rapid assessment of macro algal cover on intertidal sediments in a nutrified estuary

Ž .The Science of the Total Environment 285 2002 97�105

Rapid assessment of macro algal cover on intertidalsediments in a nutrified estuary

D.B. Nedwell�, A.S. Sage, G.J.C. UnderwoodDepartment of Biological Sciences, Uni�ersity of Essex, Colchester, CO4 3SQ, UK

Received 11 March 2001; accepted 23 May 2001

Abstract

Macroalgal blooms have been considered to be an indicator of eutrophication. A new and rapid method isdescribed for the assessment of macroalgal cover in the intertidal zone of estuaries. Macroalgal cover in theintertidal of the nutrient-enriched River Deben estuary was found to reach a maximum of 50% coverage, but thisvaried seasonally with the highest percentage cover during June and July. Macro-algae mats were particularlyassociated with areas of hard substrata providing suitable attachment points, rather than with the nutrientconcentrations along the estuary. The occurrence of macroalgae may be more related to the substrate than to thenutrient status of the estuary. � 2002 Elsevier Science B.V. All rights reserved.

Keywords: Macroalgae; Algal blooms; Percentage cover; Eutrophication; River Deben

1. Introduction

Eutrophication in response to hypernutrifica-tion by nitrogen and phosphorus loads may in-crease the presence and abundance of macroalgal

Žmats within estuaries Munda, 1993; Peckol et al.,.1994; Peckol and Rivers, 1995 , and the occur-

rence of macroalgal mats has been considered asan indicator of eutrophic conditions in estuaries

� Corresponding author. Tel.: �44-01206-872211.Ž .E-mail address: [email protected] D.B. Nedwell .

Ž .see Fletcher, 1996a,b . The occurrence of bloomsŽof macroalgae usually Enteromorpha spp. and�or

.Ul�a spp. in estuaries in response to nutrientenrichment may depress the diversity of the estu-arine fauna and flora and also decrease species

Žrichness Nicholls et al., 1981; Soulsby et al., 1982;Tubbs and Tubbs, 1983; Raffaelli et al., 1987,

.1998; Hartog, 1994 . The main effect of amacroalgal bloom is a blanketing by the algae ofthe sub-stratum which, when the algae decay, maylead to anoxia and sulfide poisoning of the ben-

Ž .thic species Gamenick et al., 1996 . This canhave serious effects on the abundances of other

0048-9697�02�$ - see front matter � 2002 Elsevier Science B.V. All rights reserved.Ž .PII: S 0 0 4 8 - 9 6 9 7 0 1 0 0 9 0 0 - 7

( )D.B. Nedwell et al. � The Science of the Total En�ironment 285 2002 97�10598

estuarine species, e.g. the reduction in diversityand abundance of benthic invertebrates dimin-ishes the numbers and species of wildfowl visiting

Žthose areas covered by macroalgal mats Nicholls.et al., 1981; Soulsby et al., 1982 .

The ability to assess the extent and develop-ment of macroalgal mats is important for theecologically sound management of estuaries andthe coastal zone. Rapid assessment and quantifi-cation of macroalgal mats can be problematic dueto the extent and inaccessibility of the areas overwhich they may occur, and to seasonal and spatialvariability. At present, several techniques are usedfor assessing the abundance of macroalgae. Re-mote sensing by infrared aerial photography is

Žuseful, although expensive Coulson et al., 1980;.Critchley, 1983 and species identification may be

Žproblematic Hubbard and Grimes, 1972; Coulson.et al., 1980; Budd and Milton, 1982 . Other meth-

ods include using randomised quadrats for sam-Ž .pling Coulson et al., 1980; Soulsby et al., 1982

with visual observations transferred to maps forŽsubsequent area estimation Tubbs and Tubbs,

.1983 . However, this requires access to the inter-tidal area, which may be difficult. Here we reporta technique for rapidly assessing visually the ex-tent of macroalgal cover on the intertidal portionof estuaries.

