Estuaries and Coasts
https://doi.org/10.1007/s12237-022-01105-6
Impact of Colonizer Copepods on Zooplankton Structure and Diversity
in Contrasting Estuaries
Ziortza Barroeta1,3
· Fernando Villate1,3 · Ibon Uriarte2,3 · Arantza Iriarte2,3
Received: 12 January 2021 / Revised: 3 July 2022 / Accepted: 7 July 2022
© The Author(s) 2022
Abstract
The impact of the occurrence of the non-indigenous species (NIS) Acartia tonsa, Oithona davisae, and Pseudodiaptomus
marinus and of the range-expanding copepods Acartia bifilosa and Calanipeda aquaedulcis on the structure and diversity
of zooplankton communities was analyzed using 18 years (1998–2015) time series from the contrasting estuaries of Bilbao
and Urdaibai (Basque coast, Bay of Biscay). Changes in the structure of communities were assessed by using multivariate
analyses of taxa abundances and changes in diversity by using descriptors of alpha, beta, and gamma diversity. The most
evident changes occurred at the upper reaches of the estuary of Bilbao, where an abundant and less diverse brackish community, dominated by the NIS, A. tonsa and O. davisae, succeeded a low abundance and more diverse community of neritic
origin. The later establishment of C. aquaedulcis was linked to further changes in the structure of the community and a
progressive increase in diversity. The seasonal pattern of diversity at the inner estuary and the beta diversity in the estuary
were also significantly affected by the arrival of the NIS and C. aquaedulcis. In contrast, the original low diversity brackish community of the estuary of Urdaibai, clearly dominated by A. bifilosa, was far less affected by the arrival of the same
copepod NIS, and A. bifilosa remained as the species best related to the changes in zooplankton structure and diversity in
the brackish habitats of the estuary.
Keywords Diversity · Community structure · Non-indigenous species · Acartia tonsa · Oithona davisae · Calanipeda
aquaedulcis
Introduction
Globalization and increasing trade have fostered the introduction and establishment of non-indigenous species (NIS)
beyond their natural distributional range in all ecosystems,
and as a consequence, there is growing concern about the
potential impacts at several levels (Thomaz et al. 2015).
Communicated by Wim J. Kimmerer
* Ziortza Barroeta
ziortza.barroeta@ehu.eus
1
Department of Plant Biology and Ecology, Faculty
of Science and Technology, University of the Basque
Country (UPV/EHU), PO Box 644, 48080 Bilbao, Spain
2
Department of Plant Biology and Ecology, Faculty
of Pharmacy, University of the Basque Country (UPV/EHU),
Paseo de la Universidad 7, 01006 Gasteiz, Spain
3
Research Centre for Experimental Marine Biology
and Biotechnology Plentzia Marine Station PiE, UPV/EHU,
Areatza Pasalekua z/g, 48620 Plentzia, Spain
This phenomenon is one of the most important ecological disturbances (Mollot et al. 2017), and warnings about
the serious threats posed by NIS that become invasive to
biodiversity (Vitousek et al. 1997; Strayer 2012; Simberloff
and Vitule 2014) have been given. Although more studies
have been carried out in terrestrial habitats than in aquatic
ones (Jeschke et al. 2012; Lowry et al. 2012), the impact of
human activities, in general, and of invasions, in particular,
are likely greater in aquatic ecosystems than in terrestrial
ecosystems (Thomaz et al. 2015). This is more evident in
estuaries and connected habitats where human impact has
caused a decrease of > 90% of formerly important species,
destroyed > 65% of the main habitats, degraded water quality, and increased species invasions (Lotze et al. 2006). The
increase in commercial shipping has made estuaries one of
the most vulnerable ecosystems to the arrival of new species (Frisch et al. 2006), due to the unavoidable presence
of a huge variety of organisms, including copepods, in ship
ballast waters (Bailey 2015), and because NIS may be more
resistant to adverse environmental conditions than native
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Estuaries and Coasts
ones (Katsanevakis et al. 2014). Although studies on benthic species are much more abundant than on pelagic ones
(Thomsen et al. 2014), the pelagic communities are pivotal
in the functioning of many aquatic systems. Indeed, zooplankton play a key role in the pelagic food webs, being the
link between primary producers and higher trophic levels
and also in biogeochemical cycles and being also good sentinels of environmental changes in the marine environment
due to their physiology and short life cycles (Webber et al.
2005; Ji et al. 2010).
NIS can affect the recipient community in highly variable
ways, from changes in the density, even local extinction of
native species, to changes in the structure, diversity, and
functions (Thomsen et al. 2014; Gallardo et al. 2015; Chan
and Briski 2017), which can influence ecosystem stability
over time because species respond differentially to temporal environmental variations (Mccann 2000; Schindler
et al. 2015). In many systems, the establishment of multiple
NIS has occurred, and scientists need to address the consequences of multiple invasions within a community (Olden
and Poff 2003). Nevertheless, it has to be born in mind also
that many of the NIS effects on the ecosystems they colonize
are not easy to observe because they may take a long time
to reveal, and therefore, the full impact on biodiversity may
not be apparent in the short term (Gallardo et al. 2015).
Conversely, several theories suggest that the diversity and
community structure of an habitat could also influence the
invasion success of a NIS in that habitat. One of the forefathers of these ideas was Charles Elton who developed the
so called diversity-invasibility hypothesis (DIH) which predicts that it is more difficult that biologically more diverse
communities are invaded by novel species (Elton 1958). He
argued that more diverse ecosystems should be more resistant to invasion by NIS, that is to say, that they would show
a higher ecological resistance.
Although global-scale diversity trends are easier to detect
under the current situation of global biodiversity loss, localscale diversity trends are more complex (Richirt et al. 2019),
because they may be strongly influenced by local ecological
context (Elahi et al. 2015). One of the main tools to study
the changes in long-term monitoring of large numbers of
species and ecosystems is diversity indices (Magurran et al.
