patterns of macroalgal species diversity in danish estuaries

457

J. Phycol. 34, 457–466 (1998)

PATTERNS OF MACROALGAL SPECIES DIVERSITY IN DANISH ESTUARIES1

Anne Lise Middelboe,2 Kaj Sand-JensenFreshwater Biological Laboratory, University of Copenhagen, Helsingørsgade 51, DK-3400 Hillerød, Denmark

and

Dorte Krause-JensenDepartement of Lake and Estuarine Ecology, National Environmental Research Institute,

Vejlsøvej 25, DK-8600 Silkeborg, Denmark

ABSTRACT

We analyzed species number of macroalgae in relationto environmental variables at two spatial levels comprising202 individual sites and 26 entire estuaries in Denmark.The species number of macroalgae increased with salinityand declined with nutrient concentrations both at the sitesand in the estuaries. Availability of hard substratum wasassociated with higher species richness at the sites. Thenumber of macroalgal species in the estuaries increasedwith higher mean depth and longer coastline, suggestingthat both the vertical and horizontal extension of the col-onization area are important for the maximum represen-tation of macroalgal species. Mean depth explained as asingle predictor 60% of the variability in species numberin entire estuaries. Estuaries with high mean depth alsotend to be large and have high salinity and transparentwaters due to efficient exchange with open waters. In con-clusion, we find that the regulation of species richness ofmacroalgae in Danish estuaries, though complex, is influ-enced predictably by salinity, water transparency, nutrientconcentration, and availability of hard substrata.

Key index words: estuaries, macroalgae, nutrient concen-tration, salinity, species diversity, substrata

Species diversity of macroalgae and other marineorganisms usually decreases from the entrance tothe inner part of bays and estuaries (Klavestad 1978,Munda 1978, Mathieson et al. 1981, Kautsky and vander Maarel 1990, Kautsky 1995, Nielsen et al. 1995).This overall pattern of macroalgal distribution hastraditionally been explained by physiological restric-tions due to decreasing salinity, while variations inspecies diversity among sites have been explained bydifferent suitability of the substratum for macroalgalcolonization (Klavestad 1978, Mathieson et al. 1981,Coutino and Seeliger 1984). Although salinitystrongly influences the growth and survival of mac-roalgae, it is likely that the species distribution inestuaries is regulated by the interaction of severalfactors, similar to the complex regulation demon-strated for freshwater plants (Møller and Rørdam1985, Rørslett 1991), terrestrial plants (Heikkinen

1 Received 14 October 1997. Accepted 27 February 1998.2 Author for reprint requests; e-mail [email protected].

and Birks 1996), fish (Mandrak 1995), and marinesnails (Fenchel 1975).

The relative importance of different factors in theregulation of species diversity depends on the spatialscale of the analysis. In the Kattegat-Baltic region,we have demonstrated the importance of salinity,physical dispersal barriers, and the suitability of thecoast as habitat for attached plants in explaining thedistribution of macroalgal species (Middelboe et al.1997). At the local scale, dispersal barriers shouldbe less important to the distribution of macroalgaebecause of the short distances involved, while salin-ity should have the same influence as at the regionalscale. The suitability and surface area of rocky sub-strata for colonization should be even more impor-tant for the local diversity of macroalgae because ofthe smaller area available than on the regional scale.The surface area of firm substrata is likely to be par-ticularly important in Danish estuaries where habi-tats for attached macroalgae are confined to stones,rock jetties, and chalky substrata scattered across thesoft seabottom.

Eutrophication is another parameter that maystrongly influence species composition and diversityin the Danish coastal waters. Increased eutrophica-tion with nitrogen and phosphorus may directly in-fluence the presence and dominance of macroalgalspecies and may also limit their growth and depthdistribution through reduced light penetration(Munda 1993, Peckol et al. 1994, Peckol and Rivers1995).

