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Zooplankton communities in twocontrasting Basque estuaries
(19992001): reporting changesassociated with ecosystem health
A. ALBAINA1*, F. VILLATE1 AND I. URIARTE2
1
LABORATORY OF ECOLOGY, DEPARTMENT OF PLANT BIOLOGY AND ECOLOGY, UNIVERSITY OF THE BASQUE COUNTRY, BILBAO 644 E-48008, SPAIN AND2
LABORATORY OF ECOLOGY, DEPARTMENT OF PLANT BIOLOGY AND ECOLOGY, FACULTY OF PHARMACY, UNIVERSITY OF THE BASQUE COUNTRY, VITORIA-GASTEIZ
E-01006, SPAIN
PRESENT ADDRESS: MOLECULAR ECOLOGY AND FISHERIES GENETICS LABORATORY, SCHOOL OF BIOLOGICAL SCIENCES, UNIVERSITY OF WALES, BANGOR LL57
2UW, UK
*CORRESPONDING AUTHOR: aitoralbaina@hotmail.com
Received February 17, 2009; accepted in principle March 17, 2009; accepted for publication March 23, 2009; published online 10 April, 2009
Corresponding editor: Roger Harris
This study is a part of the zooplankton monitoring program carried out in the euhaline region of
the estuaries of Bilbao and Urdaibai (Basque coast, Bay of Biscay), and analyses between-
estuaries differences in zooplankton spatial and temporal patterns in relation to environmental con-
ditions between July 1999 and May 2001. Environmental variables measured were water temp-
erature, dissolved oxygen saturation (DOS), Secchi disk depth (SDD) and chlorophyll a.
Relationships between zooplankton community and environmental variables were analysed using
canonical correspondence analysis; between-estuaries differences in environmental conditions and
distribution of zooplankton taxa in relation to salinity were tested using MannWhitney U-test.
Spatial differentiation of the zooplankton community was higher in the estuary of Bilbao, with therelative abundance of most of the taxa decreasing more pronouncedly towards the upstream estuary
than in the Urdaibai related to significantly lower values of DOS and SDD, reflecting the higher
degree of pollution, in the Bilbao estuary. However, the successful establishment of the Acartia dis-
caudata and A. margalefi populations, and the first records of another Acartia species, Calanipeda
aquaedulcis and Eurytemora affinis in the Bilbao estuary, along with the increasing similarity
between zooplankton assemblages of the Bilbao and Urdaibai estuaries in relation to the period
19971999, represent a new step in the recovery of the zooplankton community in the estuary of
Bilbao responding to the improvement of water quality.
I N T R O D U C T I O N
The estuary of Bilbao was originally the most exten-
sive estuarine area on the Cantabrian coast of north-
ern Spain, but the early industrial development of the
city of Bilbao in the mid-19th century dramatically
modified its natural features to form a navigable tidal
channel. Today the estuary is a man-modified system
which bears little resemblance to the original estuary,
and has received during the last 150 years high
amounts of wastes from many sources (mineral slui-cing, industrial wastes and urban effluents), which sig-
nificantly degraded the environmental quality of water
and sediments to become one of the most polluted
estuaries in Europe (Cearreta e t al ., 2000). On the
other side, the estuary of Urdaibai was declared a
Biosphere Reserve by UNESCO in 1984 and has a
much lower level of pollution (Borja et al ., 2000;
Bartolome et al., 2006).
doi:10.1093/plankt/fbp025, available online at www.plankt.oxfordjournals.org
# The Author 2009. Published by Oxford University Press. All rights reserved. For permissions, please email: journals.permissions@oxfordjournals.org
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Zooplankton is recommended as a bioindicator for
estuarine conditions because zooplankton species have
the potential to remain in the water body of appropriate
salinity (Wilson, 1994) and is considered, by the United
States Environmental Protection Agency (Gibson et al.,
2000) as an under-development indicator in order to be
incorporated in environmental management decision-making. Although several studies have reported the
decrease of zooplankton when exposed to hypoxic/
anoxic conditions related to polluted systems (e.g.
Siokou-Frangou and Papathanassiou, 1991; Soetaert
and Van Rijswijk, 1993), studies on the impact of pol-
lution on estuarine zooplankton are scarce. In this
sense, the zooplankton of the estuaries of Bilbao and
Urdaibai for the period March 1997May 1999 have
been recently analyzed to discern the response of zoo-
plankton populations to contrasting levels of pollution
(Uriarte and Villate, 2004, 2005), concluding that pol-
lution causes quantitative rather than qualitative
changes in the neritic zooplankton communities that
penetrate the estuaries. In the present study, we ana-
lyzed the zooplankton of both estuaries for the period
from July 1999 to May 2001, looking for changes in the
zooplankton community; special attention is devoted to
the copepods inhabiting the upstream estuary, as the
ongoing improvement of the water quality in these
waters is expected to impact their populations.
M E T H O D
Study area
The estuaries of Bilbao and Urdaibai are situated on the
Basque coast (respectively, 438230N 38W and 438200N
38W; Fig. 1). Therefore, both experience a similar
climate and tidal regime (macro-mesotidal), but differ
largely in their geomorphology and pollution level. The
estuary of Bilbao is a narrow (50145 m) and 29 m
depth channel of15-km long, which crosses urban and
industrial settlements and drains into a wide coastal
embayment (Abra harbour). During the past century,
this system received considerable amounts of untreated
waste water polluting its waters and sediments, although
since the 1980s the decay of industrial activities and theonset of a new sewage water treatment program is pro-
gressively improving the water quality in the still polluted
estuary (review in Borja and Collins, 2004 and references
therein; Bartolomeet al., 2006). Apart from this, river dis-
charge and stratification are higher in the estuary of
Bilbao than in the Urdaibai estuary. In contrast, the
estuary of Urdaibai (also called Gernika and Mundaka
in literature) is 13-km long, shallow (2.5 m mean
depth) is a less perturbed a system experiencing a lower
degree of pollution (e.g. Borja et al., 2000; Bartolome
et al., 2006); as a result of the lower river discharge and
stratification, tidal mixing and exchange are higher in
the estuary of Urdaibai than in the Bilbao estuary.
