigation around the 19th century, with hydrological manage-
ment aimed at supplying both irrigation and drainage needs10,47. e study area was in a late invasion stage11 at
the time of sampling, since loss of native species and exotic invasion occurred already prior to 199710, before the
data analyzed here were collected.
Data collection. Fish data were collected within monitoring programs of the Emilia-Romagna region48, the
Padova Province49, the Po River50 and the Oglio River51 over a relatively long-term period (1999–2010). Despite
this, community turnover was not a relevant factor in our study, because sh communities are typically stable
over such timescales and, despite the ample interval, most of the data were collected over a limited timeframe44,52.
Fish sampling was performed between spring and autumn by electroshing, combined with nets in sites of higher
water depth and conductivity (e.g. lower stretches of the rivers), further details on sh sampling procedures are
described in8,11.
Fish species were classied according to53, taking into account recent taxonomic determinations and common
names as listed in FishBase54. Each species was categorized as native or exotic: a species was considered as native
when naturally present in a specic basin and as exotic when human-introduced, irrespective of the time elapsed
since the introduction. Hybrid specimens or uncertain species were excluded from this study in order to avoid
taxonomic asymmetries.
Abundance of each species was expressed with Moyle classes55 ranging from 1 (lower abundance, 1–2 indi-
viduals per site) to 5 (higher abundance, more than 50 individuals per site). Unfortunately, classes of numerical
abundance tend to overestimate the ecological signicance of small-bodied species and underestimate that of
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large-bodied ones, but direct measures of body-mass were not taken at the time of sampling. Attempting to over-
come this, a weight was assigned to each species based on their average adult size in the area (1 = small body up
to 150 g; 2 = medium body 150–400 g; 3 = large body over 400 g, derived from FishBase and unpublished
data) and multiplied by Moyle abundance classes, in order to obtain a body-mass-corrected abundance, hereaer
dened simply as abundance24.
Water physicochemical sampling was performed with standard methods, in temporal and spatial proximity
to the sh sampling, by dierent Regional Environmental Protection Agencies (ARPAs, in Italian) for the Po,
the Brenta and the rivers in the Emilia-Romagna region. e Oglio River Water Authority carried out the water
sampling in the Oglio River. e geographical position and the elevation of each site were recorded. Eight phys-
icochemical variables were monitored: water temperature, electrical conductivity, chemical oxygen demand, bio-
logical oxygen demand, total suspended solids, total phosphorus, ammonia (NH4+) and nitrate nitrogen (NO3).
Land cover data were obtained from the CORINE database (2012, https://www.eea.europa.eu/data-and-maps/
data/copernicus-land-monitoring-service-corine). In the lowlands, where estimation of watershed areas is more
dicult due to low slopes and human-regulated ow, the land cover of the whole river basin or of the adminis-
trative province was used. CORINE land cover classes were merged in ve categories based on the main land use
in order to better describe the study area: urban use, agricultural use, forest, other natural area, freshwater and
brackish water. Land cover was expressed as the share of each of these categories in the watershed of each site.
Fish functional traits. In order to investigate the functional composition of sh communities, ve dier-
ent ecological functions were examined: feeding, reproduction, migration, tolerance and habitat use. Within
these ecological functions, all sh species were classied in guilds, each representing an ecofunctional trait
(Supplementary Table1, see also Noble, et al.56). Ecological functions, guilds and classication for most species
in this study were taken from24, where all available information was used to identify appropriate guilds for each
species. e same methodology was applied to classify euryhaline species that were not included in previous work
(see Supplementary Table2). A total of 59 sh species were sampled in the study area; of these 37 were native and
22 were exotic species, relatively to the national territory.
Inuence of environmental variables on functional diversity. Fish functional diversity was investi-
gated through the functional dispersion metric FDis,57. FDis was calculated using one matrix with species abun-
dance and another matrix of functional traits of sh communities through the dbFD function58. FDis calculates
the spread of traits in multidimensional space by measuring the distance of each species from a centroid weighted
by the species abundance.
As a result, FDis measures the relative diversity of functional traits in a community, communities with larger
FDis values are more diverse in species traits combinations, whereas low FDis values refer to communities with
more traits in common. e advantages in choosing the FDis metric include that it should theoretically not be
overly aected by species richness, can be computed from any distance or dissimilarity measures and take into
account any number and type of traits (also qualitative traits, as in this study), is not strongly inuenced by outli-
ers and accounts for species abundances57. FDis was calculated for both the whole sh community and for exotic
and native species separately, using species abundance as weights to dene the relative representation of each trait
in the community.
e relative inuence of geographical and land use features, as well as water physicochemical variables, on
functional diversity was investigated with a machine learning method: the boosted regression trees (BRT)59. BRT
analysis is an ecient method to describe any non-linear relationships between variables (e.g. thresholds) and
incorporate interactions between variables. Compared to traditional regression methods, BRT analysis combines
a large number of simple tree models using the boosting technique to improve the predictive performance. BRT
analysis was applied to native and exotic species separately, to investigate dierences between the factors aecting
the two categories. e relative inuence (positive or negative) of each variable was determined by the prevalent
direction of its eects on the functional dispersion of species, as no clear unimodal trends were found in our data.