2010; Vackár et al. 2012). There are different diversity types
depending on the focus: alpha diversity which reflects the
variability in a small area of homogeneous habitat, gamma
diversity which indicates variability at the regional level
(or within a system with different habitats), and beta diversity which gives us the turnover of taxa from one habitat to
another (Ricklefs 2010). It is relevant to note that the effect
of invasions in the organization of diversity in the space can
differ from local species assemblages (alpha diversity) to
diversity that accumulates from compositional differences
between local assemblages (beta diversity), depending on
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the balance of processes that cause species heterogenization
or homogenization between sites (Socolar et al. 2016). These
indices are easy to calculate, and they are not only relevant
for making science but also to inform policy, because diversity is something our societies care about (Aslaksen et al.
2015).
Zooplankton monitoring programs are an essential tool
to improve our understanding and management of effects
related to NIS in estuaries. These programs have recently
started to focus on the variations in community structure
and functional diversity based on indicators (Chiba et al.
2018), such as the Aichi Biodiversity Target indicators at
the global scale described in the Convention on Biological
Diversity (2016).
Accordingly, we made use of the monitoring program of
the zooplankton community carried out since 1998 in two
contrasting estuaries of the Bay of Biscay, i.e., the estuaries
of Bilbao and Urdaibai, to analyze variations in community
structure and diversity induced by multiple new copepod
occurrences. Over the study period, we detected the arrival
of the copepod NIS Acartia tonsa, Oithona davisae, and
Pseudodiaptomus marinus in both estuaries, as well as the
previously undetected copepods Acartia bifilosa and Calanipeda aquaedulcis in the estuary of Bilbao (Albaina et al.
2009; Barroeta et al. 2020). The latter two species were
already found in the first studies on zooplankton carried out
in the estuary of Urdaibai and other estuaries of the Basque
coast in the late 1970s and early 1980s of the past century
(Villate et al. 2004), so we do not know if they were also in
the estuary of Bilbao before it became highly polluted. The
present work aims to determine the role of the occurrence
and settlement of NIS and C. aquaedulcis and A. bifilosa on
the changes in the structure and diversity of the zooplankton communities of the estuaries of Bilbao and Urdaibai
from 1998 to 2015. Moreover, the contrasting community
structure and diversity conditions in these estuaries before
the colonization allow us to discuss about their influence in
invasion success.
Methods
Study Area
The estuary of Bilbao is a small (~ 23 km) and shallow (between
0.5 and 32 m deep) estuary located in the inner Bay of Biscay
(43º 23′ N, 03º 07′ W) (Fig. 1). It is a meso-macrotidal estuary where euhaline waters dominate (Villate et al. 2013); the
inner part is strongly stratified with salinity below the halocline
around 30, whereas the outer part is partially mixed (Intxausti
et al. 2012). Tidal flushing is relatively low; therefore, water
residence time is medium–high (~ 29 days), being lower in
the channelized upper and middle reaches than in the outer
Estuaries and Coasts
Fig. 1 Maps of the estuaries of Bilbao and Urdaibai showing the spatial range of the salinity zones (26, 30, 33, 34, and 35) that were sampled
Abra embayment, and much lower in above halocline layers
(0.1–1.6 days) than in below halocline layers (0.3–11.6 days)
for most of the estuary length (Uriarte et al. 2014) (Table 1).
The main tributaries are Ibaizabal and Nerbioi rivers entering at
the head of the estuary, although there are other small streams
draining into the middle reaches. For most of the twentieth
century, it was a highly polluted system due to the high industrialization of the area and raw sewage discharges, which gave
rise to very high heavy metal concentrations and a permanent
hypoxia/anoxia situation (Villate et al. 2013; Irabien et al.
2018). However, in 1979, a rehabilitation program was initiated
with a comprehensive plan for the sanitation of the metropolitan
13
Estuaries and Coasts
Table 1 Main hydro-morphological characteristics of the estuaries of Bilbao and Urdaibai
Estuary
a
b
d
d
Mean volume (V)
(× 106 m3)
a
Mean river flow
(m3/s)
b
Bilbao
Urdaibai
22.6
12.2
c
1798.8
183.2
402.1
12.9
35.6
3.6
d
Estuary
b
Mean tidal prism (Ω) Tidal index (Ω/V)
(× 106 m3)
d
d
Bilbao
Urdaibai
d
72
14
28
86
Length (Km)
77
4.86
Area (Km2)
1.5
1.9
0.19
0.38
Basin area (Km2)
% of subtidal area
% of intertidal area Range of
stratification index
0.9–22.8
0–13.8
Average
depth (m)
9.5
2.6
Average
salinity
stratification
8.8
2.3
Information sources: aMonge-Ganuzas et al. (2019)
b
Villate et al. (1989)
c
Cearreta et al. (2014)
d
Borja et al. (2004)
area of Bilbao, and there was also an industrial decline in the
area. Since then, heavy metal concentrations have decreased
(Fernandez-Ortiz De Vallejuelo et al. 2010), and dissolved
oxygen (Villate et al. 2013) and diversity (Borja et al. 2006)
have increased. Nevertheless, it is a completely man-modified
estuary, where land reclamation has been very extensive, the
whole estuary except the outer Abra zone became channelized
(Cearreta et al. 2004). Port facilities located in this Abra zone
are an important marine transport and logistics center in the
European Atlantic Arc.
The estuary of Urdaibai is a smaller (~ 12.5 km) and shallower (3 m depth on average) meso-macrotidal estuary located
in the inner Bay of Biscay (43º 22′ N, 02º 43′ W) (Fig. 1).