Our main goal was to evaluate the relationshipsbetween species number of macroalgae in Danishestuaries and the following attributes: size of the es-tuaries, salinity, suitability of bottom substratum,and eutrophication. We performed this analysis attwo spatial scales involving either entire estuaries orindividual sites. The analysis involved 202 individualsites in estuaries or coastal areas. The analysis of en-tire estuaries comprised 26 different estuaries eachincluding between 1 and 33 of the sites. All sitesfrom the 26 estuaries, plus about 50 additional sites,were included in the analysis of individual sites. Theinfluence of salinity, proportion of hard substrata,and nutrient concentration on the number of ma-croalgal species were analyzed at the site level. Theinfluence of size of the estuary, area potentially avail-

458 ANNE LISE MIDDELBOE ET AL.

FIG. 1. Locations of the 26 Danish estuaries included in the analysis. Isohalines show the changes in salinity from the Kattegat to theBaltic Sea.

able for colonization, mean salinity, mean nutrientconcentration, and loading rate were analyzed at thelevel of entire estuaries.

MATERIALS AND METHODS

The Kattegat and the Danish belt region constitute the tran-sient area between the high-saline North Sea (33‰) and the low-saline Baltic Sea (3–10‰; Fig. 1). The level of salinity at theentrance to Danish estuaries, therefore, decreases from the es-tuaries connected with Kattegat to those connected to the BalticSea. Secondary salinity reductions take place with distance intothe estuaries producing salinity gradients of variable steepness.The salinity differences are usually small among different siteswithin the individual estuaries (differences between sites rangedfrom 0 to 8‰), while greater variability in mean salinity is ob-served among the different estuaries (differences between estu-aries ranged from 2 to 26‰). The tidal range is small in theentire region (,10 cm). Most of the variations in water level aredue to the influence of wind. Thus, although we use the termestuary, the Danish estuaries are really nontidal with relativelyconstant sea levels and salinities.

The 26 estuaries differed greatly in surface area (Tables 1–3).The largest estuary (1500 km2, Limfjorden) was almost 400 timeslarger than the smallest estuary. The most shallow estuary had amean depth of only 1 m, while the deepest was 23 m. The coastlength of the estuaries varied from 7.6 to 272 km. The predom-inant morainic coasts had a variable proportion of hard substrata.Nutrient concentrations also were variable. Winter concentrationsof nitrate ranged from 6.5 to 20 mmol·L21 and concentrations of

phosphate varied from close to 0 to 9.5 mmol·L21. Secchi-depthsranged between 0.6 and 9 m, reflecting the eutrophic nature ofthe Danish estuaries.

Data acquisition. Data originate from investigations performedin the Danish counties in 1994. Data on species number of mac-roalgae are from 202 sites in the estuaries and coastal areas. Be-cause the frequency of samplings during the year varied amongsites, we included only one sample per site to obtain comparabledata. The last sample before September was chosen as represen-tative, yielding information on the number of macroalgal speciesin June–August. At each site, the taxonomy of all macroalgal spe-cies was recorded by scuba diving along a depth transect fromthe coast to the depth limit of the macroalgae. The number ofmacroalgal species in each estuary was calculated including thespecies observed at all study sites in the estuary. The analysis in-cluded macroalgae belonging to the classes Bangiophyceae, Fu-cophyceae, and Chlorophyceae.

Water transparency, salinity, and nutrient concentrations weremeasured monthly at 1–12 sites in each estuary. The number ofmacroalgal species at the sites was compared to the nearest chem-ical measurements. Each site for chemical measurements repre-sented between one and three sites for sampling of macroalgae.Water chemistry used in the analysis of entire estuaries was cal-culated as mean values of all sites of chemical measurements with-in the estuary. Chemical measurements were carried out accord-ing to Danish Standard, which is based on Grasshoff et al. (1983).Chemical data included in the analyses were time-weighted meanvalues for summer and winter months. The nutrient concentra-tions were described with concentrations of NH4

12N, NO22 1

459PATTERNS OF MACROALGAL DIVERSITY

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TABLE 3. Variability of environmental parameters describing hydrogra-phy, physical features, and eutrophication at sites in Danish estuaries (n5 number of sites included).

Parameter Unit Range n

HydrographySalinity—summerSalinity—winter

‰‰

3.4–31.00.5–29.7

151157

Physical parametersHard substratum—mean val-

ueHard substratum—coeffi-

cient of variation

%

%

0–100

0–165

175

162Eutrophication

Secchi-depth—summerNH4

1-N—summerNO2

2 1 NO32-N—summer

Total-N—summerPO4

32-P—summer

mmmol·L21

mmol·L21

mmol·L21

mmol·L21

0.6–9.10.24–14.60.21–38.615.7–111

0.097–11.5

164157149157157

Total-P—summerNH4

1-N—winterNO2

2 1 NO32-N—winter

Total-N—winterPO4

32-P—winterTotal-P—winter

mmol·121

mmol·L21

mmol·L21

mmol·L21

mmol·L21

mmol·L21

0.52–14.00.21–19.56.5–320

24.1–3910–9.5

0.79–10.3

157156156156157156

TABLE 4. Spearman rank coefficients of correlation (r) describing therelationships between species number of macroalgae and environmentalparameters at 156–175 sites in Danish estuaries. Only correlation coeffi-cients above 0.40 are shown. The correlations were all significant (P ,0.001).

