Scale-dependent effects of nutrient loads and climatic conditions on benthic and pelagic communities in the Gulf of Finland - [PDF Document] (2024)

ORIGINAL ARTICLE

Scale-dependent effects of nutrient loads and climaticconditions on benthic and pelagic communities in the Gulfof FinlandArno Pollumae1, Jonne Kotta1 & Ulle Leisk2

1 Estonian Marine Institute, University of Tartu, Tallinn, Estonia

2 Department of Environmental Engineering, Tallinn University of Technology, Tallinn, Estonia

Problem

Eutrophication and climate change are ranked among the

major threats to the stability of marine coastal environ-

ment and can have severe impacts on near-shore biodi-

versity and functioning (e.g. McGowan et al. 1998;

Howarth et al. 2000; Jackson et al. 2001). Nutrient loads

may lead to algal blooms, accumulation of organic matter

and development of anoxia, and consequently can cause

significant changes in ecosystems (Andersen et al. 2006;

Paerl 2006). The effects of climatic variability on coastal

ecosystems are less known due to the mismatch of impor-

tant scales between climatic conditions and biological

variables. The effects of climatic conditions operate

through local weather parameters such as temperature,

wind, rain, snow and current patterns, as well as interac-

tions among these (Stenseth et al. 2002). Shifts in climatic

conditions are known to have profound ecological

impacts, altering the patterns of distribution, abundance

and diversity of species (Hughes 2000; Lotze et al. 2006).

Such effects vary largely among regions, reflecting system-

specific attributes and direct and indirect responses that

act as a filter to modulate the responses to enrichment

and climate change (Cloern 2001; Ronnberg & Bonsdorff

2004; Hewitt & Thrush 2009). As different regions

respond differently to the same type of environmental

Keywords

Baltic Sea; benthic invertebrates; climate

change; mesozooplankton; nutrient load;

spatial scale.

Correspondence

A. Pollumae, Estonian Marine Institute,

University of Tartu, Maealuse 10a, 12618

Tallinn, Estonia.

E-mail: [emailprotected]

Conflicts of interest

The authors declare no conflicts of interest.

doi:10.1111/j.1439-0485.2009.00304.x

Abstract

Eutrophication and climate change are ranked among the most serious threats

to the stability of marine ecosystems worldwide. The effects of nutrient loads

and climatic conditions vary in direction, magnitude and spatial extent. To

date the factors that are behind the scale-specific spatial and temporal variabil-

ity are poorly known. In this study we assessed how variability in nutrient

loads and climatic conditions at local, gulf and regional scales explained the

spatial patterns and temporal trends of zooplankton and benthic invertebrates

in the Gulf of Finland. In general both local and gulf scale environmental vari-

ability had an important effect on benthic invertebrate species and the variabil-

ity was mainly due to local nutrient loading, gulf scale temperature and salinity

patterns. Zooplankton species were equally affected by environmental variabil-

ity at all spatial scales, and all nutrient load and climatic condition variables

contributed to the models. The combination of variables at all spatial scales

did not explain the substantially larger proportion in invertebrate variability

than variables at any individual scale. This suggests that large-scale pressures

such as nutrient loads and change of climatic conditions may define broad pat-

terns of distribution but within these patterns small-scale environmental vari-

ability significantly modifies the response of communities to these large-scale

pressures.

Marine Ecology. ISSN 0173-9565

20 Marine Ecology 30 (Suppl. 1) (2009) 20–32 ª 2009 Blackwell Verlag GmbH

stress, the areal-specific ecological responses should be

described.

Taking this into account, there is no single natural scale

at which the effects of nutrient loads and climatic condi-

tions could be studied (Levin 1992; Karlson & Cornell

1998). To identify the most important governing factors

one needs to determine the scales where the links between

nutrient load and climatic condition variables and biotic

patterns are the strongest (Steele & Henderson 1994).

Although it is recognized that processes affect ecosystems

simultaneously at many spatial scales (Steele & Henderson

1994; Denny et al. 2004), to date the relative importance of

small- and large-scale processes in the formation of marine

communities is little known (e.g. Hewitt et al. 2007).

Large-scale environmental stresses and disturbances (e.g.

climatically driven changes in seawater temperature, sea

level or the intensity of ice scouring) can synchronize pop-

ulation changes over wide geographical areas and define

broad patterns of distribution, if they have a direct effect

on recruitment or mortality. Within these patterns, smal-

ler-scale processes operate at a lower intensity to modify

distributions, abundances and functioning of communities

(Kotta & Witman 2009). Recently, it was shown that the

degree of interaction between large-scale environmental

factors and smaller scale variability was not consistent

across sites or species. Knowledge about such variability

may affect our ability to predict effects of nutrient loads

and changing climatic conditions on coastal communities

(Hewitt & Thrush 2009).