1.1. Study site

Ž .The River Deben estuary Suffolk, UK is anexample of a coastal plain estuary with an area of

Ž .1007 ha Davidson et al., 1991 , a total catchmentarea of 350 km2 and an estimated population ofover 20 000, mainly within the town of Wood-bridge. The estuary is approximately 12 km inlength, running in a northerly direction from thesea at Felixstowe Ferry to its furthest tidal point

Ž .at Melton Mill Fig. 1 . The estuary is within theSuffolk coast and Heaths area of outstanding

Ž .natural beauty AONB and the Suffolk heritagecoast and is also part of the Suffolk River valleys

Ž . Ženvironmentally sensitive area ESA Elliot et.al., 1994 . The Deben estuary has 251 ha of salt

marsh, which stretch from Melton to FelixstoweFerry. The relatively sheltered estuary also con-

Ž .tains extensive areas of mud flat 447 ha on itsinner reaches, with sandy deposits occurring nearthe mouth of the estuary. The Deben estuarysupports a diverse saltmarsh and mudflat commu-nity which includes some uncommon species ofinvertebrate fauna, including the nationally raremolluscs Vertigo augusior and V. pussila. The salt-marsh flora includes three nationally rare species,

Ž .Althaea officinalis Marsh mallow , Salicornea fru-Ž .ticosa Shrubby seablight and Spartina anglica

Ž .Small cordgrass .The estuary has been described as hypernutri-Ž .fied Johnes, 1994 , resulting from high inputs of

nutrients. There are two main treated sewageinputs into the Deben, at Woodbridge and Melton,discharging 4800 and 660 m3 day�1, respectively.The annual input of nitrogen from the STWs is

�1 Ž3.27 Mmoles N year average for 1995 and.1996 . The nitrogen loading to the estuary is 0.76

mol N m�2 estuary area year�1 , not high whenŽ .compared to the Colne estuary 2.19 , the upper

Ž . Ž . ŽGreat Ouse 455 or Wash 1.6 Sage et al.,.1997 . The relatively long freshwater flushing time

Ž .of the estuary is 7�15 days Sage et al., 1997 ,potentially giving rise to conditions suitable fordevelopment of macroalgal blooms. From its

Žplanktonic chlorophyll-a concentrations Burrell.et al. , 1993; Elliot et al., 1994 , the Deben estuary

was claimed to be one of the more eutrophic ofthe Suffolk and Essex estuaries. However, previ-

Žous benthic biological surveys of the estuary El-.liot et al., 1994 showed no clear signs of algal

enrichment. The annual phytoplankton primaryŽ .production is relatively low Dong et al., 2000

presumably as a result of the relatively high tur-bidity of its waters limiting primary production.Enteromorpha sp and Ul�a sp occur throughoutthe estuary and the Deben estuary may be sus-ceptible to macroalgal nuisance blooms as a re-sult of the high nutrient loadings, as has occurred

Žin other nutrified estuaries e.g. Nicholls et al.,.1981; Raffaelli et al., 1998 . Currently, there are

no data on the abundance and distribution ofmacroalgae in this estuary, and the present workwas undertaken to investigate whether the devel-opment of macroalgae reflected the estuary’s sug-gested eutrophic status.

( )D.B. Nedwell et al. � The Science of the Total En�ironment 285 2002 97�105 99

Fig. 1. The estuary of the River Deben, showing positions of sampling sites 1�9.

2. Materials and methods

2.1. Site selection

The sites for this survey were between RamsholtŽ .and Woodbridge Fig. 1 , where extensive macro

Žalgal growth has been noted previously Beardall,.Environment Agency, pers. comm. . No sites were

upstream of Woodbridge Quay as above this pointŽ .was essentially freshwater salinity �1‰ , nor

downstream of Ramsholt Quay as the sedimentshere were shifting sandbanks with no macroalgalcover.

� Site 1: Ramsholt Quay;� Site 2: Prettymans Point;


� Site 3: Pilots Reach;� Site 4: Stonner Point;� Site 5: The Tips;� Site 6: Downstream of Methersgate Quay;� Site 7: Upstream of Methersgate Quay;� Site 8: Kyson Point; and� Site 9: Woodbridge Quay.