Parameter r

Secchi-depthSalinity—winterTotal inorg. N—winterTotal-N—winterTotal-P—winterTotal-P—summerHard substratum—mean value

0.550.52

20.5020.4820.4720.41

0.40

FIG. 2. The upper figure shows variations in number of ma-croalgal species at the sites in 2.5‰ intervals of salinity. Filledcircles represent mean values in each interval, hatched boxes rep-resent 25%–75% percentiles, and whiskers represent 10%–90%percentiles. The lower figure shows the mean number of ma-croalgal species within Bangiophyceae (●), Chlorophyceae (C)and Fucophyceae (n) at the sites in 2.5‰ intervals of salinity.

NO222N, PO4

322P and total inorganic N (NH412N 1 NO2

2 1NO2

22N concentrations). Total2N and total2P included allforms of organic and inorganic nutrients. The direct annual nu-trient loading of nitrogen and phosphorus supplied with thefreshwater input to the estuaries was calculated as averages for 5years in mmol N and P ·(liter estuarine water)21·year21 (Table 1).

The size of the estuary was expressed as surface area, meandepth, and volume. A special measure of the area potentiallyavailable for colonization by the macroalgae was calculated as thearea between the coastline and the maximum depth limit forgrowth of macroalgae. The maximum depth limit was calculatedfrom the Secchi-depth according to the equation in Sand-Jensenet al. (1994). The area potentially available for colonization rep-resents a maximum estimate, since it was not corrected for theproportion of suitable substrata.

The suitability of the substrata for colonization of macroalgaewas expressed as the percentage of hard substrata at depth inter-vals along the same transects as used for sampling of macroalgae.The mean value of hard substrata for all depth intervals alongthe transect was applied in the subsequent analysis. The coeffi-cient of variation (CV 5 SD/Xmean· 100%) was used to describedifferences in substrata within the transects. Because data for theproportion of hard substratum in entire estuaries were not avail-able, this parameter was only included in the analysis of speciesnumber at the sites.

The relationships between species number of macroalgae andenvironmental factors were analyzed by simple correlation analy-ses, regression analyses, and multiple regression analyses. Theparametric analyses require that the data conform to a normaldistribution. When the initial data did not follow a normal distri-bution, this distribution was obtained by ln, 1/x, or square roottransformation of the data.

RESULTS

Number of macroalgal species at the different sites. Atotal of 126 species of macroalgae were recorded atthe different sites. Among these species, 62 be-longed to the Bangiophyceae, 37 to the Fucophy-ceae, and 27 to the Chlorophyceae. The relation-ships between number of macroalgal species at thesites and the environmental parameters showed rel-atively low coefficients of correlation (Spearmanrank correlation analyses; Table 4). The number of

macroalgal species at the sites was negatively corre-lated with the parameters describing the degree ofeutrophication (total inorganic N in winter, total-Nin winter and summer, total-P in winter and sum-mer, r 5 20.41 to 20.50). By contrast, the numberof macroalgal species was positively correlated toSecchi-depth (r 5 0.55), salinity (r 5 0.52), and thepresence of hard substrata (r 5 0.40) at the sites.

To improve the prediction of the number of ma-croalgal species, we combined the parameters inmultiple regression analyses. Different combinationsof variables in the multiple regression analyses allshowed low amounts of explained variation in num-ber of macroalgal species among the 202 sites.These weak relationships reflect the great variabilityin the data set. This variation arises because manylocal conditions influence the presence of species atthe individual sites.

To reduce the variability, we grouped the data in


TABLE 5. Determination coefficients (r2) and equations describing the relationship between species number of macroalgae and environmental conditionsat 156–175 sites in Danish estuaries. The environmental parameters were divided into intervals, and the relationship between the mean number of species(Sm) and mean values of the environmental variables for these intervals was examined. Units as in Table 3. * P , 0.05, *** P , 0.001.