The inner part of the estuary is partially stratified, with salinities below the halocline around 26, but the outer part is well
mixed. Freshwater inputs of the main river flowing into the
estuary (Oka river) are low, and seawater dominates at high
tide (Iriarte et al. 2015), water residence time being low
(Valencia et al. 2004). At the upper and intermediate reaches,
there are salt marshes and muddy intertidal areas, whereas
extensive intertidal flats, mostly sandy ones, are found at the
lower reaches (Table 1). The estuary of Urdaibai is part of a
biosphere reserve and is one of the most important wetlands
of the Iberian Peninsula. However, until 2003, dredging was a
usual activity to allow launching ships built in a small shipyard
located in the middle reaches. Nevertheless, since then, ships
are only partially built in this shipyard, no dredging has been
carried out, and the estuary has gradually become shallower
(Monge-Ganuzas et al. 2013). The main source of pollution
is a small sewage treatment plant located in the inner zone,
the estuary having a low to moderate anthropogenic impact
(Cotano and Villate 2006). In the outer reaches of the estuary, there are also two small recreational harbours (Mundaka
and Busturia) and the port of Bermeo, which is located a few
13
kilometers away from the mouth of the estuary and is one of
the main Basque fishery ports in the Bay of Biscay.
Data Source
The biological and environmental data (1998–2015 period)
used in this study were obtained from an ongoing monitoring program of the zooplankton community of the estuaries
of Bilbao and Urdaibai. Because both systems have small
estuary basins and are subject to torrential hydrological
regimes and semidiurnal tidal regimes that produce strong
temporal variations in the salinity zonation, a Lagrangian
type of sampling strategy (Modéran et al. 2010) was used,
sampling in water masses of specific salinities instead
of doing it at fixed points. Thus, samples were collected
monthly at the sites of 30, 33, 34, and 35 salinities in the
estuary of Bilbao (B30, B33, B34, and B35) and 26, 30,
33, and 35 salinities in the estuary of Urdaibai (U26, U30,
U33, and U35) during high tide (Fig. 1). The salinity values correspond to those measured at the zooplankton sampling depth. At each salinity site, zooplankton samples were
collected below the halocline by 2–3 min horizontal tows
using a 200-µm mesh size net equipped with a mechanical
flow meter (Hydro-Bios) and subsequently preserved in 4%
buffered formaldehyde for later counting and identification
to the lowest possible taxonomic level under an inverted
stereomicroscope. Zooplankton samples were diluted to a
specific volume (10–100 ml) in order to obtain a suitable
density of individuals, and we took a number of aliquots
for the identification and counting of individuals until at
least 100 individuals of the most abundant taxon and 30
individuals of the second and third most abundant taxa were
counted.
Estuaries and Coasts
Data Pre‑Treatment
Zooplankton missing values (around 6%) of the time series
were filled with the mean of the preceding and following
month values (Head and Pepin 2010; Fanjul et al. 2018).
Only those species that showed an abundance > 0.01% during the period 1998–2015 in data pooled for the two estuaries were taken into consideration for the calculation of
the diversity indices using the abundance sorting method
adapted from Ibañez et al. (1993). Zooplankton data were
grouped and analyzed at two levels: (i) the zooplankton
group level that included 19 groups and (ii) the copepod
species level that included 25 taxa (Table 2).
For the multivariate ordination analyses, taxa densities
were transformed to log10 (x + 1) (hereinafter referred to as
log (x + 1)) so that data could approach the required normal
distribution. In order to test changes in diversity indices due
to the new colonizing copepods, we distinguished three periods according to their colonization process. Thus, period
1 lasted from 1998 to 2002 (before the occurrence of A.
tonsa and O. davisae in large numbers), period 2 from 2003
to 2009 (after the establishment of A. tonsa and O. davisae and before the occurrence of P. marinus), and period 3
from 2010 to 2015 (after the occurrence of P. marinus and
a marked increase of C. aquaedulcis).
Data Analyses
Multivariate ordination methods were used to model the
variability in the taxonomic structure of zooplankton communities at each estuary using the Canoco v 4.55 software.
A principal component analysis (PCA) of the zooplankton
taxa densities (log (x + 1)) of each estuary was conducted
using month as co-variable to remove seasonal variability.
The year scores of the first two axes for each salinity site
were depicted, in order to show year-to-year variation patterns in zooplankton community structure. The position of
each taxon in the first two axes was depicted in order to
visualize which taxa contributed most to the main interannual and spatial (salinity sites) changes in the structure of
Table 2 List of taxa used in the analyses (full names and abbreviations)
Copepods
Zooplankton groups
Taxa
Abbreviation
Taxa
Abbreviation
Acartia tonsa +
Oithona davisae +
Pseudodiaptomus marinus +
Calanipeda aquaedulcis
Acartia bifilosa
Acartia clausi
Acartia discaudata
Acartia margalefi
Paracartia granii
Oithona nana
Oithona similis
Oithona plumifera
PCPC-calanus assemblage *
Temora longicornis
Temora stylifera
Euterpina acutifrons
Ditrichocorycaeus anglicus
Oncaea media
Calanus sp.
Calocalanus sp.
Centrophages sp.
Candacia sp.
Fresh water copepods
Microsetella sp.
Harpacticoids
Ato
Oda
Pma
Caq
Abi
Acl
Adi
Ama
Pgr
Ona
Osi
Opl
PCPC
Tlo
Tst
Eac
Dan
Onc
Cala
Calo
Cen
Can
Fwcop
Mic
Har
Appendicularians
Doliolids
Chaetognaths
Siphonophores
Bivalve larvae
Gastropod larvae
Cirripede larvae
Decapod larvae
Ichthyoplankton
Medusae
Echinoderm larvae
Cyphonaute larvae
Polychaeta larvae
Cladocerans
Ostracoda larvae
Isopods
Mysids
Ascidian larvae
Copepods
App
Dol
Cha
Sip
Biv
Gas
Cir
Dec
Ict
Med
Ech
Cyp
Pol
Cla
Ost
Iso
Mys
Asc
Cop
*
Includes the genera Paracalanus, Clausocalanus, Ctenocalanus, and Pseudocalanus, the species Paracalanus parvus being the dominant and
Ctenocalanus and Pseudocalanus species very scarce at the level of adults
+
NIS: non-indigenous species
13
Estuaries and Coasts
communities. For their representation in figures, zooplankton taxa and copepod species were classified into the following: NIS copepods, A. bifilosa, C. aquaedulcis and brackish
copepods, meroplankton groups, neritic groups and copepods, freshwater copepods, and other categories (benthic or
nektobenthic groups).