Guild and species abundance matrices for each sampling site were Hellinger transformed60,61 to standardize
variations among both species and community size, respectively. Environmental variables expressed as percent-
ages were arcsine transformed, while others were log-transformed. All statistical analyses were performed in R
soware version 3.4.362. FDis was calculated through the homonymous R package58. BRT was performed with
the ‘gbm’ R package63, using standard values (Gaussian distribution, bag fraction of 0.75 and shrinkage of 0.001).
Impacts of exotic invasions on functional diversity. e degree of exotic invasion in each site was
estimated through the abundance of exotic versus native species in each community (% of exotic abundance).
is measure was then spatially analyzed for all watercourses within each basin in the study area, through linear
kriging64.
We also evaluated the spatial overlap and correlation between invasion degree and functional diversity (as
expressed through the FDis metric calculated using ecofunctional traits,65). First, we used linear kriging to rep-
resent functional diversity, based on the whole community, for invaded sites (i.e. where both native and exotic
species were present, 198 out of 335 sites, excluding an invaded site at an altitude >400 m a.s.l.). We selected these
sites because we could clearly evaluate invasion eects only where both exotic and native species are present, but
also, more importantly, because it allowed us to focus our analysis on a geographically uniform area (the lowlands,
below 400 m a.s.l.) and thus avoid potentially-confounding geographical factors (i.e. altitude, as species-poor
communities at high altitudes typically have low functional diversity, even if not invaded). is area also had a
relatively homogeneous sh community at baseline conditions, so that we could consider the functional diversity
of least invaded communities as a close proxy to the baseline conditions of reference communities. Following
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this, we used the same sites to also explore the variations in overall functional diversity along the invasion degree
gradient (between 2.3% and 96.5%).
To investigate the impact of exotic invasions on functional diversity we also examined the variations in native
and exotic species richness for each stream order, alongside the respective functional diversity of each site, trying
to detect patterns indicative of invasion eects. Stream order for each site was calculated using a Digital Elevation
Model (DEM) (http://www.sinanet.isprambiente.it/it/sia-ispra/download-mais/dem20/view). Flow direction and
accumulation, as well as the watershed of each sampling site, were calculated based on the DEM layer. For the
entire river network generated by ow accumulation, stream order was derived with the Strahler method66. is
procedure was reliable for upland streams, but it was less so in the lowland, possibly due to the fact that ow
direction and magnitude in the lowlands are not always natural because of human intervention. e stream order
was thus manually checked and revised when necessary in lowland rivers and streams. Rivers were grouped into
four classes based on stream order: class 1 (Strahler stream order 1 and 2), class 2 (stream order 3 and 4), class
3 (stream order 5 and 6) and class 4 (stream order > 6). As drainage and irrigation canals could not be assigned
into any natural class, a separate class called “Canals” was created. Canals are man-made environments, usually
characterized by low habitat heterogeneity and controlled hydrology, located in the lowlands southwest of the Po
River, near its delta.
We further examined the relationship between native and exotic richness and their relative functional
diversity. We used non-linear regressions, evaluated through a combination of Akaike’s Information Criterion
(AIC) weights67 and R2 values, to estimate best-tting curves for functional diversity distributions versus spe-
cies richness and invasion degree. Non-linear best-tting regressions were estimated using the Curve Expert
Professional 2.6 soware68 and the results of the ve best regression models for each relationship were reported in
Supplementary Table3. e spatial analyses were performed with ArcGIS soware69, using its Kriging Tool and
Hydrology Spatial Analyst Tool.
Data availability
Underlying data for this paper is made available also for review as Supplementary Material and will be made
publicly available through OpenScienceFramework should the manuscript be accepted for publication.
Received: 17 April 2019; Accepted: 9 November 2019;
Published: xx xx xxxx
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Acknowledgements
We thank LL.D. V.E. Manduca and Dr. M. Rizzoli of the Fisheries Bureau of the Emilia-Romagna Region for
providing the Fish Inventories data in the context of a long-term research collaboration. e Oglio River Water
Authority (Consorzio dell’Oglio, in Italian) is also acknowledged for providing sh and water quality data for the
Oglio River. We also thank Dr R. Spaggiari and Dr S. Franceschini of the Emilia-Romagna Region Environmental
Protection Agency (ARPA-EMR), the Piemonte Region Environmental Protection Agency (ARPA-Piemonte) and
the Veneto Region Environmental Protection Agency (ARPAV) for providing the water quality database. We also
thank Jyrki Lappalainen, for his kind help with statistical analyses.
Author contributions
M.M. and A.G. conceived the idea and designed the methodology. A.G. collected and analyzed the data. M.M. led
the writing of the manuscript. M.M., A.G., J.S. and G.C. contributed critically to the dras and gave nal approval
for publication.
Competing interests
No specic funding was received for this work and the authors declare no competing interests (nancial or non-
nancial).
Additional information
Supplementary information is available for this paper at https://doi.org/10.1038/s41598-019-54210-1.
Correspondence and requests for materials should be addressed to A.G.
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... However, generalization is possible when community dynamics are affected by large scale gradients, such as for instance the upstream-downstream gradients in rivers, or gradients related to sources of human disturbance Schlosser, 1987). Moreover, local dynamics can be influenced by spatial connectivity associated for instance with the topology of stream networks, anthropogenic barriers and habitat FCUP Modelling biodiversity patterns and processes to support conservation in stream networks 198 Ch6 fragmentation Crabot et al., 2020;Erős & Lowe, 2019;Hugueny et al., 2010), as it affects meta-community mass effects mediated by dispersal (Heino et al., 2015;Tonkin et al., 2018), as well as the spread of invasive species Gavioli et al., 2019;Milardi et al., 2019;. Therefore, spatial modelling of community dynamics requires establishing relations with environmental variables predicting variation in dynamics metrics, and accounting for spatial variables reflecting the effects of connectivity. ...
