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Estuarine, Coastal and Shelf Science 87 (2010) 27–32

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Estuarine, Coastal and Shelf Science

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Effects of different types of mechanical disturbances on a charophytedominated macrophyte community

Kaire Torn*, Georg Martin, Jonne Kotta, Maarit KuppEstonian Marine Institute, University of Tartu, Maealuse 10a, 12618 Tallinn, Estonia

a r t i c l e i n f o

Article history:Received 5 October 2009Accepted 8 December 2009Available online 22 December 2009

Keywords:Baltic Seacharophytesdisturbancesensitivityrecovery

* Corresponding author.E-mail address: kaire.torn@ut.ee (K. Torn).

0272-7714/$ – see front matter � 2009 Elsevier Ltd.doi:10.1016/j.ecss.2009.12.006

a b s t r a c t

Charophytes are unique and endangered macroalgae. Mechanical stress is known to damage charophytecommunities, however, virtually nothing is known how such disturbance affect seasonal succession andrecovery of charophyte communities. We examined the response of a shallow water charophytecommunity to different types and timing of disturbances by conducting seasonal in situ field experimentin a brackish water ecosystem. The disturbances associated with mechanical removal of vegetation orsediment had the largest impact on the charophyte community. Disturbances that only partly damagedthe plants had minor effects and communities were characterized by fast recovery. The timing ofdisturbance had significant effects on the charophyte community with stronger effects when disturbed atthe early stage compared to mid-stage of seasonal succession.

� 2009 Elsevier Ltd. All rights reserved.

1. Introduction

Charophytes form a highly evolved, unique group of benthicmacroalgae. These plants are aquatic, and modern forms are foundin many freshwater to brackish habitats such as ponds, lakes,lagoons and streams (Krause, 2008). Charophyte communities areimportant habitat for a number of invertebrate and macrophytespecies and they provide important feeding and nursery areas forseveral species of fish and birds (Dugdale et al., 2006; Schmiederet al., 2006). Such habitats are often inherently fragile and thereforeprone to different types of disturbance.

In the Baltic Sea charophytes dominate shallow and shelteredsoft bottom areas together with phanerogams (Mathieson andNienhuis, 1991). Such habitats are nowadays threatened by bothdirect human exploitation and increased pressure from thedrainage area (e.g. Munsterhjelm, 2005). It has been argued thatamong other factors mechanical stress and destruction of habitatsare behind the recent decline of the number of species, distributionarea and biomass of charophytes (Yousef et al., 2001; Schubertet al., 2003; Munsterhjelm, 2005). Influence of mechanical stress onthe charophytes of the Baltic Sea has been assessed using a correl-ative approach (Yousef and Schubert, 2001; Munsterhjelm, 2005).There are only a few manipulative studies observing the recoverypotential of charophyte communities following different types ofdisturbances in a lake ecosystem (Harwell and Havens, 2003;

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Havens et al., 2004) but there are no experimental studiesaddressing the causative links between mechanical disturbanceand the structure of charophyte communities.

Trampling, boating, anchoring are the most common anthro-pogenic disturbances and ice scrape and elevated herbivory arethe most common natural disturbances. The effects of humantrampling, motorboat and scooter traffic, and motorboatanchoring on submerged macrophytes have been primarilyassessed on rocky shore communities (Brosnan and Crumrine,1994; Keough and Quinn, 1998), tropical coral reefs (Hawkins andRoberts, 1993; Francour and Koukouras, 2000) and seagrassmeadows (Eckrich and Holmquist, 2000). All these studies reportstrong influence of mechanical disturbance on nearshore marinealgal and invertebrate communities. Regular fluctuations in waterlevel in the sheltered bays during winter create disturbancecomparable to pack ice in the exposed shores. Therefore, icedisturbance is not uncommon in the charophyte habitats (Kottaet al., 2008). Ice scrape is expected to mix the sediment surface orin extreme cases even to remove the upper sediment layer. Suchdisturbances have potential deleterious effects on charophytecommunities. In addition, grazing by waterfowls can be alsoa factor that leads to the decrease of charophytes. In lakes therehas been reported a strong reverse correlation between theabundance of waterfowls and the occurrence of charophytes.Ultimately waterfowls were able to oust charophytes down to 2 mdepth (Noordhuis et al., 2002; Schmieder et al., 2006). Theforaging of herbivorous birds can affect the topmost parts ofcharophyte thallus, disturb upper sediment layer, roots ordemolish propagule bank of vegetation (Nacken and Reise, 2000;

Fig. 1. Location of study area.

Table 1Timing of disturbances (O) and sample collection (X) in our experiment.