The diversity of zooplankton groups and copepod species
was analyzed by calculating alpha, beta, and gamma diversity
indices from raw abundance data using Primer 6 software.
The Shannon index (H´ = − Ʃpi·lnpi; being pi = relative abundance) was calculated at a monthly scale for each salinity site
of each estuary to estimate alpha diversity, and pooled for all
salinity sites of both estuaries to estimate gamma diversity.
To determine beta diversity, the Whittaker index was calculated at a monthly scale for each estuary (Magurran 2004).
The monthly variations from 1998 to 2015 of all diversity
indices are shown in contour plots made using the Surfer® 10
software (Golden Software, LLC). In order to establish the
relationships of interannual changes in diversity (alpha and
gamma) with those in the density of NIS species, A. bifilosa,
C. aquaedulcis, key neritic copepod species, and zooplankton
groups (the five most abundant ones were selected in each
case) over the study period, dispersion plots of the selected
taxa deseasonalized density vs. deseasonalized diversity values were used. For this purpose, the seasonal effect, which
is the major temporal pattern of variation in plankton time
series (Ribera D´Alcalà et al. 2004; Benedetti et al. 2019),
was removed by using standardized anomalies of both copepod species/zooplankton group densities (log (x + 1)) and
Shannon index values. Standardized anomalies were calculated as the difference between each value and the mean value
for each month for the study period divided by the standard
deviation (Taboada et al. 2019). To visualize covariation patterns between diversity and density of key taxa, linear regression fits were calculated and plotted. In order to eliminate
Fig. 2 Year average scores on
the first two axes of the PCAS
of zooplankton taxa densities
(log (x + 1)) at each salinity site
in (a) the estuary of Bilbao and
(b) the estuary of Urdaibai
13
relationships likely to be spurious due to data scarcity, linear
regression lines were only shown when the number of cases
was higher than 5% of the total in the data series.
Results
Community Structure
The first component (axis 1) of the PCA of zooplankton taxa
densities from the estuary of Bilbao accounted for 41.4%
of the total zooplankton variability. The plot of year scores
along axis 1 (Fig. 2a) revealed similar trends of interannual
variation at B30, B33, and B34 sites, but the magnitude of
the change increased with decreasing salinity and was highest
at the innermost site (B30). At B34, however, a slight return
trend towards the initial community structure was observed in
the year 2009. At the outermost salinity region (B35), however, no clear trend of community change was observed. The
ordination of zooplankton taxa along axis 1 (Fig. 3) emphasized the major role of the NIS A. tonsa and O. davisae as
responsible for the zooplankton community changes during
the study period together with the NIS P. marinus, the brackish
copepods C. aquaedulcis and A. bifilosa, and bivalve larvae.
All those taxa increased in abundance over time, particularly
in the lowest salinity site. Several neritic copepods, such as
Temora stylifera, Oncaea media, Oithona plumifera and Acartia clausi, and holoplankton groups such as siphonophores and
cladocerans, also contributed to this major (axis 1) pattern of
zooplankton variation, showing an opposite trend to that of
the former taxa. The second component (axis 2) of the PCA
accounted for a much lower percentage of the total variability
(15.7%) and showed a similar interannual pattern of zooplankton variation at all salinity sites (Fig. 2a), which was mainly
explained by the common patterns of increase in time of some
Estuaries and Coasts
Fig. 3 Taxa scores on the
first two axes of the PCAs of
zooplankton taxa densities
(log (x + 1)) in the estuaries of
Bilbao and Urdaibai. Abbreviation meanings can be found in
Table 2. NIS copepods (red);
A. bifilosa, C. aquaedulcis,
and other brackish copepods
(green); meroplankton groups
(yellow); neritic groups and
copepods (blue); freshwater
copepods (black); and other
categories (gray)
meroplankton (gastropod and bivalve larvae) and holoplankton
(appendicularians) groups, and neritic copepods such as the
PCPC assemblage and Oithona similis. Only freshwater copepods showed a slightly opposite trend to those taxa (Fig. 3).
In the estuary of Urdaibai, the first component (axis 1) of
the PCA analysis accounted for a much lower variability of
the zooplankton community (23.7% of the total variability)
than in the estuary of Bilbao (Fig. 2). The plot of year scores
along axis 1 (Fig. 2b) did not show clear trends of zooplankton change throughout the study period at any salinity and
revealed that the main interannual fluctuations were similar at all salinities. The strongest change in the community
structure of the entire estuary was that occurred in 2012 as
compared to the rest of years. These fluctuations reflected
a common pattern of variation of most neritic taxa, with
the neritic copepods Euterpina acutifrons, Oithona nana,
and the PCPC assemblage showing the highest contributions. Slightly opposite trends were observed mainly for the
NIS A. tonsa. The second component (axis 2) accounted for
17.3% of the total variability and revealed an overall progressive change of zooplankton community from 1998–2002
to 2010–2015, which was similar at all salinities (Fig. 2b).
This change was mainly produced by the density variations
of the brackish NIS copepod A. tonsa, some meroplankton
groups (larvae of gastropods, polychaetes, and cirripedes),
and the brackish native copepods A. bifilosa and P. grani,
which were opposite to those of some neritic holoplankters,
i.e., siphonophores, doliolids, T. stylifera, O. plumifera, O.
media, and the PCPC assemblage (Fig. 3).
Diversity
Alpha Diversity
There were between-estuary and within-estuary (spatial) differences in the temporal variations of alpha diversity both
for copepod species and zooplankton groups (Fig. 4). In the
estuary of Bilbao, the values and seasonal variations (smallest
diversity in late winter-early spring and highest in autumn for
copepod species, and smallest in autumn–winter and highest in
late spring-early summer for zooplankton groups) were rather
similar across the entire estuary in the period 1998–2002.