... The spread of exotic species may also have affected community dynamics, due to temporal changes in their own prevalence and abundance, but also due to eventual negative effects on native species Gavioli et al., 2019;Milardi et al., 2019;Zanden et al., 2015). This is supported by faster changes in sites with higher proportion of exotic species, and by the high coefficients of variation in the abundance of exotic species when compared to most native species. ...
... rutilus). Directional changes may thus happen in the future, most likely associated with increasing prevalence and abundance of exotic species Milardi et al., 2019). ...
Thesis
Full-text available
Biodiversity is not evenly distributed across our planet. Freshwater ecosystems hold a disproportionate amount of biodiversity when compared with other biomes, though it only covers a small portion of our planet surface. Because water is essential for human activities, population growth and economic development put an enormous pressure on freshwater ecosystems. Besides the direct anthropogenic pressures, such as over exploitation, damming, habitat modification and pollution, the freshwater species usually present restricted distributions, to a watershed or a region, and face the threat of hundreds of invasive species that have been introduced to freshwater ecosystems. Due to all these factors, freshwater biodiversity is among the most threatened of our planet. Stream networks deserve special attention because they are particularly threatened and rich in biodiversity. Streams networks are linear bodies of water with a dendritic, or tree shape, organization, flowing from the headwaters to a single outlet. The distribution of organisms in stream networks are not random, resulting from several processes that work at different scales, like climate, hydrology and biotic interactions. The diversity and abundance of fish and many other organisms are usually associated with an increase in stream order, but there are also dispersal processes that should be taken into account. The distribution of some species, like invasive species, is often more a reflection of spatial processes, such as multiple introductions and posterior expansion, than environmental filters that limit the distribution. Headwaters can function as refuges from adverse biotic interactions for species that support water intermittency. Stream communities, like fish, usually persist in time in a state of dynamic equilibrium, varying between alternate states with no discernible direction of change. Deviations from this equilibrium may reflect disturbances to the community from natural states, like droughts or floods, or from anthropogenic sources. For proper conservation and management of stream networks, it is essential to understand the drivers of the spatial patterns and dynamics of stream biodiversity. Species distribution models (SDM’s) are the set of tools used to derive spatially-explicit predictions of environmental suitability, by relating species occurrences to relevant environmental data. Due to their nature and the nature of the stream network habitats, the development of SDM’s for organisms that are associated with streams is challenging. Aquatic organisms are rarely available for direct observation, and even with the help of standard techniques, like electrofishing, it is fair to assume that we will fail to detect some of the species present at any given location. This issue, known as imperfect detectability, is a common source of bias in SDM’s, and tends to be ignored by freshwater researchers. Accounting for spatial autocorrelation (SAC) improves SDM performance, but the dendritic structure of stream networks, together with strong environmental gradients, create spatial dependences with complex structures that are not completely described by Euclidean distances. Biotic interactions, such as competition or predation, are also a potential source of mismatch between the actual and the predicted distribution of species, particularly if the interactions are between invasive species and native species. Long term monitoring of communities is essential to understand the impact of anthropogenic pressures in stream ecosystems, but usually rely on data collected on any given number of discrete locations. A spatial continuous view of the temporal dynamics would be essential to study such pressures, and of value to plan conservation and management actions. The main aim of this thesis is to develop new tools and frameworks to help ecologists and conservationists to obtain a more realistic depiction of the distribution of species, and the temporal dynamics of communities at the riverscape scale. I mainly focused on solutions to the issues related to dealing with imperfect detectability, accounting for SAC in stream networks, accounting for biotic interactions, and extrapolating the community temporal dynamics to a continuous spatial prediction. To address these issues, I have collected data on the distribution of fish, crayfish, and amphibians on a specific study system, the Sabor River, a Mediterranean watershed in the Northeast of Portugal. To describe the distribution of fish species with data collected in a comprehensive electrofishing survey, while accounting for imperfect detectability, we extended the time-to-detection occupancy-detection model to include interval-censored observations, because it is difficult to ascertain the exact time-to-detection of a species when sampling fish with electrofishing techniques. Using a Bayesian hierarchical framework, we modelled the probability of water presence in stream segments, and the probability of species occupancy conditional on water presence, in relation to environmental and spatial variables. We also modelled time-to-first detection conditional on occupancy in relation to local factors, using a modified interval-censored exponential survival models. To account for SAC, we included a spatial autocovariate term in the estimation of the probability of water presence and the probability of species occupancy. Species occupancies were consistently affected by stream order, elevation and annual precipitation, while species detection rate was primarily influenced by depth and, to a lesser extent, stream width. The assumption of equilibrium between organisms and their environment is a standard working postulate in SDM’s that is seldom met, particularly for species that are expanding their range like invasive species. Furthermore, for species invading river systems, the dendritic structure of the stream network will constrain the patterns of the expansion. In this thesis, I addressed these issues by describing the distribution of two invasive crayfish in the Sabor river stream network, using a class of geostatistical models developed to deal with SAC in stream networks, known as spatial stream network models (SSNM). Accounting for SAC greatly improved model performance, evidencing that the distribution of these invasive crayfish was more of a product of spatial process than environmental filtering. Biotic interactions are