Monitoring strategy
Sampling was carried out monthly between July 1999
and May 2001 in the euhaline region of the estuaries,
around high water in consecutive days, except in March
2000 in Bilbao due to adverse weather. Zooplankton
samples were collected at four salinity sites, water
bodies of around 35, 34, 33 and 30, using a 200 mmmesh plankton net (mouth diameter: 0.5 m) equipped
with a flowmeter. Nets were towed horizontally between
3 and 5 m depth to avoid the low-salinity surface layer
and the pycnocline at stratified sites, and to avoid proxi-
mity to the bottom in shallower zones; tow duration
was short (around 3 min) to prevent mesh clogging. Net
samples were preserved immediately after collection
with 4% borax buffered formalin seawater solution.
Salinity and water temperature were measured with a
WTW LF 197 thermo-salinometer and dissolved
oxygen saturation (DOS) with an YSI 55 oxymeter
while water transparency was estimated by Secchi disk
depth (SDD); chlorophyll-a (Chl-a) was measured
according to Lorenzen (Lorenzen, 1967). Data on river
discharge were provided by the Hydrometeorology
Service of the Regional Council of Bizkaia.
The qualitative and quantitative analysis of zooplank-
ton was carried out under a stereo-microscope.Identification was made to species or genus level in the
majority of the holoplanktonic groups, and to general
categories for meroplankton (Table I) following mainly
Rose (Rose, 1933) and the ICES Identification Leaflets
for Plankton (http://www.ices.dk/products/fiche/
Plankton/START.PDF). In each sample, a minimum of
100 individuals of the most abundant taxa were
counted before finishing sub-sampling; if not possible,
the whole sample was identified. Due to the difficulty of
their classification, the copepodite stages of the genus
Acartia, and the ones of the genera Paracalanus,
Clausocalanus, Pseudocalanus and Ctenocalanus were
grouped, respectively, in the categories Acartia copepo-dites and P-Calanus; so, we considered separately only
the adult specimens of those species.
Statistical analysis
We excluded for the statistical analysis the 35 salinity
site as it was impossible to sample consistently; in 4
months out of 22 in the Bilbao estuary, and in 8 out of
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Table I: Taxonomic list
Bilbao abundance (ind. m23)
Bilbao (%)
Urdaibai abundance (ind. m23)
Urdaibai (%)
Mean Maximum M inimum Mean Mean Maximum M inimum M ean CODE
Noctiluca scintillans 46.01 922.66 0.00 1.93 0.46 6.30 0.00 0.04 NOCTI
Foraminifera 0.05 1.06 0.00 0.01 0.57 5.24 0.00 0.10
Cnidaria (others) 5.27 22.92 0.00 0.52 4.63 30.04 0.00 0.35 CNIDASiphonophora 13.86 109.38 0.00 1.18 9.04 56.76 0.00 0.59 SIPHO
Gastropod veliger 11.19 52.40 0.00 1.72 262.69 4590.89 1.39 5.69 GAVEL
Bivalve veliger 7.03 39.03 0.00 0.84 7.50 46.65 0.00 0.57 BIVEL
Polychaeta (larvae) 34.45 107.59 2.01 8.41 21.65 98.34 0.00 1.82 POLYC
Polychaeta (adults) 0.17 1.20 0.00 0.02 0.07 0.73 0.00 0.01
Bryozoa (Cyphonautes larvae) 0.38 6.40 0.00 0.05 2.67 15.56 0.00 0.38
Penilia avirostris 6.20 86.62 0.00 0.53 10.48 153.88 0.00 0.58 PENAV
Podonspp. 17.01 80.69 0.00 1.41 12.02 215.72 0.00 0.40 PODON
Evadne spinifera 3.62 65.44 0.00 0.35 4.05 45.27 0.00 0.28
Evadne nordmanni 23.09 197.99 0.00 1.50 33.40 397.09 0.00 2.06 EVNOR
Evadne tergestina 0.04 0.92 0.00 0.00 0.02 0.43 0.00 0.00
Cladocera (Riverine species) 0.13 2.32 0.00 0.15 0.00 0.00 0.00 0.00
Ostracoda 0.06 0.40 0.00 0.05 2.29 16.49 0.00 0.22
Calanidae (others) 1.45 14.74 0.00 0.08 1.42 18.09 0.00 0.07
Eucalanusspp. 0.19 4.17 0.00 0.02 0.25 4.18 0.00 0.02
Rhincalanusspp. 0.12 1.80 0.00 0.01 0.00 0.00 0.00 0.00
Ischnocalanusspp. 0.00 0.00 0.00 0.00 0.31 5.42 0.00 0.02Calocalanusspp. 0.96 14.44 0.00 0.05 2.25 45.16 0.00 0.18
Paracalanus parvus 45.88 279.38 0.00 6.31 88.23 618.94 1.08 5.55 PARAC
Clausocalanusspp. 0.21 1.44 0.00 0.06 4.23 46.00 0.00 0.33
Pseudocalanus elongatus 0.65 4.80 0.00 0.05 0.24 4.83 0.00 0.01
Ctenocalanus vanus 0.00 0.00 0.00 0.00 0.18 2.66 0.00 0.01
P-Calanus 67.84 340.05 0.23 9.37 110.04 630.41 5.87 9.21 P-CAL
Temora longicornis 1.40 9.58 0.00 0.08 33.03 750.32 0.00 0.41
Temora stylifera 12.01 123.90 0.00 1.90 30.53 205.24 0.00 2.66 TEMST
Eurytemora affinis 0.00 0.06 0.00 0.00 0.00 0.00 0.00 0.00