In this study we evaluated how nutrient load and cli-

matic condition variables estimated at local (10s km),

gulf (100s km) and regional scales (1000s km) contrib-

uted to the biomass of zooplankton and benthic inverte-

brate species in a shallow brackish water ecosystem of

the Baltic Sea. Nutrient loads have been an increasing

ecological threat in the Baltic Sea for the past 50 years.

During this time the load of nutrients has grown four-

fold for nitrogen and eight times for phosphorus, lead-

ing to an increased production at all trophic levels in

the ecosystem (Elmgren 2001; Ronnberg & Bonsdorff

2004). Although rising temperature has caused major

shifts in the community structure in many European

water bodies (e.g. Conners et al. 2002), such tempera-

ture-induced shifts have not been observed in the Baltic

Sea in recent decades. It is plausible that recent changes

in the mean water temperature are not ecologically

important as large seasonal variation counteracts the

potential effects of recent global warming. On the other

hand, the indirect effects of global warming can be

important and can potentially affect the structure and

function of the Baltic coastal communities.

Mesozooplankton is both passively and actively mobile

and capable of moving both vertically and horizontally in

the aquatic environment. Their mobility allows them to

transfer materials between different environments and to

give mesozooplankton the potential to form strong links

between different subsystems (Lundberg & Moberg 2003).

Therefore it is expected that the biomasses of mesozoo-

plankton are influenced by large-scale environmental vari-

ability rather than small-scale environmental variability.

Benthic invertebrates, however, are thought to be rela-

tively stationary, longer lived and temporally less variable

than mesozooplankton. However, benthic invertebrates

do not behave as a single entity and there exists a large

within-group variability among benthic invertebrates. Ear-

lier studies have shown that suspension-feeders are

directly linked to pelagic primary productivity (Cloern

1982; Kotta & Møhlenberg 2002) and benthic grazers and

deposit-feeders to benthic primary productivity (Graneli

& Sundback 1985; Orav-Kotta & Kotta 2004; Kotta et al.

2006). Thus, it is expected that local variables explain bet-

ter the distribution of benthic grazers and deposit-feeders

and large-scale variables that of benthic suspension-feed-

ers. Besides, mobile benthic species possess the ability to

escape direct small-scale physical disturbances or food

depletion, whereas non-migrating benthic species are

more susceptible to such disturbances and rely completely

on local food levels (e.g. Tillin et al. 2006; Kotta et al.

2008). Therefore it is also expected that local variables

explain better the distribution of non-migrating benthic

species and large-scale variables that of mobile benthic

species.

Study Area

The study was conducted in the Gulf of Finland, North-

ern Baltic Sea. The average depth of Gulf is 37 m and

the maximum depth 123 m. Sand, silt or sandy clay bot-

toms dominate. The Eastern Gulf of Finland receives

fresh water from a huge drainage area and the Western

Gulf is a direct continuation of the Baltic Sea proper,

therefore the gulf has a permanent east–west gradient of

salinity. The salinity range of stations was 2.2–7.3 psu.

The area is influenced by diffuse and point source nutri-

ent loads.

The Water Framework Directive 2000 ⁄ 60 ⁄ EC (WFD) is

the most significant piece of European water legislation

that prevents further eutrophication of the ecosystem of

the Gulf of Finland. According to the directive the waters

of the Gulf of Finland have been divided into water

bodies and the assessment of the ecosystem state is made

by these basic management units. In our study we evalu-

ated relationships between nutrient loads, climatic condi-

tions and ecosystem variables by each water body to

provide a better ecological basis for the WFD classifica-

tion scheme.

Pollumae, Kotta & Leisk Scale-dependent effects of nutrient loads and climatic conditions

Marine Ecology 30 (Suppl. 1) (2009) 20–32 ª 2009 Blackwell Verlag GmbH 21

Material and Methods

Within each water body two stations were sampled

between 1996 and 2005 (Fig. 1, Table 1). Zoobenthos

samples were collected each year during May using a Van

Veen grab (0.1 m2). The depth of sampling sites ranged

from 8 to 100 m and encompassed coarse sand, medium

sand and silt sediments. Grab samples were sieved in the

field on 0.25-mm mesh screens. The residues were stored

at )20 �C and subsequent sorting, counting and determi-

nation of invertebrate species were performed in the labo-

ratory using a stereomicroscope. All species were

determined to the species level except for oligochaetes

and insect larvae. The dry weight of species was obtained

after drying the individuals at 60 �C for 2 weeks. During

sampling we recorded near-bottom oxygen (minimum

layer) and depth-integrated salinity values.