Paramter Interval Equation r2 P

Secchi-depth (SD)Total inorg. N (TIN)Salinity (SAL)Hard substratum—mean (H)

1 m0.3 ln units2.5‰7.5%

1/Sm 5 0.048 1 0.17 · (1/SD)Sm 5 21.8 2 3.39 · ln TINSm 5 21.3 1 0.42 · SALSm 5 22.8 1 0.018 · H

0.980.800.800.30

**********

FIG. 3. The residuals from the linear regression between thenumber of species and salinity at the sites as a function of totalinorganic N concentration, Secchi-depth, and percentage of hardsubstrata.

intervals for each parameter and used the averagenumber of macroalgal species in each interval in thefollowing regression analyses (Table 5). This pro-cedure was applied to the parameters in Table 4.Since the concentrations of total inorganic nitrogenand total phosphorus were autocorrelated (r 5 0.87,P , 0.00001), the nutrient concentrations were onlyrepresented by one parameter, namely the total in-organic nitrogen concentration in winter. The pro-cedure increased the percentage of variation in spe-cies number accounted for by the parameters, be-cause the variability was deliberately reduced by us-

ing mean values for the intervals. According to thismethod, the average Secchi-depth in 10 intervalscould account for 98% of the variation in the num-ber of macroalgal species, while salinity and inor-ganic nitrogen could account for 80%, and the pres-ence of hard substrata for 30% of the variation.

The mean number of macroalgal species gener-ally increased with increasing salinity, but variationin species number was observed within the salinityintervals (Fig. 2). The increase in number of specieswith increasing salinity was due to an increase innumber of species within the Bangiophyceae andFucophyceae. The mean number of species withinChlorophyceae was relatively constant through thewhole range of salinities. The best predictive modelwas a linear increase of species number with increas-ing salinity, though the number of macroalgal spe-cies tended to saturate at salinities above 20‰. Sa-linities above 20‰ are found in Kattegat, whichserves as the recruitment area for macroalgae to theDanish estuaries and to the Baltic Sea.

After first accounting for the influence of salinityon the number of species, we subsequently exam-ined the influence of the other parameters. Thisanalysis was performed by first finding the residualsbetween the observed and the mean predicted num-ber of species from the measured salinity and thenrelating these residuals to the other selected param-eters (Fig. 3, Table 6). The mean values of the re-siduals in the intervals were used in the regressionanalyses. Parameters describing the degree of eutro-phication such as total inorganic nitrogen concen-tration and Secchi-depth accounted for 53% and39% of the residual variation, and the presence ofhard substratum accounted for 29% of the residualvariation. At a given salinity, the number of macroal-gal species increased, on average, by three to fourspecies with Secchi-depth raised to the 0.5 power.The number of macroalgal species was reduced byabout two species when the concentration of inor-ganic nitrogen increased one ln unit (52.7-fold).Finally, about five more species appeared, on aver-age, when the proportion of hard substrata in-creased from 30% to 80%.

We also analyzed the residual variation betweenthe observed and the mean number of species pre-dicted from the Secchi-depth. Total inorganic nitro-gen concentration and salinity accounted for 55%and 41%, and the presence of hard substrata for24% of the residual variation, suggesting that salin-


TABLE 6. Statistical data for regression analyses between residuals (DS) from the linear regression between number of species and salinity and variousparameters. DS: Residuals, the difference between number of macroalgal species observed at the sites and the number expected based on the salinity, unit:number of species. DSm is the mean value of residuals in the shown intervals. Units as in Table 3. * P , 0.05, ** P , 0.01.

Parameter Interval Equation r2 P

Total inorg. N (TIN)Secchi-depth (SD)Hard substratum (H)

0.3 ln units1 m7.5%

DSm 5 5.9 2 2.1 · 1n TINDSm 5 24.8 1 3.6 · SD0.5

DSm 5 22.8 1 0.10 · H

0.530.390.49

**0.052

*

FIG. 4. The relationship between the number of macroalgal spe-cies (S) in the estuaries and the mean depth (MD, meter) of theestuaries. The line represents the regression equation S 5 3.8 15.3 · ln(MD).

ity, nitrogen concentration, water transparency, andproportions of hard substrata are all directly in-volved in the regulation of macroalgal diversity atthe sites.

