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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: [email protected]

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: [email protected]

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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).

A. ALBAINA ET AL. j ZOOPLANKTON IN BASQUE ESTUARIES

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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).

R E F E R E N C E S

Agirre, X. (2000) Mantenugai eta a klorofilaren aldakortasuna kutsa-

dura maila ezberdina duten bi estuarioen eremu euhalinoan.

Lizentziatura-tesina. University of Basque Country, Bilbao.

Albaina, A. and Irigoien, X. (2007) Fine scale zooplankton distri-

bution in the Bay of Biscay in spring 2004. J. Plankton Res., 29,

851870.

Arfi, R., Champalbert, G. and Patriti, G. (1981) Systeme planctonique

et pollution urbaine: un aspect des populations zooplanctoniques.

Mar. Biol.,61, 133141.

Bailey, S. A., Duggan, I. C., Overdijk, C. D. A. et al. (2003) Viability

of invertebrate diapausing eggs collected from residual ballast

sediment.Limnol. Oceanogr.,48, 17011710.

Bartolome, L., Tueros, I., Cortazar, E. et al. (2006) Distribution of

trace organic contaminants and total mercury in sediments from

the Bilbao and Urdaibai Estuaries (Bay of Biscay). Mar. Pollut. Bull.,

52, 10901117.

Bohonak, A. J. and Jenkins, D. G. (2003) Ecological and evolutionary

significance of dispersal by freshwater invertebrates. Ecol. Lett., 6,

783796.

Borja, A. and Collins, M. (eds) (2004) Oceanography and marine

environment of the Basque Country. Elsevier Oceanography Series 70.

Elsevier, Amsterdam.

Borja, A., Franco, J., Belzunce, M. J. et al. (2000) Red de vigilancia y

control de la calidad de las aguas litorales del Pas Vasco:

Anos1998-1999. Departamento de Ordenacion del Territorio,

Vivienda y Medio Ambiente, Gobierno Vasco. Servicio Central de

Publicaciones del Gobierno Vasco- Basque government, Vitoria,

94 .pp

Carlton, J. T. and Geller, J. B. (1993) Ecological roulette: the global

transport of nonindigenous marine organisms. Science, 261,

7882.

Castel, J. and Veiga, J. (1990) Distribution and retention of the

copepod Eurytemora affinis hirundoides (Nordquist, 1888) in a turbid

estuary. Mar. Biol.,107, 119128.

Cearreta, A., Irabien, M. J., Leorri, E. et al. (2000) Recent anthropo-

genic impacts on the Bilbao Estuary, Northern Spain: geochemical

and microfaunal evidence.Estuarine Coastal Shelf Sci.,50, 571592.

Dussart, B. H. and Defaye, D. (1983) Repertoire mondial des crustaces

copepodes des eaux nterieures. I. Calanoides. Centre National de la

Recherche Scientifique, Paris.

Frietzsche, D. and von Oertzen, A. (1995) Bioenergetics of a highly

adaptable brackish water polychaete. Thermochim. Acta,251, 19.

Gaudy, R. (1985) Features and peculiarities of zooplankton commu-

nities from the Western Mediterranean. In Moraitou-

Apostolopoulou, M. and Kiortsis, V. (eds), Mediterranean Marine

Ecosystems. Plenum Publishers Corp, London, pp. 279301.

Gibson, G. R., Bowman, M. L., Gerritsen, J. et al. (2000) Estuarine and

Coastal Marine Waters: Bioassessment and Biocriteria Technical Guidance.

EPA 822-B-00-024. U.S. E.P.A., Office of Water, Washington, DC.

Gollasch, S., Lenz, J., Dammet, M. et al. (2000) Survival of tropical

ballast water organisms during a cruise from the Indian Ocean to

the North Sea. J. Plankton Res.,22, 923937.

Hairston, N. G., Jr, Van Brunt, R. A., Kearns, C. M. et al. (1995) Age

and survivorship of diapausing eggs in a sediment egg bank. Ecology,

76, 17061711.

Havel, J. E. and Shurin, J. B. (2004) Mechanisms, effects, and scales of

dispersal in freshwater zooplankton.Limnol. Oceanogr.,49, 12291238.

Heip, C. and Herman, P. M. J. (1995) Major biological processes in

European tidal estuaries: a synthesis of the JEEP-92 Project.