However, values and seasonal variations of alpha diversity
showed higher differences landwards from B34, while they
remained similar in the outer estuary (B35) in the next two
periods. At the lowest salinity site (B30), alpha diversity for
both copepod species and zooplankton groups decreased from
1998–2002 to 2003–2009, with the strongest decrease having
occurred from 2002 to 2004–2005. The seasonal pattern also
showed interannual changes, and late summer-early autumn
became the time of the year with lowest diversity values in the
2003–2009 period. In the last period (2010–2015), however, at
B30, the seasonal changes in diversity differed between copepod species and zooplankton groups. The diversity of copepod species increased and the seasonal pattern was similar to
that of the previous period, while the diversity of zooplankton
groups decreased, and the seasonal pattern showed higher variation between years. At intermediate salinities, the interannual
and seasonal changes of alpha diversity for both copepod species and zooplankton groups at B33 were more similar to those
at B30 while those of B34 were more similar to those of B35.
In the estuary of Urdaibai, alpha diversity of copepod
species and zooplankton groups decreased, in general, from
high salinity sites (U35 and U33) to the lowest salinity site
(U26) from the beginning of the study period, and showed
large interannual fluctuations, mainly at the innermost site
(U26), but no clear trends over the study period. The seasonal patterns of alpha diversity of copepod species and
zooplankton groups showed variations between years and
periods, but such variations decreased with increasing salinity in the estuary. At the outermost site (U35) the seasonal
pattern of diversity was rather similar over the study period,
generally with lowest diversity in early spring for copepod species and autumn for zooplankton groups. The main
13
Estuaries and Coasts
Fig. 4 Contour plots showing seasonal and interannual variations of the alpha diversity index (Shannon index) of the copepod species and zooplankton groups at the studied salinity sites of the estuaries of Bilbao (B30, B33, B34, B35) and Urdaibai (U26, U30, U33, U35)
differences between periods in the seasonal patterns of alpha
diversity of copepod species and zooplankton groups were
due to the decrease of diversity in spring from 1998–2002
to 2010–2015, which was more marked in copepods at intermediate salinities (U30 and U33).
The relationship between deseasonalized variations in
copepod alpha diversity and deseasonalized density variations of copepod species differed between estuaries and
salinities (Fig. 5). In the estuary of Bilbao, diversity showed
a strong negative relationship to the density of the NIS A.
tonsa at all salinities and also to the density of the NIS O.
davisae in the innermost salinity zones (B30 and B33).
Likewise, the density of P. marinus was found to influence
copepod diversity positively at B30 and the density of C.
aquaedulcis negatively at B33. In the outer salinity zones
13
(B34 and B35), however, diversity was strongly and negatively related to the density of the neritic copepod A. clausi,
but positively related to the density of the PCPC-calanus
assemblage. The density of the congeneric species O. nana
and O. similis species also showed positive relationships to
copepod diversity at some salinity zones of this estuary. In
contrast to the estuary of Bilbao, in the estuary of Urdaibai,
copepod alpha diversity showed a strong negative relationship to the density of A. bifilosa at all salinity sites, except
at U35, where it was inversely related to the densities of
A. clausi and PCPC-calanus. In this estuary, copepod alpha
diversity showed a negative relationship to the density of the
NIS A. tonsa only at U26 and U30. Regarding zooplankton
groups (Fig. 6), their alpha diversity was found to be negatively related to the density of copepods at all the salinity
Estuaries and Coasts
Fig. 5 Dispersion plots of the
deseasonalized density (log
(x + 1)) of key copepod species
vrs. the deseasonalized copepod
species alpha diversity (Shannon
index) for each salinity site of the
estuaries of Bilbao and Urdaibai.
Straight lines show the tendency
of the relationships. (a) Brackish
copepod species: Ato, Acartia
tonsa; Oda, Oithona davisae;
Pma, Pseudodiaptomus marinus;
Caq, Calanipeda aquaedulcis;
and Abi, Acartia bifilosa. (b)
Neritic copepod species: Acl,
Acartia clausi; PCPC, PCPCcalanus assemblage; Ona, Oithona
nana; Osi, Oithona similis; and
Ome, Oncaea media
sites under study in both estuaries. In addition, in the estuary
of Bilbao, alpha diversity of zooplankton groups showed
positive relationships with the densities of cirripede larvae,
gastropod larvae, and appendicularians at B35 and with
those of cladocerans and appendicularians at B33 and B34.
Gamma and Beta Diversities
Gamma diversity values and patterns of variation for copepod species and zooplankton groups differed between estuaries (Fig. 7). Copepod gamma diversity was, in general,
slightly higher in the estuary of Urdaibai, and its seasonal
pattern was less variable along the study period in the estuary of Bilbao, where it showed lowest values in late winterearly spring and highest values in autumn. A slight trend of
increase of copepod gamma diversity was observed in both
estuaries over the study period, but the increase of diversity
occurred mainly in late winter-early spring in the estuary of
Bilbao and in autumn in the estuary of Urdaibai. In contrast,
zooplankton gamma diversity was higher in the estuary of
Bilbao than in the estuary of Urdaibai, and the seasonal pattern of zooplankton diversity was similar in the two estuaries, showing lowest values in autumn–winter and highest
values in spring–summer. A clear decrease in zooplankton
gamma diversity was observed from the first (1998–2002)
to the last (2010–2015) period in the estuary of Bilbao, but
not in the estuary of Urdaibai.
Deseasonalized copepod gamma diversity was negatively
related to the deseasonalized density of the neritic species
A. clausi and the NIS A. tonsa in the estuary of Bilbao, but
showed a strong negative relation to that of the brackish
autochthonous species A. bifilosa in the estuary of Urdaibai.
In contrast, it showed a strong positive relationship to the
deseasonalized density of the neritic species O. nana and
O. similis in both estuaries, of O. media in the estuary of
Bilbao, and the PCPC-calanus assemblage in the estuary of
Urdaibai (Fig. 8a). The deseasonalized gamma diversity of
zooplankton groups was strongly and negatively related to
13
Estuaries and Coasts
Fig. 6 Dispersion plots of
deseasonalized density (log
(x + 1)) of key zooplankton
groups vrs. the deseasonalized zooplankton groups alpha
diversity (Shannon index) for
each salinity site of the estuaries
of Bilbao and Urdaibai. Straight
lines show the tendency of the
relationships. Cop, copepods;
Cir, cirripede larvae; Gas, gastropod larvae; Cla, cladocerans;
and App, appendicularians
the deseasonalized density of copepods in both estuaries, but
it was also positively related to the density of cladocerans
and appendicularians in the estuary of Bilbao (Fig. 8b).