Zooplankton was collected at the same stations as used

for zoobenthos samples in May and August over 1996–

2005. The samples were collected by vertical tows with a

Juday closing plankton net (mesh size 90 lm, mouth area

0.1 m2). The samples were preserved in 4% formaldehyde

solution in seawater. The abundances of zooplankton spe-

cies were estimated from a number of subsamples accord-

ing to the methods recommended by HELCOM (1988).

Biomasses (wet weights) were calculated using the

Fig. 1. Sampling locations (circles), weather

stations (asterisks) and water bodies along the

Estonian coastline in the Gulf of Finland.

Water bodies 1–7 are defined by the EU

Water Framework Directive, water body 0

represents the offshore conditions of the Gulf

of Finland. Black square on minimap indicates

the location of Gotland Basin.

Table 1. Characteristics of the studied water bodies (WB0...7) in the Gulf of Finland.

Environmental characteristics WB0 WB1 WB4 WB5 WB6 WB7

Water renewal time, years 1.1 1.4 0.8 0.4 0.3 0.1

Average depth, m 65 21 52 37 27 13

Mean water flow from rivers, m3Æs)1 0.0 >400 <5 10…20 10…20 <1

Near-bottom oxygen concentration, mlÆl)1 4.6 7.7 5.2 8.4 8.7 8.1

Salinity 6.3 4.5 6.4 6.2 6.2 6.3

Sea surface temperature in May 5.9 8.8 6.7 5.8 7.8 9.1

Air temperature in May 9.0 9.5 8.9 9.1 9.1 8.5

Wind speed in May 3.5 3.5 3.5 3.4 3.4 3.1

Nitrogen load from point sources

into a water body, tÆyear)1

0.0 434.1 0.1 827.2 6.0 0.0

Phosphorus load from point sources

into a water body, tÆyear)1

0.0 8.9 0.0 57.4 1.2 0.0

Riverine nitrogen load into

a water body, tÆyear)1

0.0 8941.7 115.0 1739.2 1487.1 0.0

Riverine phosphorus load

into a waterbody, tÆyear)1

0.0 798.4 4.4 32.3 31.7 0.0

Scale-dependent effects of nutrient loads and climatic conditions Pollumae, Kotta & Leisk

22 Marine Ecology 30 (Suppl. 1) (2009) 20–32 ª 2009 Blackwell Verlag GmbH

biomass factors for different taxonomic groups and devel-

opmental stages (Hernroth 1985).

The data on the annual point source and riverine loads

of total N and total P to the Gulf of Finland in 1996–

2005 was obtained from the Estonian Ministry of Envi-

ronment and from the MARE homepage (http://

www.mare.su.se/). The data of annual total N and total P

loads and runoff of River Neva was obtained through Bal-

tic-Nest (http://nest.su.se/nest/) from NW Administration

of Roshydromet (Russia). The loads into six water bodies

of the Estonian coast of the Gulf of Finland were used as

nutrient load variables at the local scale. In general, the

diffuse nutrient loads were the major type of loading in

the study area. Depending on the water body the contri-

bution of the diffuse nutrient N loads to the total N loads

varied between 68 and 100% and the contribution of the

diffuse nutrient P loads to the total P loads between 35

and 100%. The sum of loads due to Estonia, Finland and

Russia represented nutrient load variables at the gulf

scale. The concentrations of total N and total P in the

Central Baltic Sea in winter were used as a proxy of

regional nutrient load variables because the plankton has

not yet taken up the nutrients. Inorganic nutrients that

have accumulated during the winter are assimilated dur-

ing the following spring bloom (HELCOM 2002).

As a proxy of atmospheric conditions the winter index

of the North Atlantic Oscillation was used to relate the

global climate pattern to the variation of biological data

in the study area (NAO December–March, http://www.

cgd.ucar.edu/cas/jhurrell/nao.stat.winter. html) (Barnston

& Livezey 1987; Ottersen et al. 2001). The NAO is an

alternation in the pressure difference between the sub-

tropical atmosphere high-pressure zone centred over the

Azores and the atmospheric low-pressure zone over Ice-

land. NAO’s connection with the wind, temperature and

precipitation fields is strongest during winter. The link

between the NAO and sea water temperature may persist

over the summer, however, being highly region-depen-

dent and should be assessed for each site separately (e.g.