Centropagesspp. 7.54 38.24 0.00 0.53 16.52 97.59 0.00 1.03 CENTR
Calanipeda aquaedulcis 0.01 0.26 0.00 0.00 0.05 0.71 0.00 0.01
Candaciaspp. 0.05 0.70 0.00 0.01 0.70 14.16 0.00 0.01
Acartia clausi 169.96 1023.70 0.34 8.29 116.59 1 781.06 0.00 4.71 ACCLA
Acartia discaudata 1.25 14.84 0.00 0.18 0.00 0.00 0.00 0.00
Acartia margalefi 1.10 10.43 0.00 0.09 0.00 0.00 0.00 0.00
Acartia bifilosa 0.00 0.00 0.00 0.00 898.94 19 089.68 0.00 12.58 ACBIF
Acartiasp. 0.01 0.21 0.00 0.00 0.00 0.00 0.00 0.00Acartiacopepodites 454.03 6192.22 0.55 13.90 393.06 3737.15 0.53 13.73 ACCOP
Oithona plumifera 1.88 9.69 0.00 0.51 5.00 35.18 0.00 0.73 OITPL
Oithona similis 25.18 127.33 0.00 2.54 88.10 639.87 0.00 8.71 OITSI
Oithona nana 31.31 267.70 0.00 6.07 32.03 286.32 0.00 2.19 OITNA
Other cyclopoids 1.71 14.34 0.00 2.94 0.05 0.63 0.00 0.01 CYCLO
Oncaeaspp. 3.28 25.06 0.00 0.49 29.85 215.47 0.00 4.42 ONCAE
Corycaeusspp. 0.77 2.88 0.00 0.23 5.01 27.75 0.00 0.46
Clytemnestraspp. 0.00 0.00 0.00 0.00 0.07 1.06 0.00 0.02
Euterpina acutifrons 5.81 29.02 0.00 1.18 33.01 392.20 0.00 2.12 EUTER
Microsetellaspp. 0.00 0.08 0.00 0.00 0.07 1.34 0.00 0.02
Other harpacticoids 0.99 2.96 0.00 0.31 6.10 36.67 0.00 0.69 HARPA
Caligoidea 0.07 0.83 0.00 0.02 0.05 0.59 0.00 0.01
Copepoda nauplius 5.11 19.97 0.00 0.66 24.40 80.73 0.00 1.89 COPNA
Cirripedia larvae 227.86 1160.80 0.40 18.93 173.67 1115.90 0.00 11.05 CIRRI
Amphipoda 0.02 0.46 0.00 0.02 0.01 0.14 0.00 0.00
Isopoda (Paragnathia) larvae 0.07 0.59 0.00 0.02 5.98 36.83 0.00 0.52 PARAG
Isopoda (Epicarida) larvae 0.25 2.60 0.00 0.02 2.22 18.46 0.00 0.17Cumacea 0.00 0.00 0.00 0.00 0.24 2.66 0.00 0.01
Decapod larvae 2.11 11.31 0.00 0.33 17.17 288.83 0.00 0.49
Mysidacea 0.02 0.35 0.00 0.01 0.05 0.88 0.00 0.01
Euphausiacea nauplius 0.00 0.00 0.00 0.00 0.08 1.71 0.00 0.01
Sagittaspp. 3.00 15.55 0.00 0.70 2.36 10.38 0.00 0.25 SAGIT
Echinodermata larvae 1.08 12.80 0.00 0.10 0.34 4.18 0.00 0.03
Fritillariaspp. 3.85 43.50 0.00 0.47 2.73 51.58 0.00 0.18
Oikopleuraspp. 54.96 287.17 0.04 4.43 28.20 255.13 0.00 1.87 OIKOP
Doliolumspp. 0.90 4.91 0.00 0.10 4.04 57.01 0.00 0.33
Continued
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evaluate the significant variables under analysis by
means of Monte Carlo test (999 permutations).
Differences of environmental variables and zooplankton
taxa between estuaries at each salinity site were made
using MannWhitney U-test for relative abundances
(%) using the same taxa as in the CCA; relative abun-
dances were used in order to compare the organization
of the zooplankton community within the estuaries.
Surfer 8.0 (Golden Software) was used for the spatio-
temporal representation of the results.
R E S U L T S
Environmental variables
The annual cycle of water temperature and river flow
(represented as the accumulated daily flow for the 3
days previous to the sampling date) for the two estuaries
(Fig. 2A) showed the highest flow values matching with
the autumn-winter period while the dry season corre-
sponded to the summer where a peak of Chl-a devel-oped (Fig. 2B; average summer values of 9.4 and
2.2 mg L21 in the 3034 salinity range for, respectively,the Bilbao and Urdaibai estuaries). The spatial distri-
bution of Chl-a showed similar values along the salinity
gradient in the estuary of Bilbao and a decrease
towards the downstream estuary in the Urdaibai estur-
ary, with the higher values being attained in the Bilbao
estuary. The spatial pattern for temperature showed
more extreme temperatures in the upstream estuary in
both systems, as expected by the reduction in volume of
water towards the river. Both the SDD and the DOS
showed significant differences between both estuaries
salinity sites, with the lowest values attained in theestuary of Bilbao (Table II). While the minimum SDD
values were measured in the upstream estuary in both
ecosystems (average values of 0.9 and 1.8 m in the 30
salinity water mass for, respectively, the Bilbao and
Urdaibai estuaries) without presenting any clear seaso-
nal trend, the minimum DOS values were reported in
the upstream estuary during the summer-autumn
period (Fig. 2B; average summer-autumn values of 25
and 70.5% in the 30 salinity water mass for, respect-
ively, the Bilbao and Urdaibai estuaries).