Hydrobiologia,311, 17.

Iriarte, A., de la Sota, A. and Orive, E. (1998) Seasonal variation ofnitrification along a salinity gradient in an urban estuary.


Katajisto, T. (2006) Benthic resting eggs in the life cycles of calanoid

copepods in the northern Baltic Sea. W. and A. de Nottbeck

Foundation Sci. Rep. 29, pp. 1 46. ISBN 952-99673-0-6 (paper-

back), ISBN 952-10-2933-1 (PDF), http://ethesis.helsinki.fi/

julkaisut/bio/bioja/vk/katajisto/benthicr.pdf

Lorenzen, C. J. (1967) Determination of chlorophyll and phaeopigments

by spectrophotometric equations.Limnol. Oceanogr.,12, 343 346.


751


14/14

Marcus, N. H., Lutz, R., Burnett, W. et al. (1994) Age, viability, and

vertical distribution of zooplankton resting eggs from an anoxic

basin: Evidence of an egg bank. Limnol. Oceanogr.,39, 154158.

Masero, R. and Villate, F. (2004) Composition, vertical distribution

and age of zooplankton benthic eggs in the sediments of two

contrasting estuaries of the Bay of Biscay. Hydrobiologia, 518,

203214.

Mauchline, J. (1998) The biology of calanoid copepods. Advances in

Marine Biology. Vol. 33. Academic Press, London.

Panov, V. E., Krylov, P. I . and Riccardi, N. (2004) Role of diapause in

dispersal and invasion success by aquatic invertebrates. J. Limnol.,

63(Suppl. 1), 5669.

Regner, D. (1987) The impact of pollution on the copepod community

from the eastern Adriatic coast. Chemosphere,16, 369379.

Roman, M. R., Gauzens, A. L., Rhinehart, W. K. et al. (1993) Effects

of low oxygen waters on Chesapeake Bay zooplankton. Limnol.

Oceanogr.,38, 16031614.

Rose, M. (1933) Copepodes pelagiques. Faune de France. Vol. 26.

Lachevalier, Paris.

Simpson, E. H. (1949) Measurement of diversity. Nature,163, 688.

Siokou-Frangou, I. and Papathanassiou, E. (1991) Differentiation ofzooplankton populations in a polluted area. Mar. Ecol. Prog. Ser., 76,

4151.

Soetaert, K. and Van Rijswijk, P. (1993) Spatial and temporal patterns

of the zooplankton in the Westerschelde estuary. Mar. Ecol. Prog. Ser.,

97, 4759.

ter Braak, C. J. F. and Smilauer, P. (2002) CANOCO Reference Manual

and CanoDraw for Windows Users Guide: Software for Canonical Community

Ordination (Version 4.5).Microcomputer Power.

Uriarte, I. (2001) Evaluacion de la respuesta del zooplancton al estres

ambiental en un sistema con elevado g rado de alteracion antropica

(estuario de Bilbao) en relacion a un sistema poco alterado (estuario

de Urdaibai).PhD Thesis. UPV/EHU, 118 pp.

Uriarte, I. and Villate, F. (2004) Effects of pollution on zooplankton

abundance and distribution in two estuaries of the Basque coast

(Bay of Biscay). Mar. Pollut. Bull.,49, 220228.

Uriarte, I. and Villate, F. (2005) Differences in the abundance and dis-

tribution of copepods in two estuaries of the Basque coast (Bay of

Biscay) in relation to pollution. J. Plankton Res.,27, 863874.

Uye, S., Yoshiya, M., Ueda, K. et al. (1984) The effect of organic sea-

bottom pollution on survivability of resting eggs of neritic calanoids.

Crustaceana, (Suppl. 7), 390403.

Van Damme, D., Heip, C. and Willems, K. A. (1984) Influence of pol-

lution on the harpacticoid copepods of two North Sea estuaries.


Villate, F. (1997) Tidal influences on zonation and occurence of resi-

dent and temporary zooplankton in a shallow system (Estuary of

Mundaka, Bay of Biscay). Sci. Mar., 61, 173188.

Wilson, J. G. (1994) The role of bioindicators in estuarine manage-

ment. Estuaries,17, 4101.

Zaitsev, Y. P. (1992) Recent changes in the trophic structure of the

Black Sea.Fish. Oceanogr.,2, 180189.


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