2.2. Sur�ey

Sites were surveyed between June and Decem-ber, 1996, covering the seasonal extremes betweenmid-summer and mid-winter. Surveys were car-ried out from the shore at low tide using a tele-

Ž .scope 50� magnification fitted with a cross hairgraticule on a tripod. At each site the telescopewas used to observe five randomly selected fieldsof view along each of five visual transects downthe intertidal on the opposite shore. The tran-sects, running from the high tide mark to the lowtide mark, were selected as follows: the first bypointing the telescope directly across the estuary;the second and third by pivoting the telescope at10� intervals to the left of the original transect;the fourth and fifth by pivoting the telescope thesame degrees to the right of the original transect.Along each transect five fields of view were se-lected by positioning the telescope at the top ofeach transect, then measuring the angle of de-pression to the water line. Dividing the angle ofdepression by 4 gave the degrees of depressionbetween each of the five fields of view. Occur-rence of macro algae at the cross hairs wasrecorded as a ‘hit’. The proportion of ‘hits’ com-pared to ‘misses’ gave an estimate of the percent-age cover by macroalgal mats at each of the sites.No attempt was made to identify algal speciesusing the telescope, it was used only as a meansof assessing presence or absence of algal cover.

The method was compared initially with a‘ground truthing’ survey, carried out concurrently,using 1-m2 quadrats. At each site, the same fivetransects used for the telescope visual methodwere measured from the high tide mark to thelow tide mark and divided to give five quadratsites per transect. Five random quadrats wereused within each site along the transect, giving 25

quadrat estimates per transect. The percentage ofeach quadrat area covered by macroalgal biomasswas determined by visual estimation using cross-wires to sub-divide the quadrat. Identification ofthe species of macroalgae in the quadrats wasalso carried out concurrently.

Water samples were collected at each site oncea month at high tide for 1 full year. The watersamples were immediately filtered through glass

Ž .fibre filters Whatman GF�C and analysed col-Ž .orimetrically for nitrate Kirkwood, 1996 in a

Žnutrient autoanalyser Skalar Analytical B.V.,.Breda, The Netherlands on return to the labora-

tory.

3. Results

In the initial intercomparison between the twomethods, there was no significant differencebetween the estimates of macroalgal cover ob-tained by the visual inspection method with those

Ž 2from the random quadrat surveys � test of.arcsin transformed data, P�0.01, n�400 .

One way analysis of variance on the arcsineŽ .transformed percentage cover data Zar, 1996

was used to compare macroalgal cover betweensites and between seasons. Percentage cover ofthe intertidal zone by macroalgae varied signifi-cantly seasonally, increasing in spring to a peakduring July and decreasing again towards winterŽ . Ž .P�0.001 Fig. 2 . Percentage cover by macroal-

Žgae varied significantly along the estuary P�.0.001 . Post-hoc Tukey tests showed that site 2

Ž .had a significantly higher proportion P�0.01 ofŽ .macroalgal cover maximum 55% than the other

Ž .sites maximum cover 40% , while site 8 had aŽ .significantly lower P�0.02 percentage coverŽ .than the other sites Fig. 3 .

For each of the five transects at a site, the ‘hits’were totalled for the two fields of view in the

Župper shore and lower shore areas giving a possi-ble maximum of 10 ‘hits’ in either upper or lower

. 2shores . � tests showed significant differences inmacroalgal cover between upper and lower shore

Ž .areas along the estuary Fig. 4, P�0.01 but notŽ .seasonally Fig. 5, P�0.1 . During July the algal

cover in the lower shore peaked at sites 6 and 7,


ŽFig. 2. Seasonal changes in the cover of macroalgae in the intertidal of the River Deben estuary average of all sites through the.year, bars show standard errors .

and decreased both up and down the estuary.There were no macroalgae in the lower shore atsite 1. In the upper shore algal cover increased upthe estuary, from site 8 to site 1.

Table 1 shows the occurrence of 11 species ofŽmacro algae. Chlorophyte macroalgae Enter-

Fig. 3. The average cover by macroalgae at each site along theŽestuary mean of all measurements, bars indicate standard

.errors .

.omorpha spp. and Ul�a spp. dominated the com-munities except at site 2, where only brown andred algae were present.

Fig. 6 shows the annual means of nitrate con-centrations at each of the sampled sites along theestuary.

Fig. 4. Comparison of macroalgal cover in upper and lowerintertidal at all sites during June 1996.


Fig. 5. Comparison of macroalgal cover in upper and lowerintertidal areas at site 2, where macroalgal cover was greatest.