Zooplankton community
Copepods dominated the zooplankton assemblage
during most of the year (Fig. 3A) Acartia clausi,
Paracalanus parvus and Oithona nana being the dominant
species in the Bilbao estuary, while in the Urdaibai,
dominants were Acartia bifilosa, A. clausi, P. parvus, Oithona
similis and Oncaea spp. (Table I). In the Bilbao estuary,
maximum copepod abundances were reached during
the spring followed by a secondary peak in summer,
whereas minimum levels were attained in winter with
values decreasing towards the upstream estuary during
the whole period studied; the temporal pattern was the
same in the Urdaibai estuary, showing similar values
along the salinity gradient, except from a maximum in
the summer of 1999 in the upstream estuary (Fig. 3A).
Highest species diversity values for the copepod com-
munity were found in the downstream estuary mainly
in autumn (Fig. 3B).The environment-taxa biplots of the CCA for both
estuaries are shown in Fig. 4; the cumulative explained
variance for the species environmental relationship
taking the first two axes into account was 85.6 and
83.4% for the Bilbao and Urdaibai estuaries, respect-
ively. While in the Bilbao estuary, the environmental
variables explaining most of the variance in each axis
were water temperature (93.8%) for the first axis, and
salinity (41.2%) and DOS (38.8%) for the second one;
in the Urdaibai estuary, salinity (84.4%) and DOS
(78.3%), and water temperature (49.6%), explained
most of the variance along, respectively, the first and
second axes. The CCA clearly differentiated Noctilucascintillans, Penilia avirostris and Temora stylifera as the taxa
more associated with high salinity waters in both estu-
aries; while Polychaete larvae and other cyclopoid
copepod categories comprised the taxa more restricted
to lower salinity waters in the estuary of Bilbao, A. bifi-
losa and Gastropod larvae prevailed in that water body
in the Urdaibai estuary. The CCA also showed a com-
parable temporal cycle in both estuaries with A. clausi
Table I: Continued
Ascidian larvae 0.09 0.71 0.00 0.02 0.02 0.40 0.00 0.00
Teleostei eggs 2.77 29.89 0.00 0.21 1.53 7.97 0.00 0.12
Teleostei larvae 0.62 4.73 0.00 0.07 0.36 1.84 0.00 0.03
Copepods (total) 840.74 7885.46 16.68 55.87 1920.30 23 206.10 66.00 71.82
Zooplankton (total ) 1306.92 8362.12 22.97 100.00 2530.84 28 657.58 81.89 100.00
Taxonomic list with mean, maximum and minimum values for abundance (ind. m23
) and mean values for relative abundance (%) of each taxon in both
Bilbao and Urdaibai estuaries for the 3034 salinity sites. Column CODE shows the codes used in the canonical correspondence analysis (CCA).
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Fig. 2. (A) The annual cycle of water temperature (C, average value for the 30 34 salinity sites) (continuous line; left axis) and the river flow,expressed as the accumulated daily flow (m3 s21) for the 3 days previous to the sampling data (line with squares; right axis), for the estuaries ofBilbao and Urdaibai (left and right graph, respectively). March 2000 in the estuary of Bilbao was not sampled; (B) Spatial distributions ofenvironmental variables along the salinity gradient (bottom axis; 30 35 salinity sites) for the 2-year period (left axis; from July 1999 to May2001); from left to right: water temperature (8C), dissolved oxygen saturation (DOS; %), Secchi disk depth (SDD; m) and Chlorophyll-a (Chl-a;mg L21), in both Bilbao and Urdaibai estuaries (upper and bottom graphs, respectively). All scales superimposed.
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and O. similis being the main taxa in cold waters,
whereas N. scintillans, P. avirostris and T. stylifera rep-
resented the warm water community.
Between-estuary differences by salinity site (Mann
Whitney U-test; Table III) showed that the relative
abundances of Polychaete larvae, A. clausi, the other
cyclopoids category Cirripedia larvae and Oikopleura
spp. were significantly higher in the estuary of Bilbao,
mainly at low salinities. On the other hand, the relative
abundances of Gastropod veligers, A. bifilosa, Acartia
copepodites, O. similis, Oncaea spp., the other harp-
acticoids category, nauplii of Copepoda, Isopoda
Paragnathia and total copepods were significantly
higher in the estuary of Urdaibai, with the significance
increasing towards lower salinities, except for Oncaea
spp. and the other harpacticoids category. Although not
significantly different, copepod diversity was higher inthe estuary of Urdaibai than in the Bilbao esturary for
the whole salinity range.
In both estuaries, the bulk of zooplankton population
was mainly comprised of Acartia populations (Fig. 5A).
While in the estuary of Urdaibai, the Acartia population
was comprised of A. bifilosa in the upstream estuary and
the neriticA.clausiin the downstream estuary; the estuary
of Bilbao was dominated by A.clausi, withA.discaudata, A.
margalefiand another unidentified Acartia(Acartia sp.) occur-
ring in low abundance at the 3334 salinity sites during
the cold water months (Fig. 5). Apart from this new
Acartia species record, the copepod Calanipeda aquaedulcis,
common in the upstream estuary of Urdaibai, was firstreported in March and May 2001 in the estuary of
Bilbao; along with this, Eurytemora affinis was recorded
once in the estuary of Bilbao in December 2000.
While A. clausi peaked in both estuaries during
the spring, A. bifilosa had a bimodal distribution in
the Urdaibai estuary, with a main peak in summer
1999, and a secondary one in both autumn periods
(Fig. 5).