Beta diversity (Fig. 7) increased both for copepod species and zooplankton groups from the 1998–2002 period
to the following periods in both estuaries, but the increment was higher in the estuary of Bilbao. However, from
13
2003–2009 to 2010–2015, both beta diversities increased
in the estuary of Bilbao, while they showed a slight
decrease in the estuary of Urdaibai. The seasonal pattern
of beta diversity for copepod species and zooplankton
groups differed between years and periods in both estuaries. However, the most obvious variations of the seasonal
pattern of beta diversity between periods was observed for
Estuaries and Coasts
Fig. 7 Contour plots showing seasonal and interannual variations of the gamma diversity index (Shannon index) (upper panel) and beta diversity
index (Whittaker index) (bottom panel) of the copepod species and zooplankton groups in the estuaries of Bilbao and Urdaibai
copepods in the estuary of Bilbao, where beta diversity
values showed the most marked increase in summer.
Discussion
Overall, results revealed that the NIS copepods detected
during the 18-year-study had a much higher impact on zooplankton community structure and diversity in the estuary
of Bilbao than in the estuary of Urdaibai. This impact was
highest in the uppermost zone and decreased with increasing salinity in both estuaries, being negligible at the highest salinity sites located at the lower estuary. Therefore, our
results agree with other observations in which the lower
salinity habitats of the upper reaches, characterized by a
minimum of native species richness, are the most sensitive to
biological invasions in estuaries (Nehring 2006). However,
more importantly, they showed that the impact of arriving
species may differ largely between estuaries due to a complex interaction of factors, including the history of human
perturbations which may determine the suitability of a system to be colonized by new species.
Changes in Zooplankton Structure
In the estuary of Bilbao, the occurrences of the copepod
NIS A. tonsa and O. davisae, and that of C. aquaedulcis,
and to a lesser extent the occurrences of A. bifilosa and the
13
Estuaries and Coasts
Fig. 8 Dispersion plots (a) of the deseasonalized density (log (x + 1))
of key species vrs. the deseasonalized copepod species gamma diversity (Shannon index) and (b) of the deseasonalized density (log
(x + 1)) of the most abundant zooplankton groups vs. the deseason-
alized zooplankton groups gamma diversity (Shannon index) of the
estuaries of Bilbao and Urdaibai. Abbreviations of copepod species
and zooplankton groups as in Figs. 5 and 6, respectively
NIS P. marinus caused marked changes in the structure
of zooplankton communities throughout the study period,
communities changing most drastically in the uppermost
site. The occurrence of some of these species in other areas
in Europe, such as O. davisae in the Black Sea (Gubanova
et al. 2019) and A. tonsa in ponds of Doñana Natural park
located in the southwest of Spain (Frisch et al. 2006), also
affected the native zooplankton community structure.
While in the lowest salinity habitat, the main mode of
variation (PCA, axis 1) indicated a progressive increase
of zooplankton in the presence of the brackish NIS and A.
bifilosa and C. aquaedulcis, in intermediate salinity waters
of 34, a slight return towards the initial community structure was observed, this denoting a landward increase in the
influence of neritic taxa, to the detriment of the seaward
advance of brackish species. This fact may be related to
the changes in water quality during the study period, as
we can infer from the increase of dissolved oxygen levels (Villate et al. 2013; Iriarte et al. 2016). Aravena et al.
(2009) found that oxygen levels affected the proportion
of A. tonsa to A. clausi densities at intermediate salinities of the estuary of Bilbao, because the density of A.
clausi increased at higher oxygen levels, whereas A. tonsa
showed a competitive advantage over A. clausi under low
oxygen conditions due to its higher tolerance to hypoxic
conditions (Marcus et al. 2004; Richmond et al. 2006).
Some holoplankton and meroplankton groups, mainly
appendicularians and larvae of gastropods and bivalves,
showed a general interannual trend of increase along the
entire estuary, as evidenced by the second main mode of
variation of the zooplankton (PCA, axis 2), which supports
the idea that the improvement of environmental conditions
13
Estuaries and Coasts
had a positive effect on zooplankton density in the estuary
of Bilbao.
In the estuary of Urdaibai, unlike in the estuary of Bilbao,
NIS copepods were not involved in the main changes of the
zooplankton community structure, as shown by their low
contribution to the PCA axis 1, and no clear differences in
the trends of zooplankton change were identified between
salinity habitats. The strong interannual variations observed
were mainly driven by neritic copepods such as the PCPCcalanus assemblage, O. nana and E. acutifrons. This might
be attributable to the stronger hydrodynamics and shallowness of the estuary of Urdaibai which give rise to a lower
water column stability and higher sensitivity to climate factors (Iriarte et al. 2016), as it has been observed also in other
small estuaries of southern Europe (Vieira et al. 2015). The
strong changes in zooplankton observed in 2012 at all the
salinity sites in the present study were already reported for
the outer marine zone of both estuaries and were suggested
to be linked to a hydro-climatic event (Fanjul et al. 2017).
Our results suggest that such event could have affected the
zooplankton structure along the entire estuary and that it had
a smaller effect on the zooplankton of the estuary of Bilbao.
Brackish copepods, mainly A. tonsa and A. bifilosa,
together with some meroplankton groups, were the taxa that
contributed most to the second mode of zooplankton variation in the estuary of Urdaibai. Before the colonization by
A. tonsa and O. davisae, the estuary of Urdaibai, unlike the
estuary of Bilbao, had the typical brackish zooplankton community with a dominant species (A. bifilosa), and the dominance of A. bifilosa seems to have limited both the abundance
(and relative abundance) of the congeneric NIS A. tonsa and
the length of the season in which it is abundant (Villate et al.