4. Discussion

Comparison of the visual inspection methodwith estimation of cover with quadrats showedthat there was no statistically significant differ-ences in the estimates of percentage covers ofmacroalgae. The visual inspection by telescopemethod did not require access onto the intertidalmud and was much more rapid than the quadratmethod. It therefore, provides a rapid and easymethod for assessing macroalgal cover in estuar-ies.

The Deben estuary was relatively species poor,with only 11 species of macroalgae identified

Ž .Table 1 . Estuarine macroalgal species richnesshas been found to range from 5 to 40 species,with richness being negatively correlated to the

Ž .degree of eutrophication Middelboe et al., 1998 .The low species richness in the Deben estuarymay reflect its suggested eutrophicated statusŽ .Burrell et al., 1993; Elliot et al., 1994 . However,

Žmore recent work in the Deben estuary Dong et.al., 2000 indicated that phytoplankton primary

production was relatively low and appeared to belight limited because of the water’s high turbidity.

The visual survey of the Deben estuary showedthat the macroalgae had a distinct seasonal cycle.Percentage cover was highest in July, and de-clined during autumn. The regulation of speciesrichness and abundance of macroalgae in estuar-ies, though complex, is influenced by a variety offactors including salinity, water transparency,nutrient concentration and availability of hard

Ž .substrata Middelboe et al., 1998 . In the Debenestuary there was a strong nutrient gradient in-

Ž . �creasing up the estuary Fig. 6 with NO con-3Žcentrations in the water remained high �25

. ��M throughout the year. NH concentrations4Ž .also were high during summer �20 �M falling

Ž . Ž .during winter �5 �M Sage et al., 1997 . How-ever, it was apparent that there was no correla-tion between the macroalgal cover and the nutri-ent concentration in the water in the estuary.Nutrient-poor, oligotrophic coastal areas are usu-ally dominated by slow growing algae, which at

Table 1Macroalgal species found at each site in the Deben estuary

Species Site

1 2 3 4 6 7 8

�Bryopsis plumosa� �Ceramium sp�Chondrus crispus� �Enteromorpha compressa� � � �Enteromorpha intestinalis� �Enteromorpha sp� � � �Fucus spiralis� � � �Fucus �esiculosus� � � �Gracilaria sp

� �Unknown Rhodophyte onMytilus

� � � � �Ul�a lactuca


Fig. 6. Changes of nitrate concentrations at high tide alongŽthe Deben estuary means of all measurements at each sam-

.pling site, bars indicate standard errors .

low nitrogen concentrations seem more competi-tive than the fast growing but ephemeral bloom-forming species. The bloom-forming macroalgaesuch as Ul�a spp. and Enteromorpha spp. havehigh requirements for NO� and NH�

3 4Ž .Walentinus, 1984; Pedersen and Borum, 1997compared to the slow growing species, caused bytheir high N content per unit biomass at maxi-mum growth rates. However, fast growing speciesseem to take up ammonium and nitrate 4�6 timesfaster per unit of biomass than the slow growingspecies at both high and low concentrations of Nand seem to have higher affinities for both nitrate

Ž .and ammonium Pedersen and Borum, 1997 . Thissuggests that these bloom forming algae shouldperform better in all nutrient conditions than theslow growing, long lived algae, at least in the

Žshort term out competing other species Kautsky,1982; Owens and Stewart, 1982; Pedersen and

.Borum, 1997; Raven, 1995 . However, the slowgrowers seem better able to accumulate nutrientsintracellularly than the ephemerals, carrying themthrough periods of nutrient depletion during the

Ž .summer Raven, 1995 , an advantage lost to thebloom forming algae in the presence of perma-nently elevated nutrient concentrations.