important drivers of species distributions. When native species are displaced from part of their distributional range, they may persist in ecological refuges. These refuges may be patches of habitat that are unsuitable for invasive species or areas where invasive species have not reached due to distance, physical barriers or time lags in the expansion. Identifying the distribution and the environmental drivers of these refuges is of conservation concern. We modelled the distribution of amphibian ecological refuges in the Sabor river catchment, by including as predictor variables the probability of presence of the two invasive crayfish, among other environmental and spatial predictors. We found that the refuges of amphibians are located mainly in the headwaters, and that, under plausible expansion scenarios of the crayfish species, these refuges are likely to contract in the future. Management of stream networks is usually planned at the river basin scale, and as such, it is important to develop frameworks that allow the extrapolation of the community dynamics observed at discrete segments of rivers to a continuous spatial view of the entire river basin. We collected stream fish data on 30 locations on the Sabor river basin, between 2012 and 2019, and used a novel framework to describe and compare the trajectories of the fish communities using their geometric properties in a given dissimilarity space. We computed the mean velocity and the overall directionality of change of the fish community, and used the SSNM framework to relate these metrics to environmental drivers and extrapolate the community dynamics to the entire watershed. We found no evidence of directionality in the change of the Sabor fish communities, supporting the hypothesis that these communities exist in a loose equilibrium state. However, the rate of change was higher in streams draining into the hydroelectric reservoir located near the mouth of the Sabor River. These streams are likely under increased stress from the reservoir, due to alterations of the flow regime and/or expansion of alien species from the reservoir. Overall this thesis advances our understanding of the drivers that govern the distribution of species in stream networks, providing key information for the conservation of these ecosystems. The new set of tools presented here can aid ecologists and conservationists to obtain a more realistic depiction of species distribution and their temporal dynamics at the riverscape scale.
... Damming also favours alien species introduction in reservoirs (Han et al., 2008). Despite the need to condense the multiple hypotheses on invasion mechanisms in a comprehensive impact framework (Crystal-Ornelas & Lockwood, 2020), alien species are widely acknowledged as one of the major factors affecting the loss of fish biodiversity worldwide (Milardi et al., 2019;Su et al., 2021). Alien fish disturb native fish communities in multiple ways: genetic alteration; transmission of diseases and parasites; predation and habitat competition; and habitat and food web alterations (Ilhéu et al., 2014;Jia et al., 2019). ...
... Exotic species invasions often result in native biodiversity loss. One of the most evident effects of biological invasions is the loss of native taxonomic diversity; however, current knowledge on invasions effects underlined a potential increase in functional diversity 28,29 . The particular vulnerability of freshwater biodiversity also reflects the fact that freshwater is a resource for humans that may be extracted, diverted, contained or contaminated in ways that compromise its value as a habitat for organisms. ...
... Damming also favours alien species introduction in reservoirs (Han et al., 2008). Despite the need to condense the multiple hypotheses on invasion mechanisms in a comprehensive impact framework (Crystal-Ornelas & Lockwood, 2020), alien species are widely acknowledged as one of the major factors affecting the loss of fish biodiversity worldwide (Milardi et al., 2019;Su et al., 2021). Alien fish disturb native fish communities in multiple ways: genetic alteration; transmission of diseases and parasites; predation and habitat competition; and habitat and food web alterations (Ilhéu et al., 2014;Jia et al., 2019). ...
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Freshwater fish biodiversity is experiencing an alarming decline worldwide. Understanding the main factors behind its deterioration is a key step for ecosystem restoration. In this work, large‐scale and long‐term data were used to identify the causes of the decline of native species richness in Castilla‐La Mancha. This region in central Spain covers part of six river basins belonging to four of the 11 biogeographical provinces for freshwater fish in the Iberian Peninsula. Firstly, we built a dataset that associates the presence of several fish species and a wide range of environmental variables (e.g. hydrological and hydromorphological indicators, land use classes, presence of alien fish species) at selected river sites for two different time periods (1980–2000 and 2001–2020). Secondly, we conducted an exploratory data analysis to identify possible temporal trends in the dataset. Finally, we applied the random forest algorithm to predict the response of different ecological guild‐based metrics of fish richness to the selected variables. The exploratory data analysis revealed a decrease in native fish species richness in 74% of the area studied. There was no sustained temporal trend for stressor variables, except for the number of alien species, which increased in most river sites (63%). The models of the richness of native rheophilic, native intolerant, alien rheophilic, and alien limnophilic species performed satisfactorily. Magnitude of maximum discharge, presence of alien species, land use in the catchment area and altitude were the most important predictors of richness of native intolerant and rheophilic species. Alien limnophilic species proved to be sensitive to variables related to flow regime alteration, such as the presence of dams and the number of river flow reversals, while a less degraded habitat was found to be favourable to alien rheophilic species. The results suggest that the cumulative effect of persistent altered flow regimes and water pollution, coupled with a strong increase in the number of alien species, have led to the decline of native species in the area studied. The restoration of near‐natural magnitudes of high flows when implementing environmental flows emerged as a key measure to restore ecosystem integrity. Starting from a long‐term and large‐scale dataset, this study provides new, quantitative insights into stressor–ecosystem relationships in rivers and could inform future environmental policy initiatives because it has identified the main factors leading to native fish decline and alien fish proliferation. Our findings emphasise the importance of considering metrics based on fish assemblage composition and ecological functional groups in order to disentangle the effects of stressors on fish communities.