2018; Barroeta et al. 2020). As the NIS A. tonsa is functionally similar to the indigenous species A. bifilosa (David
et al. 2007), no novel impact on zooplankton community that
could otherwise cause ecosystem change happened, as found
in other works too (see Doherty-Bone et al. 2019 and references therein). It is interesting to point out that meroplankton groups like gastropod and polychaeta larvae showed a
similar level of contribution to that of the dominant brackish
copepods to the changes in the zooplankton of the estuary of
Urdaibai. In this system, gastropod larvae share salinity habitats with brackish copepods and may become the dominant
taxa in the zooplankton assemblage of the inner estuary in
summer (Villate et al. 1993; Villate 1997).
Changes in Diversity
Spatial Changes in Both Estuaries
Overall, the alpha diversity of both copepod species and zooplankton groups decreased with decreasing salinity from the
mouth to the head over the entire study period in the estuary
of Urdaibai and since the establishment of a dominant brackish assemblage comprised by the NIS copepods in the estuary of Bilbao. This pattern of change in diversity with salinity is in agreement with the relationship between these two
variables depicted in the Remane diagram (Remane 1934)
for the salinity range analyzed in our study and has also
being observed for copepods and zooplankton communities
in other estuaries (e.g., Grindley 1981; Duggan et al. 2008;
Whitfield et al. 2012). Therefore, the higher alpha diversity
obtained in the inner estuary of Bilbao prior to the colonization by the brackish copepod NIS, with values similar to
those measured in the outer estuary, may be considered as an
indicator of impaired brackish estuarine communities, since
the negligible presence of brackish copepods in the estuary of Bilbao during the first period of study (1998–2002)
allowed the occupation of the inner reaches of this estuary
by a lower abundance but higher diversity assemblage of
neritic zooplankton (Uriarte et al. 2016).
Interannual Changes in the Estuary of Bilbao
In the estuary of Bilbao, the main interannual changes in
copepod alpha diversity occurred in the innermost zone
and were mainly explained by A. tonsa and O. davisae
density variations. The strong drop of diversity values
from 2002–2003 to 2004–2005 coincided with the sudden
increase of A. tonsa and to a lesser extent of O. davisae and
the decrease of neritic species such as A. clausi (Barroeta
et al. 2020). A similar case that relates a remarkable decrease
in copepod diversity to a decrease in density of some species
at the same time that other species increased in dominance
was reported for a site in Arcachon Bay (Bay of Biscay) by
Richirt et al. (2019). However, the progressive increase in
diversity that occurred later, with highest values in the last
period (2020–2015) in the estuary of Bilbao, was mainly due
to the arrival and increase in abundance from 2008 to 2010
of C. aquaedulcis and P. marinus (Barroeta et al. 2020).
This is an interesting finding, because it showed that the
previous establishment of NIS that became dominant (A.
tonsa and O. davisae) did not hinder the successful colonization of the inner estuary by other new arriving species,
and suggests that this estuary is able to receive more NIS or
range-expanding species which could contribute to increase
even more the diversity in the future. The progressive colonization of the inner estuary by NIS and C. aquaedulcis had
also an evident effect on the beta diversity, because prior to
the occurrence of NIS in large numbers, the community was
more similar at all salinities due to the dominance of neritic
species along the entire estuary, but the recovery of an estuarine community dominated by brackish species increased
species heterogeneity at the estuarine system level. Dispersion plots showed that A. tonsa contributed considerably to
the changes in copepod gamma diversity in the estuary of
13
Estuaries and Coasts
Bilbao, but that neritic species were even more influential.
Copepod gamma diversity, however, showed much smaller
variations than alpha and beta diversities. In some cases,
although a modification in species numbers or densities
affected the alpha diversity of some sites, gamma diversity
did not change because other sites maintained the species
pool (Bonecker et al. 2013). In our case, the pool of neritic
species in the estuary of Bilbao was much richer in species
than the pool of colonizing brackish NIS copepods plus A.
bifilosa and C. aquaedulcis, which did not affect the structure of the neritic assemblage in the lower estuary.
Seasonal Changes in the Estuary of Bilbao
The seasonal patterns of alpha diversity in zooplankton
groups and copepod species at the inner estuary of Bilbao
were also substantially modified by the progressive copepod
colonization because NIS peaked in summer-autumn and
C. aquaedulcis in spring–summer (Barroeta et al. 2020).
Before the occurrence of NIS, the seasonal pattern of alpha
diversity was similar at all salinities, being the typical seasonal pattern of the neritic community, with low values
during the first part of the year (from January to June) and
an increase during the second part (from June to December), also observed in other temperate coastal regions of the
North Atlantic (Johnson et al. 2011). When A. tonsa and O.
davisae became very abundant and dominant since 2003
(Barroeta et al. 2020), the diversity of copepods decreased
during the second part of the year, in a similar way to
observations in summer in the Uruguayan Solís Grande
estuary (Gómez-Erache et al. 2000) and Doñana Park
(Spain) artificial ponds (Frisch et al. 2006) due to A. tonsa
increases. When A. bifilosa and C. aquaedulcis occurred in
large numbers from 2010 onwards (Barroeta et al. 2020),
the diversity of copepods increased in the first part of the
year, reflecting a more estuarine type of seasonal pattern of
diversity (Soetaert and Van Rijswijk 1993, Primo et al. 2009),
and similar to that found in the inner estuary of Urdaibai.
Seasonal differences in copepods’ gamma diversity diminished over the study period mainly due to the progressive
increase of diversity in the first half of the year from one
period to the next. Copepods’ diversity minima in the first
part of the year in the estuary of Bilbao is attributable to
the strong dominance of A. clausi in late winter-early spring
(Fanjul et al. 2016) and the absence of abundant brackish
copepods in the inner estuary; the increase in diversity in
winter-spring in the entire estuary is attributable to the progressive occupation of the inner estuary by NIS, and finally,
by C. aquaedulcis, which peaks in spring (Barroeta et al.
2020). The seasonal change in copepod beta diversity from
lowest values in summer-autumn during the first period
(1998–2002) to highest values in the same season during
13
the last period (2010–2015) was related to the occupation
of the inner estuary by the thermophilic NIS A. tonsa and
O. davisae, which comprised a brackish community typical
of the warm period, clearly segregated from the species-rich
neritic assemblage within the estuary (Barroeta et al. 2020).