Number of macroalgal species in different estuaries. Be-tween 4 and 41 species of macroalgae were recordedin the 26 estuaries. The mean depth of the estuarieswas the single parameter that explained most of thevariation (r 2 5 0.60) in number of macroalgal spe-cies among estuaries (Fig. 4, Table 7). We alsofound significantly positive relationships betweenthe number of macroalgal species and the volumeof the estuary, the salinity, the length of the coast,and the surface area of the estuary. The number ofmacroalgal species decreased significantly with in-creasing loadings of N and P via the supply of fresh-water. The volume of the estuary was strongly cor-related with the length of the coast and the surfacearea of the estuary, but volume better predicted thenumber of macroalgal species in the estuaries, pre-sumably because it is related to the mean depth ofthe estuary.

The combination of mean depth, salinity, and vol-ume of the estuary could account for 79% of thevariation in number of macroalgal species in the es-tuaries in multiple regression analysis (Fig. 5, Table8). Due to the high correlation between volume andsurface area, a similarly high percentage of variabil-ity was accounted for if volume was replaced by sur-

face area of the estuaries in the model. The numberof macroalgal species increased on the average by7–10 species when the mean depth increased oneln unit (52.7 times). On average, one more speciesappeared when salinity increased by 1‰ and two tothree more species appeared when the size of theestuary increased 2.7-fold in volume or area.

When mean depth and area of the estuary wereexcluded as independent parameters in the model,salinity and nitrogen loading in combination ac-counted for most of the variation (r 2 5 0.73) innumber of macroalgal species in the estuaries. Salin-ity and nitrogen loading were not correlated (r 50.004). The variance explained by salinity and nitro-gen loading in combination was high, compared totheir importance as individual predictors (Table 7),and implies that both variables were important pre-dictors for the number of macroalgal species in theestuaries.

DISCUSSION

The species number of macroalgae was analyzedat two spatial levels comprising 202 individual sitesin the estuaries and 26 entire estuaries. Salinity andinorganic nitrogen were strong predictors of thespecies number of macroalgae both at the level ofsites and estuaries. The proportion of hard substratawas also important as a predictor of the species num-ber at the sites. In entire estuaries, the species num-ber was most strongly correlated to the mean depthof the estuary, which accounted for 60% of the vari-ability. By including two or three independent vari-ables simultaneously, we could better account forthe variability in species number among the 26 es-tuaries. However, the mechanisms by which the vari-ables influence species richness are systematicallydifferent. Salinity influences species richness by de-fining the proportion of the regional species poolthat potentially can grow within the estuary (Fig. 2),while the other variables influence the realized spe-cies richness. Mean depth and surface area set thevertical and horizontal extension of macroalgal col-onization. Enhanced nitrogen loading restricts lightavailability and depth penetration of the macroalgaeby stimulating the growth of phytoplankton, epi-phytes, and ephemeral macroalgae, which can ben-efit from the excessive nutrient supply (Littler andMurray 1975, Lazaridou et al. 1997).

Importance of salinity. Many previous studies havedemonstrated the importance of salinity for the re-gional distribution of species composition and di-


TABLE 7. Determination coefficients (r2) and equations describing the relationships between the total species number of macroalgae in the estuaries (S)and various environmental parameters. Only significant relationships are shown. Units as in Tables 1 and 2. * P , 0.05, ** P , 0.01, *** P ,0.001.

Parameter r2 Equation P

Mean depthVolumeN-loadingP-loadingSalinity—summer

0.600.500.470.430.35

S 5 3.9 1 11.5 · ln(Mean depth)S 5 27.6 1 4.5 · ln(Volume)S 5 58.5 2 4.7 · ln(N-loading)S 5 41.9 2 4.6 · ln(P-loading)S 5 25.1 1 1.6 · Salinity—summer

***************

Salinity—winterNH4

1-N—summerSurface area of estuariesLength of coast

0.280.250.210.21

S 5 2.1 1 1.0 · Salinity—winterS 5 16.9 1 5.5 · ln(NH4

1-N—summer)S 5 6.0 1 3.5 · ln(Area)S 5 22.9 1 6.5 · ln (Length of coast)

*****

TABLE 8. Multiple linear regressions describing the relationship betweenthe species number of macroalgae in the estuaries (S) and different envi-ronmental parameters. r2: Coefficient of determination, MD: mean depth(m), Sal: salinity-summer (‰), V: volume of the estuary (km3), A: surfacearea of the estuary (km2). Units as in Tables 1 and 2. The regressionmodels were all significant (P , 0.001).