D I S C U S S I O N
The differences in water quality between the estuaries
of Bilbao and Urdaibai during the study period are
reflected by the highly significant difference in both theSDD and DOS. Both measures showed the lowest
values in the estuary of Bilbao corresponding to the
highest eutrophication level (Borja and Collins, 2004);
in this sense, the severe hypoxia present in the upstream
estuary of Bilbao is attributed to the high biological
oxygen demand by heterotrophic bacterial activity
(Iriarte et al., 1998). While the minimum SDD values
were attained in the upstream estuary in both ecosys-
tems without showing any clear seasonal trend, the
minimum DOS values were reported in the upstream
estuary during the summer-autumn period correspond-
ing to the highest water temperature and Chl-a; more-
over, the higher Chl-a values attained in waters of theestuary of Bilbao is related to nutrient enrichment from
anthropogenic sources (Agirre, 2000; Borja and Collins,
2004). This higher degree of pollution in the upstream
estuary of Bilbao is reflected in the zooplankton pattern
by showing reduced abundance and diversity values
when compared with Urdaibai estuary waters.
The annual cycle for temperature, along with that of
zooplankton abundance and the seasonal patterns of
zooplankton taxa, was similar in both estuaries as
expected from the close geographical location of both
systems, and followed the same pattern reported pre-
viously for these estuaries (e.g. Villate, 1997; Uriarteand Villate, 2004). While the CCA showed comparable
taxonomic assemblages in the temporal context, driven
by water temperature; the spatial assemblages, driven
by salinity and DOS gradients, differed between estu-
aries for the upstream assemblage, which was character-
ized by A. bifilosa and gastropod larvae in the Urdaibai
estuary, and by polychaete larvae, freshwater/estuarine
cyclopoids and meiobenthic harpacticoids in the Bilbao
Table II: Environmental variable Mann Whitney U test
30 33 34
Bilbao Urdaibai
PP-value
Bilbao Urdaibai
PP-value
Bilbao Urdaibai
PP-valueAverage (SD) Average (SD) Average (SD) Average (SD) Average (SD) Average (SD)
Water temp. (8C) 16.53 (3.45) 16.45 (3.72) NS 16.28 (3.01) 15.95 (3.37) NS 16.49 (2.95) 16.3 (3.22) NS
DOS (%) 27.87 (18.09) 83.74 (10.89) *** 57.64 (17.17) 93.49 (8.45) *** 81.72 (14.72) 94.84 (8.61) *SDD (m) 0.93 (0.24) 1.92 (0.55) *** 1.03 (0.34) 2.53 (0.7) *** 1.05 (0.44) 3 (0.83) ***
Chl-a(mg L21) 4.18 (4.66) 2.45 (1.74) NS 1.78 (1.86) 1.5 (0.92) NS 3.86 (4.26) 1.06 (0.58) NS
Mean values and range of variation (standard deviation (SD) in brackets) for environmental variables at each salinity site of the estuaries of Bilbao and
Urdaibai, along with the results of MannWhitney U-test for the differences between estuaries at each salinity site. Water temperature (8C), dissolved
oxygen saturation (DOS; %), Secchi disk depth (SDD; m) and chlorophyll-a(mg L21). The 35 salinity site was not taken into account for the statistical
analysis.
NS, not significant.
***P, 0.001, **P, 0.01, *P, 0.05.
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estuary. The results of Mann Whitney U-tests showed
the impact of the distinct degree of pollution over the
relative abundance of taxa. In this sense, although themajority of species observed in both estuaries were
neritic Bay of Biscay species (Albaina and Irigoien,
2007), and their relative abundances decreased towards
the upstream estuary as expected, this decrease was sig-
nificantly more pronounced in the estuary of Bilbao
(Table III); this was related to the minimum values for
DOS and SDD caused by the higher degree of pol-
lution. Looking at the response of taxa to pollution, two
patterns are evident: pollution-sensitive taxa decreasing
in relative abundance towards the upstream estuary of
Bilbao, and pollution-tolerant ones increasing their rela-
tive abundance in those waters. Among the latter ones,
the main taxa were the opportunist polychaete larvae
(mainly spionids) and A. clausi, with reported, respect-
ively, high tolerance to oxygen deficits (Frietzsche andvon Oertzen, 1995), and a well-known capacity to
develop in eutrophic and polluted areas (Arfi et al .,
1981; Gaudy, 1985; Regner, 1987; Siokou-Frangou and
Papathanassiou, 1991; Zaitsev, 1992). On the other
hand, the total copepods category and most of the
identified copepod taxa showed lower presence in the
upstream estuary of Bilbao as explained by the general
low tolerance of copepods to hypoxia (e.g. Roman et al.,
1993). However, it has to be taken into account that
some meroplanktonic taxa are less useful for comparing
the pollution impact between both estuaries, as it is dif-
ficult to disentangle this from the response to differences
in the substrate the adults inhabit; this is the case of the
Cirripedia larvae category, comprising the nauplius and
cypris stages, with higher presence in waters of the
Bilbao estuary likely due to the large expanse of interti-
dal hard substrate in this estuary.
Changes in the zooplankton community
To look at the temporal evolution of water quality and
the zooplankton response to contrasting pollution level,
we compare the results of the present study with those
obtained for the period March 1997May 1999
(Uriarte and Villate, 2004, 2005), taking into accountonly the categories analyzed for both periods (both
environmental variables and zooplankton taxa), as
shown in Table IV. To obtain a reliable comparison,
we had to recalculate our MannWhitney U-test
results for the copepod species so as to show relative
abundance of these against total copepod abundance
as in Uriarte and Villate (Uriarte and Villat, 2005);
apart from these, the rest of the categories were com-
parable (see legend for further information).