... We then calculated an invasion degree, i.e. the share of introduced species in freshwater fish communities, based on the abundance of introduced and native species see e.g. 9,49 . A high invasion degree equals to a high share of introduced species and a low share of native species. ...
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We analyzed the large-scale drivers of biological invasions using freshwater fish in a Mediterranean country as a test case, and considering the contribution of single species to the overall invasion pattern. Using Boosted Regression Tree (BRT) models, variation partitioning and Redundancy Analysis (RDA), we found that human factors (especially eutrophication) and climate (especially temperature) were significant drivers of overall invasion. Geography was also relevant in BRT and RDA analysis, both at the overall invasion and the single species level. Only variation partitioning suggested that land use was the second most significant driver group, with considerable overlap between different invasion drivers and only land use and human factors standing out for single effects. There was general accordance both between different analyses, and between invasion outcomes at the overall and the species level, as most invasive species share similar ecological traits and prefer lowland river stretches. Human-mediated eutrophication was the most relevant invasion driver, but the role of geography and climate was at least equally important in explaining freshwater fish invasions. Overall, human factors were less prominent than natural factors in driving the spread and prevalence of invasion, and the species spearheading it.
... Carp with noticeable reductions in sportfish and catostomid species (Solomon, Pendleton, Chick, & Casper, 2016 This increase may be affecting the functional community of the Open River by lowering functional diversity. This supports other studies indicating invasive species undermine functional diversity in freshwater ecosystems (Milardi, Gavioli, Soininen, & Castaldelli, 2019;Shuai, Lek, Li, & Zhao, 2018). We also found that estimates of the Shannon index indicated high-functional diversity in the La Grange pool, but the Simpson index described low-functional diversity. ...
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Large rivers are susceptible to anthropogenic alteration, which can result in drastic changes to their functional ecology. We evaluated spatial–temporal changes in the functional fish communities of the Upper Mississippi River System (UMRS) using data from six study reaches. Species were classified into one of 14 feeding guilds and mass per unit effort (MPUE) was then calculated for each feeding guild annually per gear type. MPUE was standardized using the multigear mean standardization method (MGMS) and log‐transformed. Both ANOSIM and Chi‐square tests were used to determine differences in MPUE among reaches. We then estimated functional diversity by calculating the number of functional groups (N), Margalef's d, Pielou's J′, Shannon's Diversity, and Simpson's Diversity Index. An AR(1) time series model was used to investigate proportional changes in each guild over 25 years. To evaluate the effect of invasive Carp species in invaded reaches, a Chow test was applied to observations between 2000 and 2005. Analyses revealed differences in the functional fish community among reaches. We found differences in functional diversity metrics among study reaches, but there was little evidence that this differed between invaded and non‐invaded reaches. Results determined that invertivore/detritivores have been consistently declining system‐wide, with few groups showing a net change. There was also little evidence that invasion altered the proportion of any functional guild. Evaluating the spatial–temporal patterns of functional communities is beneficial to understanding the resilience of a system and can provide further insight into its trophic needs when considering future restoration initiatives.
... Where present, it tends to dominate the community of predator fishes (~ 30% of the whole fish community biomass, M. Milardi, unpublished data). Wels catfish and other introduced fish species are a major problem also for native fish diversity in Italian freshwaters (Milardi et al. 2018(Milardi et al. , 2019a(Milardi et al. , 2020a(Milardi et al. , 2020b(Milardi et al. , 2020c, but to date, little has been done to address this problem. A recent review by Cucherousset et al. (2018) underlined how the species is widespread and abundant also in the rest of its introduced range (e.g. ...
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Predatory fish have occasionally been observed preying on birds, sometimes repeatedly, but few studies were able to unravel the overall significance of avian prey in fish diet and the predation impacts on bird populations. We used a control/impact study setup, using a Nature Reserve in northern Italy and a nearby control area, to determine: 1) the contribution of waterbirds to wels catfish diet in the Reserve, 2) the population density of wels catfish in the Reserve and control area and 3) the potential impacts of waterbird depredation by wels catfish on waterbird population trends. Our stable isotope Bayesian mixing model indicated that birds contributed 12.2% (5-27.9%, 50% confidence interval) of the diet of large wels catfish (> 98 cm in total length). Large individuals constituted the majority of the population in the shoreline areas of the reserve in 2013-2019, where the population was stable despite control efforts. Numbers were below detectable levels in the control area. Large wels catfish consumed an average of 224, 148 and 187 kg of birds during the 2019 chick growing period, as estimated through three different bioenergetic models. Compared to the control area, mallard reproductive success was diminished in the Reserve, likely due to higher rates of fish predation, although effects were variable in different years. Overall, our data suggest that high densities of invasive wels catfish might impact waterbird reproductive success through predation on bird chicks, but further studies would be needed to reduce uncertainties related to the intrinsic variability of field ecology data. Our study constitutes a preliminary attempt to assess the potential of introduced wels catfish to affect the conservation value of waterbird protection areas, and should be repeated at broader spatial and temporal scales.