Ottersen et al. 2001). During the years of high NAO there

is a substantial increase in the rainfall and consequently

of the fresh-water inflow into the Baltic Sea (Hanninen

et al. 2000). The increased pressure differences result in

higher winter temperatures in Northern Europe (Rogers

1984). As an additional global climatic conditions vari-

able, we used the Baltic Sea Index (BSI), which is the dif-

ference of normalized sea level pressures between Oslo in

Norway and Szczecin in Poland. The BSI is significantly

related to NAO and is used as a regional calibration of

the North Atlantic Oscillation index (Lehmann et al.

2002). As the local, gulf and regional scale proxies of cli-

matic condition variables we used average wind speed, air

and water temperatures, water column salinity and near-

bottom oxygen concentration and water temperatures at

the respective scale obtained from the Estonian Hydrome-

teorological Institute (Table 2).

Multivariate data analyses on abiotic environment and

invertebrate communities were performed by the statisti-

cal program PRIMER version 6.1.5 (Clarke & Gorley

2006). Invertebrate biomass data were square-root trans-

formed to down-weigh the dominant species and increase

the contribution of rarer species in the multivariate analy-

sis. Similarities between each pair of samples were calcu-

lated using a zero-adjusted Bray–Curtis coefficient. The

coefficient is known to outperform most other similarity

measures and enables samples containing no organisms at

all to be included (Clarke et al. 2006). Environmental

variables were normalized prior to analyses. Non-metric

multidimensional scaling analysis (MDS) on square-root

transformed data of macrobenthic biomasses was used to

quantify the dissimilarities between study areas and inver-

tebrate species. Statistical differences in benthic inverte-

brate and mesozooplankton communities among water

bodies were assessed by the ANOSIM permutation test

(Clarke 1993).

BEST analysis (BVSTEP procedure) was used to relate

the patterns of environmental variables measured at local,

gulf and regional scales to the biomasses of inverte-

brate species. The analysis shows which environmental

variables best predict the observed biotic patterns. A

Spearman rank correlation (r) was computed between

the similarity matrices of environmental data (abiotic

variables; Euclidean distance) and different invertebrate

species (a zero-adjusted Bray–Curtis distance). A global

BEST match permutation test was run to examine the sta-

tistical significance of observed relationships between

environmental variables and biotic patterns. The separate

and additive contribution of nutrient loads and climatic

condition variables was assessed in one analysis and the

contribution of local, gulf and regional scale variables in

another analysis.

Results

Generally, correlations between the studied abiotic envi-

ronmental variables were poor (P > 0.05). Among nutri-

ent load variables there were significant correlations

between total N at 10 m surface layer in Gotland Basin

during winter and total P at 10 m surface layer in Got-

land Basin during winter (Spearman rank correlation,

R = 0.47, P < 0.05), total N and total P point discharges

at local scale (R = 0.98, P < 0.001), total N point dis-

charge and riverine total P load at local scale (R = 0.85,

P < 0.001) and among climatic condition variables

between sea surface temperature predicted by nearest air

temperature and sea surface temperature at station during

Pollumae, Kotta & Leisk Scale-dependent effects of nutrient loads and climatic conditions

Marine Ecology 30 (Suppl. 1) (2009) 20–32 ª 2009 Blackwell Verlag GmbH 23

sampling (R = 0.52, P < 0.05), sea surface temperature

predicted by nearest air temperature and average air tem-

perature during May at nearest weather station (R = 0.64,

P < 0.05) and average yearly wind speed at nearest

weather station and average wind speed during May at

the nearest weather station (R = )0.53, P < 0.05). There-

fore, total P at 10 m surface layer in Gotland Basin dur-

ing winter, total Estonian N load into the Gulf of

Finland, total P load from point sources into a water

body, average wind speed during May in all weather

Table 2. The list of the studied abiotic variables with their relation to spatial scale, nutrient loads and climatic conditions.