Comparisons of dissolved oxygen values revealed a
noticeable improvement in waters of .33 salinity in
the Bilbao estuary; while oxygen values in the Bilbao
estuary at 34 salinity sites were significantly lower thanthose of Urdaibai estuary during March 1997 May
1999, attaining a P, 0.001 value, this changed to a
P, 0.05 value for the period July 1999May 2001
(Table IV). Improvements in the ecosystem health of
the Bilbao estuary have been reported recently (review
in Borja and Collins, 2004 and references therein), and
are supported by the present results on zooplankton
similarity between both estuaries communities. Among
Fig. 3. Spatial distributions along the salinity gradient (bottom axis;3035 salinity sites) for the 2-year period (left axis; from July 1999 toMay 2001) of (A) total zooplankton abundance (left graph; ind. m23)and total copepod abundance (middle graph; ind. m23) and (B)Simpsons diversity index (S) values for the copepod community (rightgraph; no units) in both Bilbao and Urdaibai estuaries (upper andbottom graphs, respectively). All scales superimposed.
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Fig. 4. Canonical correspondence analysis (CCA) biplot for zooplankton taxa abundance and environmental variables for (A) estuary of Bilbaoand (B) estuary of Urdaibai. Only taxa that conform more than 0.5% of the zooplankton community abundance were taken into account(species code as in Table I). CCA identifies environmental variables that explain directions of variance in the species data along one or moreaxes; in this case only the first two axes are shown. CCA included five environmental variables: water temperature (Water Temp.), salinity,dissolved oxygen saturation (DOS), Secchi disk depth (SDD) and Chlorophyll-a (Chl-a). None of the data were weighted. The 35 salinity site wasnot taken into account for the statistical analysis.
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holoplanktonic taxa, seven of the tests reduced the sig-
nificance of between-estuaries differences between the
19971999 period and the present one, while only
three showed increased differences. The reduction of
differences was more evident towards 34 salinity
waters, and was related to the improvement of DOS
values in those waters when comparing both periods.
This sense of recovery, from the downstream estuary to
the upstream one, is related to the higher degree of
dilution of contaminants and oxygenation enhance-ment due to mixing with surrounding neritic waters,
and to higher distance to the contaminant sources,
mainly located in the upstream estuary. The reduction
of differences between the relative abundance of many
taxa in the Bilbao and Urdaibai estuaries was mainly
accounted for by the increase of the relative abun-
dance of pollutant-sensitive taxa in the estuary of
Bilbao, while they remained stable in the Urdaibai
estuary. To illustrate this, the relative abundance ofEuterpina acutifrons, a species with reported sensitivity to
pollution in North sea estuaries (van Damme et al .,
1984), in the copepod community of the Bilbao
estuary, shifted from around 1% in the study of Uriarte
and Villate (Uriarte and Villate, 2005) ( period 1997
1999) to 2% in the present one (19992001) at the 33
and 34 salinity sites, while in the Urdaibai estuary, it
remained around 3.5% for both periods; because of
this, between-estuaries differences for E. acutifrons weresignificant in the 33 and 34 salinity sites in the 1997
1999 period, and resulted in non-significance in the
19992001 one. Present results suggest that the recov-
ery of the zooplankton community is progressing
towards the upstream estuary as DOS values increase.
This is also supported by the occurrence in the estuary
of Bilbao of several copepod species not recorded
previously.
Table III: Zooplankton community Mann Whitney U test
30 33 34
CODE
Bilbao Urdaibai
PP-value
Bilbao Urdaibai
PP-value
Bilbao Urdaibai
PP-valueAverage (SD) Average (SD) Average (SD) Average (SD) Average (SD) Average (SD)
NOCTI 0.27 (0.48) 0 (0) NS 0.02 (0.03) 0.03 (0.05) NS 3.66 (6.48) 0.11 (0.2) NS
CNIDA 0.37 (0.43) 0.25 (0.32) NS 0.5 (0.42) 0.53 (0.44) NS 0.6 (0.4) 0.6 (0.64) NSSIPHO 0.54 (0.80) 0.48 (0.66) NS 1.02 (1.27) 0.69 (0.68) NS 1.4 (149) 1.12 (0.97) NS
GAVEL 1.19 (1.42) 6.57 (6.68) *** 2.09 (2.12) 5.44 (3.02) *** 1.33 (1.18) 5.92 (5.61) **
BIVEL 1.34 (1.97) 1.2 (1.62) NS 0.65 (0.83) 0.6 (0.37) NS 0.9 (0.86) 0.82 (0.86) NS
POLYC 19.77 (19.33) 4.46 (445) * 12.17 (11.91) 2.2 (1.35) * 2.98 (2.94) 1.67 (1.33) NS
PENAV 0.05 (0.09) 0.08 (0.14) NS 0.18 (0.31) 0.52 (0.72) NS 0.85 (1.28) 1.17 (1.76) NS