... Exotic plants can cause a variety of problems in native plant communities: excluding native species; altering the habitat, hydrology, and nutrient cycling; and greatly impacting plant and animal diversity [123][124][125][126][127]. Exotic species can transform the structure and species composition of ecosystems by repressing or excluding native species, either directly by out-competing them for resources or indirectly by changing the way nutrients are cycled through the ecosystem [124,126,128,129]. The increasing global prevalence of relatively few invasive species threatens to create a relatively homogenous planet rather than one characterized by its rich biological diversity and local distinctiveness [124,125,[130][131][132]. Therefore, the invasion of alien organisms, a potentially lasting and pervasive imposition, is considered to be one of the main threats to biodiversity in the modern world [133][134][135][136][137]. Furthermore, the prevention and control of new invasions is a clear priority in emerging policies [124,128,[138][139][140][141]. ...
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In order to ecologically restore coal mine spoils, tolerant species were selected through vegetation surveys on the abandoned coal mine spoils and natural forests established on the poor environment similarly to there. In addition, tolerant species were selected through cultivation experiments in the laboratory. Many C4 plants were included among the tolerant species selected through cultivation experiments. Soil was ameliorated by applying commercial organic fertilizer that can improve both physical and chemical properties of soil at the same time. Vegetation introduced for restoration was prepared by combining plant species tolerant to the degraded environment of coal mine spoils and the reference information. The treatment with a soil ameliorator improved the chemical properties of soil, such as the pH and nutrient contents, and promoted the growth of sample plants significantly. However, additional improvements were required compared with the chemical properties of healthy forest soil. The sites restored by ameliorating soil and introducing tolerant species showed a more similar species composition to the reference sites compared with the afforested and non-restored sites in both lowland and upland areas. However, such restoration did not play a significant role in increasing species diversity or excluding exotic plants. In this respect, more active restoration is recommended.
... However, we have just begun to address the freshwater biodiversity concerns and recognise it as a priority for conservation strategies since the early 2000s [5,[9][10][11]. Currently, around one-third of the freshwater biodiversity is at risk of extinction, owing to anthropogenic disturbances, such as over-exploitation [2], habitat loss [12], pollution discharge [5], and introduction of exotic species [13]. Moreover, the extinction of species is expected to exacerbate with the ever-increasing population and the ongoing climate change [6]. ...
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Deprivation of protection for aquatic hyphomycetes is disturbing because they are key players in freshwater ecosystems across the globe. To attain a more holistic conservation paradigm for biodiversity in freshwaters, it is necessary to broaden our ecological perception of microfungi, mainly in aquatic hyphomycetes. A considerable groundwork still needs to be accomplished in progressing towards conserving aquatic hyphomycetes. Overcoming the paucity of information regarding the rare and endangered species, biogeography and above all, a global biodiversity database, would be a significant contribution in the initiation of an overarching conservation strategy for aquatic hyphomycetes. Being aware that the biodiversity decline in freshwaters is alarming, here we seek to explore why biodiversity data of aquatic hyphomycetes are missing. This article closely exam- ines the threats to the biodiversity of aquatic hyphomycetes and freshwater ecosystems. Moving forward, we advocate a structured approach to gaining a thorough understanding to embrace aquatic hyphomycetes biodiversity into the conservation strategies. Including aquatic hyphomycetes in the conservation objectives may attract more funding opportunities for global surveys to initiate a fungal inclusive conservation era. Fungal conservation ventures can profit from interdisciplinary collaborations and cutting-edge science and technology, leading to informed decision making for biodiversity assessment and management.
Chapter
Variation in physiological traits can influence the relative resilience of individuals, populations and species of fish to environmental change. Thus, understanding the extent, origins, and consequences of physiological diversity is a key challenge for fish conservation. Physiological diversity within a species can arise as a result of ontogeny, growth, and differences between sexes, and can also be generated by various types of phenotypic plasticity including acclimation, developmental plasticity and transgenerational plasticity. Genetic differences among individuals, populations, and species are also crucial drivers of physiological diversity, and interact with all of the other processes to result in the physiological diversity of living systems. Describing and preserving physiological diversity not only can help target management actions, but also has intrinsic value because high physiological diversity increases ecosystem resilience and influences the capacity for evolutionary adaptation of species to changing environments. However, quantifying the extent of physiological diversity among fishes and assessing its impacts on resilience to environmental change is a daunting task. Despite this, there have already been success stories for fish conservation to date, and taking physiological diversity into account will continue to be critically important for the management and conservation of fish in the Anthropocene.