Variable Nutrient loads Climatic conditions Regional Gulf Local

Total N at 10 m surface layer in

Gotland Basin during winter

+ +

Total P at 10 m surface layer in

Gotland Basin during winter*

+ +

Total N at 220 m in Gotland Basin + +

Total P at 220 m in Gotland Basin + +

Nearbottom oxygen concentration in

Gotland Basin

+ +

Total Finnish N load into GoF + +

Total Finnish P load into GoF + +

Average near-bottom oxygen

concentration in GoF

+ +

Total Estonian N load into GoF* + +

Total Estonian P load into GoF + +

Near-bottom oxygen concentration at

station during sampling

+ +

Total riverine N load into a water body + +

Total riverine P load into a water body + +

Total N load from point sources into a water body + +

Total P load from point sources into a water body* + +

NAOdecmar + +

BSI + +

Maximum ice cover in the whole Baltic Sea during winter + +

Salinity at 100 in Gotland Basin + +

Sea surface temperature in Gotland Basin in May + +

Average number of days with wind >5 mÆs)1 in

all weather stations

+ +

Average salinity in GoF + +

Average air temperature during May–August

in all weather stations

+ +

Average wind speed during May

in all weather stations*

+ +

Average salinity at station during sampling + +

Sea surface temperature at station

during sampling

+ +

Average yearly air temperature

at nearest weather station

+ +

Average yearly wind speed

at nearest weather station

+ +

Sea surface temperature predicted

by nearest air temperature*

+ +

Number of days with wind >5 mÆs)1

at nearest weather station*

+ +

Average air temperature during

May at nearest weather station*

+ +

Average wind speed during May

at nearest weather station*

+ +

An asterisk denotes variables not used in the statistical analyses.

Scale-dependent effects of nutrient loads and climatic conditions Pollumae, Kotta & Leisk

24 Marine Ecology 30 (Suppl. 1) (2009) 20–32 ª 2009 Blackwell Verlag GmbH

stations, sea surface temperature predicted by nearest air

temperature, number of days with wind >5 mÆs)1 at near-

est weather station, average air temperature during May

at nearest weather station and average wind speed during

May at nearest weather station were excluded from the

further statistical analysis. The lack of other strong corre-

lations suggested that colinearity was never a problem for

the final models.

Altogether, 27 benthic invertebrate and 21 zooplankton

taxa were identified in the study area. Macoma balthica,

Monoporeia affinis, Saduria entomon, Acartia spp., Euryte-

mora affinis and Synchaeta baltica were the most fre-

Table 3. Average biomass of benthic (mgÆdry weightÆm)2) and pelagic (mgÆwet weightÆm)2) in each water body in May 1996–2005.

Species ⁄ taxon WB 0 WB 1 WB 4 WB 5 WB 6 WB 7

Benthic invertebrates

Balanus improvisus 0 0 0 0 2 89

Bylgides sarsi 0 0 0 6 0 0

Cerastoderma glaucum 0 0 0 0 0 1584

Chironomidae larvae 0 0 0 0 192 8

Corophium volutator 0 2 0 5 0 118

Gammarus salinus 28 0 0 0 0 15

Halicryptus spinulosus 0 0 59 111 30 16

Hediste diversicolor 0 0 0 0 0 48

Hydrobia ulvae 0 0 0 3 4 23

Hydrobia ventrosa 0 0 0 5 2 0

Idotea chelipes 0 0 0 0 0 0

Jaera albifrons 0 0 0 0 0 0

Macoma balthica 497 16,970 10,127 33,513 35,495 21,491

Manayunkia aestuarina 0 0 0 0 0 0

Monoporeia affinis 48 107 17 94 2 6

Mya arenaria 0 0 0 127 57 10,370

Oligochaeta 0 13 0 0 2 9

Pontoporeia femorata 184 0 5 0 1 0

Potamopyrgus antipodarum 0 6 0 0 26 0

Pygospio elegans 0 0 0 0 0 0

Saduria entomon 887 629 112 501 0 29

Theodoxus fluviatilis 0 18 0 0 0 59

Trichoptera larvae 0 0 0 0 0 1

Total zoobentos 1673 17,745 10,319 34,373 35,818 33,889

Pelagic invertebrates

Acartia spp. 879 23 361 349 177 211

Balanus improvisus nauplii 0 0 0 0 0 2

Bivalvia larvae 77 976 689 269 15 46

Bosmina maritima 4 15 0 2 1 0

Centropages hamatus 32 0 29 8 2 10

Cercopagis pengoi 0 0 0 0 0 0

Cyclopidae 10 32 2 1 0 0

Eurytemora affinis 699 66 224 43 34 56

Evadne nordmanni 34 13 8 21 24 28

Frittillaria borealis 179 4 185 185 169 69

Keratella cochlearis 0 1 0 0 0 0

Keratella cruciformis 0 0 0 0 0 0

Keratella quadrata 20 19 5 3 0 1

Limnocalanus macrurus 587 106 336 6 6 1

Pleopsis polyphemoides 0 0 0 1 0 15

Podon intermedius 0 0 0 0 1 0

Pseudocalanus elongatus 156 1 310 14 7 13

Synchaeta curvata 0 0 0 0 2 21

Synchaeta monopus 20 2 5 4 43 4

Synchaeta baltica 1992 167 1097 1936 512 407

Temora longicornis 30 1 39 14 4 11

Total zooplankton 6731 1594 4392 4793 1554 1329

Pollumae, Kotta & Leisk Scale-dependent effects of nutrient loads and climatic conditions

Marine Ecology 30 (Suppl. 1) (2009) 20–32 ª 2009 Blackwell Verlag GmbH 25

quently detected taxa. The total biomass of benthic and

pelagic invertebrates in samples ranged from 0 to

188 gÆdry weightÆm)2 and from 3 to 62,000 mgÆwet

weightÆm)2, respectively (Table 3).