PODON 0.88 (1.24) 0.22 (0.31) NS 1.12 (1.51) 0.33 (0.5) NS 2.07 (2.59) 0.49 (0.64) NS
EVNOR 0.83 (1.36) 0.59 (0.95) NS 1.29 (1.98) 3.01 (5.22) NS 1.77 (2.38) 1.39 (2.21) NS
PARAC 4.747 (5.73) 2.59 (2.6) NS 7.22 (6.11) 4.11 (2.27) NS 7.01 (4.65) 8.95 (6.79) NS
P-CAL 5.00 (5.53) 6.32 (5.58) NS 11.19 (8.7) 9.84 (6.3) NS 11.56 (9.98) 10.07 (5.55) NS
TEMST 1.24 (1.92) 1.14 (1.77) NS 2.36 (2.99) 2.99 (3.53) NS 2.26 (2.79) 4.72 (6.16) NS
CENTR 043 (0.48) 1.1 (1.16) NS 0.5 (0.52) 0.94 (0.93) NS 0.6 (0.57) 1.79 (2.09) NS
ACCLA 9.86 (11.22) 1.9 (2.26) * 7.11 (6.56) 3.47 (4.17) NS 9.75 (9.19) 4.67 (6.33) *
ACBIF 0 (0) 17.18 (18.84) *** 0 (0) 7.72 (9.24) *** 0 (0) 5 (6.58) **
ACCOP 8.82 (9.15) 17.42 (8.27) ** 12.7 (12.14) 14.2 (10.24) NS 11.34 (11.39) 8.95 (7.92) NS
OITPL 0.19 (0.30) 0.18 (0.19) NS 0.58 (0.74) 1 (1.34) NS 0.79 (0.94) 1.1 (1.32) NS
OITSI 1.12 (1.39) 8.98 (10.94) * 3.31 (2.91) 10.44 (11.91) NS 2.67 (2.44) 8.68 (9.63) NS
OITNA 3.68 (4.26) 1.3 (1.35) NS 5.78 (7.39) 1.65 (1.58) NS 743 (8.69) 3.59 (3.27) NSCYCLO 7.56 (11.21) 0.01 (0.01) ** 0.15 (0.25) 0.01 (0.02) NS 0.01 (0.01) 0.01 (0.02) NS
ONCAE 0.21 (0.27) 2.36 (345) NS 0.5 (0.74) 4.97 (6.72) * 0.61 (0.72) 6.55 (7.81) *
EUTER 0.66 (0.62) 1.21 (1.38) NS 1.3 (1.38) 2.38 (1.8) NS 1.22 (1.2) 2.34 (1.66) NS
HARPA 0.51 (0.51) 1.03 (1.14) NS 0.27 (0.28) 0.84 (0.83) NS 0.23 (0.26) 0.81 (0.8) *
COPNA 0.60 (0.48) 3.08 (2.85) * 0.61 (0.54) 2.22 (2.26) * 0.79 (0.52) 2.05 (2.14) NS
CIRRI 23.58 (22.91) 14.87 (12.96) NS 17.6 (17.17) 11.14 (10.51) NS 19.33 (15.19) 10.17 (9.9) *
PARAG 0.03 (0.06) 0.8 (0.64) *** 0 (0) 1.23 (143) *** 0.02 (0.04) 0.54 (0.7) *
SAGIT 0.40 (0.54) 0.08 (0.1) NS 0.6 (0.74) 0.38 (0.36) NS 0.92 (0.95) 0.4 (0.3) NS
OIKOP 4.42 (4.58) 1.23 (142) * 6.24 (5.32) 2.26 (1.93) * 4.49 (2.57) 1.92 (1.68) **
Copepods 45.49 (27.19) 66.57 (22.1) * 54.79 (21.08) 67.83 (17.65) NS 57.5 (2044) 70.63 (13.55) NS
Simpsons index 0.40 (0.11) 0.37 (0.13) NS 0.34 (0.09) 0.31 (0.11) NS 0.35 (0.12) 0.30 (0.10) NS
Mean values and range of variation (standard deviation (SD) in brackets) for relative abundance (%) of zooplankton taxa and the Simpsons diversity
index values for the copepod community at each salinity site of the estuaries of Bilbao and Urdaibai, along with the results of MannWhitney U test
for the differences between estuaries at each salinity site. Only taxa that conform more than 0.5% of the zooplankton community abundance in any of
the estuaries were taken into account (species code as in Table I). Note thatA . bifilosawas not present in the estuary of Bilbao. The 35 salinity site
was not taken into account for the statistical analysis.NS, not significant.
***P, 0.001, **P, 0.01, *P, 0.05.
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Fig. 5. (A) Temporal distribution of total zooplankton abundance (log10ind. m23; mean value for the 30 34 salinity sites) (left axis, continuous
line) and the accumulated percentage of total zooplankton for the dominantAcartia species (right axis) (ind. m23; average value for the 3034salinity sites) for the estuaries of Bilbao and Urdaibai (left and right graph, respectively): A. clausi (black dotted white area), A. bifilosa (whitedotted black area) and Acartia copepodites (striped white area); the rest of Acartia species are not shown due to extremely low abundance incomparison with the dominant ones; (B) spatial distributions of Acartia species (abundance, ind.m23) along the salinity gradient (bottom axis;3035 salinity sites) for the 2-year period (left axis; from July 1999 to May 2001); from left to right: A. clausi,A. discaudata,A. margalefi, Acartia sp.and Acartia copepodites for the estuary of Bilbao (upper graphs) and, A. clausi, A. bifilosa and Acartia copepodites for the estuary of Urdaibai(bottom graphs). All scales superimposed.
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In the period 19971999, copepods of the estuaries
of Bilbao and Urdaibai were mainly represented byAcartia species: A. clausi and A. bifilosa in the Urdaibai
estuary and A. clausi, A. discaudata and A. margalefi
(reported firstly asA.teclae) in the Bilbao estuary (Uriarte,2001; Uriarte and Villate, 2005); however, bothA.discau-
data and A. margalefi were first reported from the Bilbao
estuary in that cited period. Apart from the successful
establishment of the former pair of species (Fig. 5B), a
new species ofAcartia(Acartiasp.) was recorded in Bilbao
in the 19992001 period, although the identification to
species level was not possible. Beside this, the copepods
C. aquaedulcis and Eurytemora affinis were also found for
the first time in the Bilbao estuary. Calanipeda aquaedulcis
is a common species in estuarine waters in Europe (e.g.