In the Deben estuary, macroalgae occurred onthe upper shore in the lower estuary and on thelower shore areas in the upper estuary. Entero-morpha and Ul�a spp. were only found at the

edges of the saltmarsh, tangled in the saltmarshplants, and wrapped around large stones. At-

Ž .tached species of macroalgae e.g. Fucus spp.were limited to areas which provided suitableattachment points e.g. rocky substratum or gravelbanks and areas with quantities of bivalve shells,which were located predominantly in upper shoreareas. No macroalgae were found on areas ofmud or sand. The mid-section of the estuary hadsediments with a higher percentage of fine sandthan the upper or lower estuary and many areas

Žof shingle, bivalve shells and bivalve beds Sage et.al., 1997 . In particular, site 2, with a rocky sub-

stratum, consistently exhibited the highest per-centage cover of macroalgae, dominated by brownand red algae rather than greens. The rockynature of the substratum at this site may haveprovided shelter from desiccation and tidal actionŽLowthion et al., 1985; Peckol et al., 1994; Peckol

.and Rivers, 1996; Middelboe et al., 1998 . Al-though we do not have direct measurements ofthe number of attached algae at each site, ourdata suggest that the availability of suitable at-tachment points may be more important thannutrient availability in controlling the occurrenceof macroalgae, even in high nutrient estuaries.Therefore, the absence of macroalgal blooms insuch estuaries cannot be taken as an absoluteindicator of acceptable nutrient status.

The macroalgal mats present in the Debenestuary were limited to areas providing suitableattachment points. This contrasts with other areassuch as Langstone Harbour, Chichester Harbourand Portsmouth Harbour where the intertidalmudflats may be completely covered by macro-algae and where such extensive cover has beenattributed to increased discharges of treated

Žsewage effluent Tubbs, 1977; Nicholls et al., 1981;.Tubbs and Tubbs, 1983 . However, in addition to

any effects of algal nutrients, it seems likely thatthe sheltered nature of Langstone Harbour con-tributes greatly to the growth and survival of algalmats. In other less sheltered areas, such as thehypernutrified Ythan estuary and many Danish

Žestuaries, large macroalgal mats also occur Raf-.faelli et al., 1998; Middelboe et al., 1998 , but

higher species richness and abundance have beenfound to be associated with availability of attach-


Žment points or hard substratum Middelboe et al.,.1998 i.e. lack of macroalgal blooms may not be

unequivocal evidence of absence of eutrophica-tion, but presence of macroalgae may also resultfrom availability of attachment sites rather thaneutrophication. However, while bearing thesecautions of data interpretation in mind, our datadoes not indicate that the Deben estuary is sub-ject to large macroalgal blooms resulting fromeutrophication, despite the relatively high nutri-ent concentrations.

The technique reported here allows rapid col-lection of statistically sound data relating tomacroalgal cover of the intertidal portion of estu-aries. The size of the area covered by the crosshairs, and thus inspected for algal presence orabsence, will change with distance. Assuming awidth of 0.25 mm for the cross hair line, and adistance of 4 cm from the cross hairs in thetelescope eye-piece lens from the eye of theobserver, the tangent of the angle � from the eyeto the edge of the cross hair will be 0.125�40�

Ž .0.00315 ��0.18� . The radius of the field ofinspection will be given, therefore, by tan��distance �0.00315�D. At 50 m the inspectedradius will be 15.6 cm, and at 100 m will be 31.5cm. In the Deben estuary, the distance of viewingvaried between approximately 150 and 200 m. Asa measure of the percentage cover at a particularsite, it does not matter that the inspected area

Žchanges the percent of positive or negative hits.will be similarly affected . It will, however, influ-

ence the sensitivity of the size of a solitary patchof alga, or a bare patch of substratum, that will bemeasured and therefore, the lower limit of sensi-tivity of percent cover by this method. The utilityof the method for any particular estuary shouldbe established by ground truthing in that estuary

The rapidity of the technique is such that awhole estuary may be characterised in a matter ofhours, providing information on percentage cov-erage of the intertidal area, position of macro-algae in relation to the high and low water marksand position along an estuary. Longer term sur-veys also catalogue seasonal variation. Percentagemake-up of different sediment types may also beassessed using the reported technique, by record-

ing presence of sand, mud, rocks etc. Combiningthis technique with axial surveys of nutrient con-centrations and of macroalgal species type mayprovide further insight into the factors controllingmacroalgal occurrence and abundance in estuar-ies.

Acknowledgements

The authors wish to acknowledge JulianGreaves and Kevin Young for their assistancewith data collection in the field. We thank the

Ž .Environment Agency Anglian Region, Ipswichand particularly, Mark Johnson, for help to ob-tain environmental data for the Deben estuary.

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rapid assessment of macro algal cover on intertidal sediments in a nutrified estuary

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