When all biomasses of pelagic and benthic invertebrates

were pooled, the ordination of stations reflected the east–

west gradients of the Gulf of Finland. ANOSIM analysis

confirmed the trend and showed that most water bodies

were significantly different in terms of the biomass struc-

ture, i.e. the studied water bodies behave independently

of each other (global R = 0.448, P < 0.001) (Fig. 2).

Pelagic species had larger spatial and temporal variabil-

ity of biomasses compared to that of benthic invertebrate

species. In terms of spatial and temporal variability pat-

terns the majority of benthic invertebrate species were

statistically distinguished from zooplankton species

(ANOSIM test, P < 0.05). However, mobile benthic spe-

cies such as Corophium volutator, Pontoporeia femorata,

M. affinis and S. entomon were statistically dissimilar from

zooplankton species (ANOSIM test, P > 0.05). Small and

abundant rotifers were placed inside the zooplankton

cluster but close to the non-migrating benthic species,

whereas larger and less dominating copepods were sepa-

rated from the non-migrating benthic species (Fig. 3).

The relationship between abiotic environment and ben-

thic invertebrate species was strongest at local and gulf

scales (depending on the species, Spearman rank correla-

tions varied between r = 0.19 and 0.38) and weak at

regional scale (r = 0–0.17). The regional scale variability

was significant only for Halicryptus spinulosus (r = 0.11),

Mya arenaria (r = 0.14) and M. balthica (r = 0.18). The

combination of variables at all spatial scales did not

explain the substantially larger proportion of benthic

invertebrate variability than variables at any individual

scale (difference in rall scales combined)any scale = 0–0.05)

(Fig. 4).

In contrast to benthic invertebrates the relationship

between abiotic environment and zooplankton species

was often described by abiotic variability at all spatial

scales studied (depending on the species Spearman rank

correlations varied between r = 0.18 and 0.42). As an

exception, the biomass of bivalve larvae and Pleopsis

polyphemoides in May was only described by environmen-

tal variability at local scale (r = 0.18 and r = 0.19)

(Fig. 5).

Among benthic invertebrates P. femorata, H. spinulosus,

Hydrobia spp., Oligochaeta and Chironomidae larvae were

described only by nutrient load variables (r = 0.18–0.56)

and S. entomon and Hediste diversicolor only by climatic

condition variables (r = 0.17–0.37). Among mesozoo-

plankton, P. polyphemoides and bivalve larvae were

described only by nutrient load variables (r = 0.17–0.18)

and Bosmina maritima and Keratella quadrata by climatic

condition variables in May (r = 0.23–0.27). Pleopsis polyp-

hemoides was explained by nutrient load variables

(r = 0.56) and S. baltica and Cyclopidae by climatic con-

dition variables in August, respectively (r = 0.33–0.37).

All other benthic and zooplankton species were related to

both climatic conditions and nutrient load variables

(r = 0.17–0.63) (Fig. 6). In the biomass models of zoo-

plankton species the contribution of nutrient load vari-

ables increased almost linearly with the contribution of

climatic condition variables (Fig. 7). For some dominant

benthic invertebrate species such as M. affinis, Potamopyr-

gus antipodarum and Theodoxus fluviatilis the links

between environmental variability and biotic patterns

were not statistically significant. For mesozooplankton the

models for Balanus improvisus larvae, Cyclopidae and

Cercopagis pengoi were not statistically significant in May

Fig. 2. Similarity of water bodies according to the benthic and pela-

gic invertebrate communities. Pooled samples collected within each

water body and each year during the late spring (May) were used for

this ordination.

Fig. 3. Ordination of taxonomic groups; pooled samples collected

within each water body and each year during the late spring (May)

were used.

Scale-dependent effects of nutrient loads and climatic conditions Pollumae, Kotta & Leisk

26 Marine Ecology 30 (Suppl. 1) (2009) 20–32 ª 2009 Blackwell Verlag GmbH

and the models for Balanus improvisus larvae, Limnocal-

anus macrurus were not significant in August.