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Aim Exotic species are a major threat to biodiversity and have modified native communities worldwide. Invasion processes have been extensively studied, but studies on species richness and beta diversity patterns of exotic and native species are rare. We investigate such patterns among exotic and native fish communities in upland and lowland rivers to explore their relationship with environmental drivers. Location Northern Italy. Methods Exotic and native fish beta diversity patterns were investigated separately in lowland and upland sites using Local Contribution to Beta Diversity (LCBD) and Species Contribution to Beta Diversity (SCBD) analyses. To examine the main environmental variables affecting the LCBD, a Boosted Regression Trees (BRT) method was used. Community dispersion among and within stream orders was investigated with the PERMDISP test. Results In lowland sites, exotic species richness was higher than native species richness, especially in large rivers and drainage canals. An opposite trend was found in upland sites, where native species richness was higher than exotic species richness, especially in large rivers. No clear LCBD patterns were found along stream orders in the lowland, whereas higher stream orders in the upland showed the highest LCBD. Its patterns in upland and lowland sites were related to a number of factors, such as total suspended solids and total phosphorus. Community dispersion among stream orders did not show a relationship with environmental heterogeneity. SCBD values were positively correlated with species occupancy in the study area, and native species showed higher SCBD values than exotic species only in the uplands. Main conclusions Large rivers in the uplands are important in maintaining native fish diversity and should be protected against invasive fish. In contrast, most lowland rivers have suffered from biological homogenization. Some rare native species can show low contribution to beta diversity, but still need conservation actions due to their risk of local extinction.
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Global spread of non‐native species profoundly changed the world biodiversity patterns, but how it translates into functional changes remains unanswered at the world scale. We here show that while in two centuries the number of fish species per river increased on average by 15% in 1569 basins worldwide, the diversity of their functional attributes (i.e. functional richness) increased on average by 150%. The inflation of functional richness was paired with changes in the functional structure of assemblages, with shifts of species position toward the border of the functional space of assemblages (i.e. increased functional divergence). Non‐native species moreover caused shifts in functional identity toward higher body sized and less elongated species for most of assemblages throughout the world. Although varying between rivers and biogeographic realms, such changes in the different facets of functional diversity might still increase in the future through increasing species invasion and may further modify ecosystem functioning.
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Functional composition of communities across scales is increasingly used to infer resilience of biotic communities to environmental change. To assess the relevance of these concepts to management of large rivers, analyses were applied to fish community data of the Upper Mississippi River. First, to evaluate whether there was evidence for structural patterns in fish size distributions, a discontinuity analysis was performed. Using long‐term fish data, consistent discontinuities were identified across 14 reaches, suggesting similar structuring processes occur throughout the nearly 1300 river kilometers represented by those reaches. Increased variability in species abundance in relation to proximity to edges of body size aggregations supports the discontinuity hypothesis that body size aggregations are structured by key processes. Functional richness and redundancy were quantified within and across identified scales for each of 14 river reaches. Diversity of trophic and spawning guilds was generally greater in the upstream reaches in comparison with downstream reaches, with the exception of the diversity of large‐bodied spawning guilds. Evidence of functional shifts in the composition of fishes occurred, but differed by size aggregations, likely reflecting scale‐specific resource availability. Redundancy of spawning and trophic groups across body size aggregations suggested downstream reaches of this system may be less resilient to disturbances and were weakly associated with reduced habitat diversity. These findings suggest that discontinuities in large river fish assemblages do occur and may provide indication of shifting resource availability. Further investigation of the underlying processes and scales that support resource availability will be critical to managing for resilience in large river ecosystems.
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Biological invasions are considered to be one of the main threats to biodiversity. Invasions lead to a loss of native species, changes to species composition, and a shift in the functioning and stability of ecosystems. In this study, derived from nine consecutive years of monitoring data and based on morphological functional trait values measured at the individual-level, we quantified the functional differences between native and non-native fish species and further assessed how biological invasions impact on species richness and functional diversity in the large subtropical Pearl River in southern China. Specifically, we differentiated intraspecific functional variability by separating individuals of a species according to their different life stages. Our results provided strong evidence that native and non-native fish were significantly different in their functional attributes. Invasion caused no obvious change in species richness; however, the yearly increase in non-native populations was accompanied by a significant decrease in functional niches of native species and change in several aspects of functional diversity in the fish community. Decreasing functional richness, and increasing functional divergence and specialization, indicated that most native species had been replaced by non-native species with different specific functional traits, which may affect ecosystem stability. Notably, this study provided empirical evidence that functional diversity was more sensitive to biological invasions than species richness. Our results show that control of non-native aquatic species is both necessary and urgent in the Pearl River. An understanding of the processes described in this study can form the basis of conservation in fish community, which is critical to sustainable and successful fisheries.
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The invasion of exotic species is one of the main threats to worldwide biodiversity and can be aided by changes in environmental conditions. We hypothesized that a temporal trend of decreasing discharge and increasing temperature might have favored the invasion of warm-adapted, lentic exotic fish species in the lower Po River, northern Italy. We used presence/absence data over a long-term period (over 20 years) to investigate the dynamics of exotic fish invasion along water temperature and discharge gradients. Mean annual discharge and temperature did not show a clear trend and did not affect exotic fish species invasion, which progressed with time irrespective of these factors. The total number of species fluctuated without a clear trend, which underlined a progressive substitution of native species with exotic ones. Perhaps surprisingly, the community composition changed over time towards more temperature tolerant but also rheophilic, benthivore and generalist fish species. These results highlight how species interactions could be one of the main factors driving the invasion. Furthermore, our data underlines a continuously rising tide of exotics, which questions the success of past control strategies. Considering the current conservation resources limitations, priority should be given to the development of prevention strategies in order to avoid new species introductions.