Model r2

(I) S 5 23.3 1 7.3 · ln(MD) 1 1.1 · Sal 1 2.6 · ln(V)S 5 220.5 1 9.7 · ln(MD) 1 1.1 · Sal 1 2.5 · ln(A)

(II) S 5 32.3 1 1.1 · Sal 2 4.7 · ln(N-loading)

0.790.780.73

FIG. 5. The relationship between number of species observedin the estuaries and number of species predicted by multiple lin-ear regressions. Independent parameters include mean depth, sa-linity, and volume of the estuaries in model I and salinity and N-loading in model II (Table 8).

versity along salinity gradients in large estuaries andestuarine complexes (length 100–1000 km, Klaves-tad 1978, Munda 1978, Mathieson et al. 1981, Cou-tino and Seeliger 1984, Kautsky 1995, Middelboe etal. 1996). Salinity also influenced species richness ofmacroalgae at single sites and in small estuaries(length 8–100 km) included in this study, but lightand nitrogen availability were of similar importanceat both spatial levels. The influence of mean depthon species diversity in the estuaries also was strong.Thus, shallow depths combined with a high level ofeutrophication in the inner estuaries contribute tothe reduction in macroalgal species number.

Salinity in Danish estuaries is influenced both bythe regional pattern of decreasing salinity fromnorth to south in the Kattegat-Baltic region and bythe local salinity reduction from the outer to theinner parts of the estuaries. The salinity in the openwaters decreases from about 23‰ in the westernKattegat to 8–9‰ in the western Baltic Sea, whilethe number of macroalgal species in the region de-creases from 318 to 128 (Nielsen et al. 1995). This

regional difference appears to have little influenceon the number of macroalgal species in the estuar-ies along the north-south gradient. If salinity hadbeen essential, the northern estuaries, connected tothe high-saline Kattegat, would have held the mostspecies. In fact, the species number in the salineLimfjord to the north (26‰, 41 species) was similarto that of the less saline Flensborg Fjord to the south(14‰, 36 species).

The strong influence of factors other than salinityalso was reflected by the variation in species richnessamong sites located within the same narrow salinityranges (Fig. 2). Large variations were distinct whenthe number of species in this analysis was comparedwith the number of species around the island ofBornholm (sites not included in this analysis). Thus,while the mean species number was 6.6 (at 7 out of9 stations the number was below 8) among sites withsalinities between 7.5 and 10‰ (Fig. 2), the meannumber was 14 (with only one of 17 sites having lessthan 10 species) around the island of Bornholm inthe western part of the open Baltic Sea at a salinityof 7.3‰. The stable salinities around Bornholm,the exposed rocky shores suitable for algal attach-ment, and the transparent waters allowing all pos-sible vertical algal zones to be represented may ex-plain why the species number is high at Bornholmcompared to most other sites of similar salinity. Thesignificantly positive influence of high Secchi-trans-parency, low nutrient loading, and high percentageof hard substratum on the residual variation of spe-cies number within salinity intervals is also demon-strated by Figure 3.

Species-area relationships. Regions of large surface


area tend to have more habitats and more individ-uals than small regions (Rosenzweig 1995). Areasincluding many individuals also tend to hold morespecies and in larger populations than small areas,thereby reducing the risk of species extinction dur-ing unfavorable periods (Kohn and Walsh 1994).Moreover, if a species disappears, the possibility forreproductive units to recolonize from neighboringregions will be higher when a larger area is available.These influences of surface area have been dem-onstrated on numerous occasions with terrestrial(e.g. Williams 1943, Diamond 1974, Simberloff1976) and freshwater organisms (Møller andRørdam 1985, Rørslett 1991, Taylor 1996). In thepresent study, the species number of macroalgaealso increased with the mean depth, the surface areaand the coast length of the estuaries, and the pro-portion of suitable substrata. Estuaries with a highmean depth tend to have a long coastline and alarge surface area for macroalgal growth and in-clude more exposed sites where different verticalmacroalgal zones are represented. At the same time,deep estuaries tend to have a high rate of water ex-change with open coastal waters and, thereby, ob-tain a higher salinity, lower nutrient loading, andhigher Secchi-transparency than shallow estuaries.The influence of surface area on species richness is,however, expected to be weaker in the marine wa-ters than on the continents because the geographi-cal barriers to dispersal are generally weaker and thespecies more widely distributed in the oceans (Rap-oport 1994).