Discussion

The main findings of the study are that (i) the effect of

local and gulf scale environmental variability was impor-

tant on benthic invertebrate communities and (ii) the

variability was mainly due to local nutrient loading, gulf

scale temperature and salinity patterns. In addition, we

found that (iii) zooplankton species were equally affected

by environmental variability at all spatial scales and that

(iv) all nutrient loads and climatic condition variables

contributed to the models of zooplankton species.

This suggests that large-scale pressures such as nutrient

loads and change of climatic conditions may define broad

patterns of distribution but that within these patterns,

small-scale environmental variability significantly modifies

the response of communities to these large-scale pres-

sures. As such, this confirms the recent findings of Hewitt

& Thrush (2009) on the nature of scale-dependent inter-

actions between climatic condition variables and benthic

invertebrate patterns, supports the multiscale theory that

assumes interactions between processes operating over

different scales (e.g. Wu et al. 2000), and can be used to

predict location-dependent responses of the studied

broad-scale factor in the Gulf of Finland. Our study also

suggests that the consistency of effects of broad-scale fac-

tors likely depends on the degree of the small-scale heter-

ogeneity of habitat (models included those local variables

that are known to have large variability) and the develop-

mental characteristics of species (pelagic versus benthic

species, larval development versus direct development)

(Kotta & Witman 2009). Our results show a clear differ-

ence between how benthic invertebrates and mesozoo-

plankton responded to changes in nutrient load and

climatic condition variables. Namely, the predictive power

of the benthic invertebrate model was highest using a

mixture of local and gulf scale variables. In contrast, for

the mesozooplantkton model, all studies scales were sta-

tistically significant.

Increasing nutrient loads are known to lead to higher

abundances and biomasses of benthic invertebrates, but

too high concentrations are known to cause hypoxia and

disappearance of the species (Posey et al. 1999; Kotta

Fig. 5. Separate and combined effects (Rho, BVSTEP) of abiotic envi-

ronmental variables at different spatial scales on zooplankton species.

Only significant relationships are shown.

Fig. 4. Separate and combined effects (Rho, BVSTEP) of abiotic envi-

ronmental variables at different spatial scales on benthic invertebrate

species. Only significant relationships are shown.

Pollumae, Kotta & Leisk Scale-dependent effects of nutrient loads and climatic conditions

Marine Ecology 30 (Suppl. 1) (2009) 20–32 ª 2009 Blackwell Verlag GmbH 27

et al. 2000, 2007; Karlson et al. 2002). Among benthic

invertebrates, Pontoporeia femorata, Oligochaeta, Hydrobia

spp., Halicryptus spinulosus, and Chironomidae larvae

were only related to nutrient load variables. The former

two species are severely decimated at low oxygen levels

and the strong inverse relationship between nutrient load

variables and invertebrates may refer to the negative con-

sequences of hypoxia to the named species. On the other

hand, Hydrobia spp. prefer elevated nutrient loads and

tolerate moderate hypoxia. The latter two taxa are the

typical inhabitants of severe organic enrichment and hyp-

oxic conditions and the positive relationship between

nutrient load variables and biomasses indicates the facili-

tative effect of nutrient loading on the species (Kotta &

Orav 2001; Lauringson & Kotta 2006).

Fig. 7. Relationship (Rho, BVSTEP) between nutrient loads, climatic condition variables and zooplankton species. Only significant relationships are

shown.

Fig. 6. Relationship (Rho, BVSTEP) between nutrient loads, climatic

condition variables and benthic invertebrate species. Only significant

relationships are shown.

Scale-dependent effects of nutrient loads and climatic conditions Pollumae, Kotta & Leisk

28 Marine Ecology 30 (Suppl. 1) (2009) 20–32 ª 2009 Blackwell Verlag GmbH

We are not aware of any studies reporting clear evi-

dence of the links between nutrient load variables and

zooplankton communities in the Baltic and North Sea

areas (e.g. Colijn et al. 2002). There is some indication

that the density of adult Temora longicornis increases with

eutrophication level (Fransz et al. 1992). Besides, nutrient

loading is known to correlate with mesozooplankton

communities in the Gulf of Finland (Pollumae & Kotta

2007). However, the latter study did not take into

account other abiotic factors (e.g. weather patterns, long-

term hydrology) that may be behind this relationship. In

fresh-water ecosystems, nutrient loading is known to raise

the biomass and change the species composition of zoo-

plankton (Ostoji 2000; Kangur et al. 2002; Straile & Geller

1998). In this respect our result on the significant interac-

tions between nutrient load variables and zooplankton

communities in the brackish Gulf of Finland should be

treated as exceptional. Our study not only reports zoo-

plankton total biomass but also takes into account the

community composition. Total biomass, as solely

reported in many other studies, may not capture the links

between nutrient load variables and the responses of sepa-

rate zooplankton species.