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1. The long-term impact of river regulation on fish functional diversity by a dam immediately upstream from the upper Paraná River floodplain, Brazil, was evaluated. It was expected that the resulting alterations in natural flow, downstream from the dam, would negatively impact fish species, resulting in a functional simplification of the ichthyofauna. In addition, this effect was expected to be more pronounced in the directly affected main channel of the Paraná River than in its tributaries, the Baía and Ivinhema rivers. 2. Fish were sampled before (pre) and after (post) dam closure (the intervention). The functional traits used were diet, habitat use, mouth position, migration, parental care, internal fertilisation and maximum total length. Differences in trait composition between periods (pre and post) were tested using a PERMANOVA main-test. An indicator value analysis (IndVal) was applied to identify which traits significantly increased or decreased in abundance after the intervention. The indexes used were functional richness (FRic), Rao’s quadratic entropy (FDQ) and functional redundancy (FRed). The intervention analysis based on linear models for time series was used to evaluate differences in these indexes over time. 3. Traits most representative during pre-intervention were large-bodied species with long reproductive migrations, pelagic, with subterminal and superior mouths, and herbivorous. Traits most representative during the post-intervention were omnivorous species, with parental care, benthopelagic and insectivorous, which typically characterise fishes that inhabit stable environments. FRic decreased in Paraná and Baía rivers after the construction of the dam. However, the Ivinhema River showed an increase in mean FRic in the post-intervention period. FDQ decreased substantially in all three rivers, while FRed increased. 4. The combined results of FRic, FDQ and FRed corroborate the functional simplification hypothesis expected from flow regulation by dams on functional diversity. As expected, the most pronounced simplification occurred in the Paraná River. Therefore, hydroelectric power plants can act as environmental filters strongly selecting functional traits of the downstream fish fauna, generating long-lasting impacts on ecosystem functioning and services.
Article
Although one of the most evident effects of biological invasions is the loss of native taxonomic diversity, contrasting views exist on the consequences of biological invasions on native functional diversity. We investigated this topic using Mediterranean stream, river and canal fish communities as a test case, at 3734 sites in Italy, and distinguishing between exotic and translocated species invasion in three different faunal districts. Our results clearly confirmed that introduced species were widespread and in many cases the invasion was severe (130 communities were completely composed by introduced species). Exotic and translocated fish species had substantially different geographical distribution patterns, perhaps arising from their differences in introduction timing, spread and invasion mechanisms. We also found a clear decreasing trend of functional dispersion along an invasion gradient, confirming our hypothesis that the invasion process can diminish the relative diversity of ecofunctional traits of host fish communities. Furthermore, our results suggested that exotic species might have a greater negative effect than translocated species on the relative diversity of ecofunctional traits of fish communities. This could also be linked to the fact that translocated species are more ecofunctionally similar to native ones, compared to the exotics. Our multivariate analysis of site-specific combinations of ecofunctional traits highlighted some traits characteristic of all invaded communities, while our discriminant analysis underlined how there was a substantial ecofunctional overlap between native, exotic and translocated species groups in most areas.
Article
Rivers worldwide are impacted by human activities such as habitat degradation, habitat fragmentation, waterway flow regulation, and introduction of exotic species, which are responsible for the reduction or the disappearance of native species in many parts of the world. The Oglio River, a tributary of the Po River in Northern Italy, is a good example of a river with a long history of human alteration and where exotic invasions are present. We used data on water parameters and fish communities along the watercourse to investigate whether low flow conditions, degraded water quality, abundant exotic species, and the presence of migration barriers could be a disadvantage for native species. We used ordination methods (redundancy analysis), variance partitioning analysis, and the threshold indicator taxa analysis to explore changes in community composition and ecofunctional traits along an altitude gradient. We found that exotic species affected native ones more than water quality and hydromorphological parameters. Native species were most abundant in the upper reach of the Oglio River, despite low flow and shallow depth. Moreover, rheophilic and clear water native fish decreased rapidly in the lower reach of the river, where exotic species increased. This distribution could be explained by the presence of barriers in the middle reach, which block exotic species migrating upstream from the highly invaded Po River, and by a lower suitability of the upper reach for some exotic species. Our results provide a general description of the fish fauna of a strongly regulated river and can contribute to develop more effective fish and water management practices.
Article
The implementation of the European Water Framework Directive, especially regarding the establishment of fish indexes for riverine habitats, has taken different paths in different countries. For example, in Italy previous efforts have been directed towards a taxonomy-based index, contrarily to most other European countries where an ecofunctional approach took place. Taxonomical indexes are particularly hard to apply to Mediterranean countries, where fish taxonomy is often revised causing problems in practical implementation. Alternatively, ecofunctional characteristics of fish communities could be exploited to inform on river habitat quality and to detect anthropogenic impacts, thus reducing the index sensitivity to the taxonomical variability of the fish fauna. We therefore proposed a new, multimetric index based on ecofunctional traits of fish species (EFFI, EcoFunctional Fish Index) and tested it on 208 river sampling stations of the Emilia-Romagna region, northern Italy. Using theoretical reference communities, ecological quality ratios were estimated for the whole area expressing the ecological distance of each site from reference conditions. Perhaps unsurprisingly, this work underlined how fish communities were more degraded at lower altitudes than at higher ones. EFFI scores were remarkably close to two already-established indexes for chemical (LIM) and macrozoobenthos communities (IBE) alteration. Further work should explore the validity of this approach over a wider geographical range as well as investigate the definition of environmental class boundaries and its potential intercalibration with other indexes.
Presentation
An oral presentation documenting the extinctions and range shifts of native fish species caused by eutrophication and exotic species