Interannual Changes in the Estuary of Urdaibai
In the estuary of Urdaibai, no clear trends in alpha diversity
and no remarkable changes in the diversity of the inner estuary were observed after the arrival and settlement of A. tonsa,
this denoting that the zooplankton community was resilient to
the invasion-induced disruption in terms of changes in diversity. Regarding gamma diversity, the only copepod NIS that
successfully established in this estuary, i.e., A. tonsa, clearly
made a smaller contribution to the changes in diversity than
the congeneric autochthonous brackish species A. bifilosa.
However, an increase in beta diversity during the summerautumn period was observed in the estuary of Urdaibai after
the occurrence of A. tonsa, whose presence in the estuary
was limited to the warm season (Barroeta et al. 2020). Such
increase in taxa heterogeneity was in agreement with the
observed spatial segregation of the population of A. bifilosa,
which was displaced seaward after the colonization of the
inner estuary by A. tonsa (Villate et al. 2018). The seasonal
and spatial segregation of these two congeneric species has
also been reported in other European estuaries (Baretta and
Malschaert 1988; Soetaert and Van Rijswijk 1993; David
et al. 2007).
Seasonal Changes in the Estuary of Urdaibai
In the estuary of Urdaibai, the observed decrease in alpha
diversity in spring in waters of lower than 33 salinity was
associated to the advance of the annual peak of A. bifilosa
from summer to late spring after the establishment of the congeneric NIS which had its annual maxima in summer (Villate
et al. 2018; Barroeta et al. 2020). In the Westerschelde estuary,
the occurrence of A. tonsa is also limited in time and space,
occupying the upstream area in summer, this also causing A.
bifilosa (a winter-spring species in this region) to be absent
more upstream in summer, affecting the seasonal pattern of A.
bifilosa and the copepod community diversity pattern (Soetaert
and Van Rijswijk 1993). Overall, all our results revealed that
A. bifilosa is the key species that has driven all the changes in
zooplankton diversity in the estuary of Urdaibai, although its
effect on the increase and seasonal variations of gamma and
beta diversities over the study period were attributable to its
seasonal and spatial displacements induced by the colonization
of the inner estuary by A. tonsa.
Estuaries and Coasts
The Role of Diversity and Community Structure
Prior to the arrival of the New Copepod Species
in the Differential Impact of These Species
in the Two Estuaries
The diversity of copepod species and zooplankton groups
was higher in the inner zone of the estuary of Bilbao
than in the inner zone of the estuary of Urdaibai in the
period previous to the arrival and establishment of the
new copepod species in the inner zone of both estuaries.
The colonization success and the resulting impact on the
zooplankton structure and diversity of the arriving species were, however, much higher in the first estuary than
in the second one. These findings apparently go against
the Elton’s hypothesis (Elton 1958), which suggests that
resident diversity is an important determinant of invasion
success because the high diversity increases the competitive environment of communities and makes those environments more difficult to be invaded (Naeem et al. 2000).
In our case, however, the higher diversity of both copepod
species and zooplankton groups in the inner estuary of
Bilbao than in the inner estuary of Urdaibai could not be
related to higher ecological resistance to invasions in the
sense of the Elton’s hypothesis, since the initial diversity
measured in the inner estuary of Bilbao corresponded to a
lower abundance but higher diversity assemblage of neritic
copepod species and zooplankton groups that penetrated
the inner estuary when the environmental improvement
due to cleaning actions in the estuary allowed so (Uriarte
et al. 2016). However, such assemblage of neritic species represents a post-disturbance community unable to
compete with brackish invaders for the low salinity niches
(Kneitel and Perrault 2006). If we focus on the brackish
component of the zooplankton, the initial community of
the inner zone of the estuary of Bilbao was less complex
and diverse than that of the inner estuary of Urdaibai, the
latter being dominated by the brackish species A. bifilosa
(Barroeta et al. 2020), and therefore, it may be inferred
that the lack of true estuarine competitors rather than the
presence of a diverse neritic community determined the
invasion success in the estuary. As the lack of typically
brackish copepod species in the initial period in the estuary of Bilbao is attributable to the previous environmental
deterioration of the inner estuary (Uriarte et al. 2016), our
results are consistent with the refined version of the Elton’s
hypothesis which recognizes that habitat disturbances may
facilitate invasions (Hobbs and Huenneke 1992; Reznick
et al. 2020).
Acknowledgements The authors thank the WGEUROBUS of the
International Council for the Exploration of the Sea (ICES) for facilitating this research. They also thank the High Technical School of
Navigation of the Faculty of Engineering in Bilbao (UPV/EHU) for
the facilities offered to carry out the field work.
Author Contribution All authors contributed to the study conception
and design. Material preparation, data collection, and analysis were
performed by Ziortza Barroeta, Fernando Villate, Ibon Uriarte, and
Arantza Iriarte. The first draft of the manuscript was written by Ziortza
Barroeta, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Funding Open Access funding provided thanks to the CRUE-CSIC
agreement with Springer Nature. This work was supported by the University of the Basque Country (UPV/EHU) (UPV/EHU, GIU19/059)
and the Basque Government (PIBA2020-1-0028 & IT1723-22) and
through a grant to Z. Barroeta to carry out her PhD (UPV/EHUn Ikertzaileak Prestatzeko Kontratazio Deialdia 2016).
Data Availability The datasets generated during and/or analyzed during the current study are available on request from the corresponding
author under specific conditions of use.
Code Availability The code generated during and/or analyzed during
the current study is available from the corresponding author on reasonable request.
Declarations
Conflict of Interest The authors declare no competing interests.
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long
as you give appropriate credit to the original author(s) and the source,
provide a link to the Creative Commons licence, and indicate if changes
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included in the article's Creative Commons licence, unless indicated
otherwise in a credit line to the material. If material is not included in
the article's Creative Commons licence and your intended use is not
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copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
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