Change of climatic conditions is known to cause the

massive blooms of benthic invertebrates (Lawrence 1975),

replacement of key species (Southward et al. 1995) and

other major shifts in community structure (Conners et al.

2002). Among other effects benthic communities are

exposed to severe winter storms and reduced ice scour

under rapidly changing climate (Gutt 2001; Strasser et al.

2001). We are not aware of studies reporting the effects

of climatic conditions on the distribution of benthic spe-

cies in the Baltic Sea.

In our study the distribution of Saduria entomon and

Hediste diversicolor was only related to climatic condition

variables. Similarly, the distribution of Macoma balthica,

Cerastoderma glaucum, Mya arenaria and Gammarus

salinus also had a large component of climatic condition

variability. In contrast, the distribution of these species

was previously thought to be largely regulated by tro-

phic status of the Baltic Sea (e.g. Kotta et al. 2007).

At the same time the population dynamics of the bival-

ves is strongly related to seawater temperatures in

Northwestern European estuaries where a series of

mild winters results in low bivalve recruit densities and

small adult stocks (Philippart et al. 2003). In the North

Sea area, however, low temperatures strongly affect

Cerastoderma edule but cause no increased mortality in

M. arenaria or M. balthica (Strasser et al. 2001). It is

likely that changes in the mean water temperature of

the Baltic Sea are not very important for benthic inver-

tebrates as large seasonal variation counteracts the

potential effects of climatic condition change on water

temperature and the indirect effects of climatic condi-

tions change such as increased wave action, decreased

ice scrape, reduced photosynthetic light intensity (cloud-

iness) and diminished salinity are more important and

potentially affect benthic invertebrates. Practically all our

models demonstrated the strong links between salinity

and biomass patterns of benthic invertebrates referring

to salinity limitation. Most invertebrate species of mar-

ine and fresh-water origin live near to their distribution

limit in the Gulf of Finland. Therefore reduction in

salinity (associated to recent mild winters) has important

consequences for these species. As an exception, S. ento-

mon is a glacial relict and temperature and ice condi-

tions determined the observed pattern of the species

(Leonardsson 1986), whereas the effect of salinity was

not significant.

Earlier studies have clearly demonstrated the links

between climatic condition variables and zooplankton

communities in the Baltic Sea area (Hinrichsen et al.

2007) and established the functional relationships between

temperature, salinity, species composition and biomass of

zooplankton (Ojaveer et al. 1998; Vuorinen et al. 1998;

Mollmann et al. 2000). Piontkovski et al. (2006) demon-

strated that the effect of climatic condition variables on

zooplankton community depended on geomorphology of

the basin; pelagic communities in small basins responded

faster to climatic condition change than those in large

basins. In our study we observed significant relationships

between environmental variability and zooplankton com-

munities at all scales. Thus, differences in geomorphology

of the studied water bodies do not explain the observed

patterns of zooplankton communities. More likely, the

spatial distribution of zooplankton reflects the east–west

gradient in the water circulation patterns of the Gulf of

Finland shown by the statistical significance of salinity

and spring-time temperature in the models of zooplank-

ton species.

To conclude, our study demonstrated that nutrient

loads and climatic condition variables largely explained

the observed patterns in benthic and pelagic invertebrate

communities. The mobility of organisms determined the

relative contribution of small- and large-scale environ-

mental variability to the biomass patterns of invertebrates.

Knowledge on the correlation scales between environmen-

tal and biotic patterns can provide an insight into how

processes generate these patterns. The prevalence of the

key processes, however, is further complicated to an

unknown extent by regional scale variability. We believe

that together with the increase in studies on relationships

between nutrient loads, climatic condition variables and

biotic patterns at multiple spatial scales and in different

regions, meta-analyses (e.g. Gurevitch et al. 2001) can

tackle this problem.

Pollumae, Kotta & Leisk Scale-dependent effects of nutrient loads and climatic conditions

Marine Ecology 30 (Suppl. 1) (2009) 20–32 ª 2009 Blackwell Verlag GmbH 29

Acknowledgements

Funding for this research was provided by target financed

projects SF0180013s08 of the Estonian Ministry of Educa-

tion and by the Estonian Science Foundation grants 6015,

6016, and 7813.

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