The fact that the number of macroalgal specieswas related to mean depth, surface area, and coastlength suggests that both the vertical and horizontalextension of the colonization area are important forthe regulation of species richness. The vertical ex-tension of algal growth can be particularly impor-tant for species richness because it allows for specieswith different adaptations, tolerances, and biotic in-teractions to be represented. Deep and large estu-aries with transparent waters and exposed coastsshould permit the maximum vertical developmentof the algal zones, while small shallow estuaries withturbid waters should have vertically compressed al-gal zones or even some zones excluded. In the tide-less Danish estuaries, the vertical extension canrange from a maximum of 10–15 m with a cleardepth zonation of green, brown, and red algae to aminimum of 0.5 m with only green algae represent-ed. In our study, a certain proportional increase inthe vertical distribution of macroalgae apparentlygenerated more new habitats and allowed more spe-cies to be present in the estuaries than the sameproportional increase in the length of the coast line.Thus, when the mean depth increased one ln unit(52.7-fold), about 12 more species appeared,whereas only two to three more species appearedwhen the surface area increased by the same relativemagnitude.

Influence of eutrophication. The distribution pat-terns of salinity and nutrient concentrations are of-ten inversely related because freshwaters are com-monly richer in nutrients than saline waters. In thelarge data set presented here, however, it was pos-sible to document the effects of eutrophication sep-arately from the effect of decreasing salinity.

Eutrophication can influence the macroalgalcommunity by reducing the amount of light avail-able for growth and by triggering a shift in speciescomposition. Increased light attenuation in the wa-ter column can diminish the number of macroalgalspecies at the sites (Table 5) by restricting the ver-tical extension of algal colonization. Increased nu-trient concentrations also favor the development ofopportunistic fast-growing species with a short life-time (Isaksson and Phil 1992), which are believedto eliminate other species through strong competi-tion for light and space. The macroalgal communi-ties present at very eutrophic conditions are lesscomplex than the species-rich communities devel-oped under more oligotrophic conditions. Species-rich communities often have a higher functional di-versity, including both canopy forming species andan understory of small macroalgal species.

Indeed, the decline of macroalgal biodiversity atthe highly eutrophic estuarine sites would have beeneven more profound than was observed if we hadused a measure including structural or taxonomicdiversity of the macroalgal communities as well (viz.Warwick and Clarke 1995). High taxonomic diver-sity and many thallus forms among red, brown, andgreen algae are commonly represented under un-polluted conditions, while the highly eutrophic sitesmay contain only filamentous and thin fronds ofgreen algae (Peckol et al. 1994, Peckol and Rivers1995). Hence, combined measures of biodiversity in-cluding species number, morphological diversity,and taxonomic diversity are likely to provide a moresensitive description of the site-specific differencesin macroalgal communities and a better account ofthe influence of light, salinity, nutrients, and bottomsubstrata than species number alone.

Concluding remarks. Our results show that speciesrichness of macroalgae at Danish estuarine sites isregulated by salinity, availability of hard substrata forattachment, water transparency, and nutrients. De-spite the complexity of regulation, it is nonethelesspossible to obtain a relatively accurate prediction (r 2

5 0.73–0.79) of the number of macroalgal speciesin the estuaries based on their mean depth, surfacearea, and salinity, or their salinity and nitrogen load-ing. However, manipulative experiments are neededto verify cause and effect relationships between en-vironmental parameters and species richness. Weforesee that more accurate and sensitive descrip-tions of the variability of biodiversity in macroalgalcommunities among sites can be obtained if, in ad-dition to species richness, the taxonomic and mor-


phological diversities of the species are included infuture studies.

This work was supported by grants from the Danish ResearchAcademy to A.L.M. and from the European Commission (MAS 3-CT98-0160) and the Danish Natural Science Foundation to K.S.J.We thank Poul M. Pedersen and Aase Kristiansen for continuoussupport and Lena Kautsky and Klaus Brodersen for comments tothe manuscript.

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patterns of macroalgal species diversity in danish estuaries

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