Dussart and Defaye, 1983) that inhabits the Urdaibai
estuary (Villate, 1997), and E. affinis is a dominant
species in the upstream waters of Northern Europeanestuaries (e.g. Heip and Herman, 1995).
The spatial distributions of all the new species found
in Bilbao skewed towards the upstream estuary, since the
few specimens of Acartia sp. recorded, along with the C.
aquaedulcisandE.affinis, were always caught at the 3033
salinity sites. The progressive appearance of new species
of copepods in lower salinity waters of the Bilbao estuary
does not mean that they will settle successfully,
developing stable populations in the future. For example,
E. affinis needs water bodies of 0.5 to 5 salinity to settle
(e.g. Castel and Veiga, 1990), but in the estuary of Bilbao,
euhaline waters (.30 salinity) predominate within the
estuary and usually penetrate as far as the upper reaches
in depth, preventing the existence of extensive meso- and
polyhaline water bodies, except for short periods of highriver discharge. However, these increasing records indi-
cate the improvement of water quality towards the
upstream estuary. There are two potential vectors for the
appearance of the reported species: the reappearance of
hypothetical autochthonous species via resting egg bank
reservoirs, and the colonization by invasive species. In
this sense, the presence of a bank of resting eggs has
been reported for the Bilbao estuary (Masero and Villate,
2004); however, although resting eggs can remain viable
for years or even centuries in the sediment (Marcus et al.,
1994; Hairston et al., 1995) and can remain viable for
months, possibly years, under anoxic conditions (review
in Katajisto, 2006 and references therein), the decades of
anoxic conditions of the sediment and upper water layer,
along with the continuous dredging in the estuary of
Bilbao (Borja and Collins, 2004) makes this mechanism
highly improbable, as increasing mortality of resting eggs
in the sediments over time has been attributed to
exposure to adverse environmental factors (e.g. low
oxygen and H2S) (Uye et al., 1984). In this sense, the
introduction by ballast waters is the most plausible expla-
nation for the recovery of the copepod community of the
Bilbao estuary. Port activities are well developed in this
estuary, and the ballast water and associated sediments of
long distance cargo ships are considered the mostimportant transmission agent across oceanic barriers for
estuarine or freshwater aquatic organisms, including
copepods (e.g. Carlton and Geller, 1993; Gollasch et al.,
2000; Bailey et al., 2003). Beside this, resting eggs may
also lead to colonization by invasive species as there is
evidence of dormant stages being transported, at least
over short distances, by wind or water currents or by
animal vectors, although there is controversy over the sig-
nificance and extent of such dispersals (e.g. Bohonak and
Jenkins, 2003; Havel and Shurin, 2004). In this sense,
organisms that produce diapausing resting stages, as
most of the Acartia and Eurytemora species do (e.g.
Mauchline, 1998), are especially difficult to control,because they are able to survive extreme conditions
during transport (Panovet al., 2004).
C O N C L U S I O N S
Our results illustrate a new step in the recovery of the
water quality in the Bilbao estuary since the late 1980s,
Table IV: Comparison with the 1997 1999period (Mann Whitney U test)
Uriarte and Villate (2004,
2005) Present study
30 33 34 30 33 34
CODE PP-value PP-value PP-value PP-value PP-value PP-value
DOS *** *** *** *** *** *
SDD *** *** *** *** *** ***
GAVEL NS *** ** *** *** **
POLYC NS NS NS * * NS
CIRRI * ** ** NS NS *
Copepods NS * ** * NS NS
ACCLA ** *** *** ** * **
OITSI NS NS NS * NS NS
ONCAE NS NS * NS * *
EUTER NS ** *** NS NS NS
HARPA NS NS *** NS NS *
MannWhitney U test results for the study of March 1997May 1999
(Uriarte and Villate, 2004, 2005) along with present study (July 1999
May 2001) results. Only categories analyzed for both periods and that
presented significant differences between estuaries in the 3034 salinity
sites in, at least, one of the compared period are shown. Species code
as in Table I; dissolved oxygen saturation (DOS; %) and Secchi disk
depth (SDD; m) are the environmental variables compared. Relative
abundance of zooplankton was compared for GAVEL, POLYC, CIRRI and
Total Copepods; for copepod species the relative abundance is estimated
against the copepod community.
NS, not significant.
***P, 0.001; **P, 0.01; *P, 0.05.
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after the decay of industrial activities and the onset of a
new sewage water treatment program (review in Borja
and Collins, 2004). The improvement of environmental
conditions was supported by the higher oxygenation of
the euhaline waters during the study period (1999
2001), thus allowing the occurrence of new species such
as C. aquaedulcis, Eurytemora affinis and a new unidentifiedAcartia species, along with the establishment of the
A.discaudataand A.margalefipopulations, first reported in
the 19971999 period. Beside this, the ongoing recov-
ery of the zooplankton community in the estuary of
Bilbao is confirmed by the increasing similarity with the
zooplankton community of the low polluted Urdaibai
estuary, as shown by comparing present results (1999
2001 period) with a previous study (19971999 period).
The observed changes in relation to previous data
confirm that the health of the Bilbao estuary is improv-
ing towards the upstream estuary, and reinforces the
need for monitoring zooplankton communities to asses
the health of estuarine waters.
A C K N O W L E D G E M E N T S
Thanks to Rakel Masero and Estibaliz D az for support
during sampling. We would also like to thank the two
anonymous reviewers for their useful comments and to
Mark de Bruyn for revising the text.
F U N D I N GA.A.s work was supported by a fellowship from the
Education, Universities and Research Department of
the Basque Country Government. This research was
financially supported by the University of the Basque
Country (project UPV 118.310-EA207/98).
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