06 07 08 09 10 072007 2007 2007 2007 2007 2008

Timing 1 O X X X X XTiming 2 O X X X X

K. Torn et al. / Estuarine, Coastal and Shelf Science 87 (2010) 27–3228

Van den Berg et al., 2001). Similarly, there exists some circum-stantial evidence on the high grazing pressure on charophytes insome parts of the Baltic Sea area (Schubert et al., 2003). Besidesherbivorous birds invertebrate invertebrate grazing in macrophytebeds may play a major role in controlling the growth of vegetation(Paalme et al., 2002; Orav-Kotta and Kotta, 2004; Kotta et al.,2006; Orav-Kotta et al., 2009).

Thus, disturbance of the structure of charophyte communitiescan shift the stability of soft bottom ecosystems and have severeimpacts on nearshore biodiversity and functioning. Despite oftheir functional importance virtually nothing is known howdifferent types of disturbance affect seasonal succession andrecovery of charophyte communities. Recoveries of other macro-algae depend on intensity and extent of the disturbance, theirinteractions with communities (Benedetti-Cecchi and Cinelli,1996; Kim and DeWreede, 1996; Milazzo et al., 2002b, 2004;Konar, 2007; Herkul and Kotta, 2009; Kotta et al., 2009), and arerelated to species competitiveness and successional stage ofcommunity (Benedetti-Cecchi and Cinelli, 1996; Creed and AmadoFilho, 1999). Thus, the magnitude of effects on charophytecommunities is also expected to largely vary among differenttypes and timing of disturbances.

The objective of this paper was (1) to evaluate experimentallythe response of charophyte community to different types andtiming of disturbances and (2) to assess the potential recovery ofthe charophyte community in a period of one year. We predict thatthe disturbances associated to sediment reworking result largesteffect sizes and are characterized by longest recoveries. We alsopredict that timing directly affects the outcome of disturbance. Thestrongest effects are expected for communities disturbed whenthey are well developed. Such communities do not have enoughtime to re-establish in the current growing season and thereforeare also expected to perform poorly in the following vegetationperiod.

2. Materials and methods

2.1. Study area

Rame Bay is a shallow and semi enclosed bay in the in the northeastern Baltic Sea (Fig. 1). The bay receives the waters of the West-Estonian Archipelago Sea which is regarded as frontal zone betweeneutrophic waters of Gulf of Riga and less eutrophied waters of thenorthern Baltic Proper (Suursaar et al., 1998). The maximum depthof the area is 1.5 m but most of the bay is shallower than 1 m. Thebottom is composed of fine sand and thick layer of fine fractionedsilt. Salinity varies 3–5 and is highly dependent on rainfall. Beingsheltered Rame Bay provides excellent habitat for luxurious char-ophyte populations together with aquatic phanerogams. The mostwidespread species is Chara aspera Willd., which covered the entiresheltered part of the bay (Torn and Martin, 2003).

2.2. Experimental procedure

The experiment was carried out from June 2007 to July 2008.Experiment was established within a dense Chara aspera commu-nity with plot sizes of 1.5�1.5 m. Mechanical disturbance treatmentinvolved the following levels: 1) cutting the tips off plants 2) removalof plants 3) mixing of the sediment surface layer 4) removal of thesurface sediment layer 5) control (i.e. undisturbed plots). We useda full random design when establishing the experiment. For the firsttreatment the upper 5 cm of the vegetation was cut by diver. For the

Table 2Repeated measures ANOVA multivariate test of significance about the effect of timing and disturbance on the biomasses of different macrophyte groups in 2007–2008.

df Total biomass Charophytes Filamentous algae Vascular plants

Wilks’ value F p Wilks’ value F p Wilks value F p Wilks’ value F p

Timing 4 0.136 20.68 0.0000 0.101 28.99 0.0000 0.304 7.46 0.0024 0.371 5.95 0.0052Disturbance 16 0.004 13.51 0.0000 0.001 22.87 0.0000 0.062 3.75 0.0003 0.170 2.13 0.0245Disturbance� Timing 16 0.046 4.39 0.0001 0.011 8.41 0.0000 0.085 3.13 0.0017 0.128 2.60 0.0063Intercept 4 0.012 271.12 0.0000 0.012 259.10 0.0000 0.050 62.15 0.0000 0.150 19.77 0.0000

K. Torn et al. / Estuarine, Coastal and Shelf Science 87 (2010) 27–32 29

second treatment plants were removed gently by hands. These twotreatments mimic the foraging of herbivorous birds. For the thirdtreatment sediment was mixed together with vegetation approxi-mately to 0.1 m depth. Mixing of the sediment surface layer was usedto imitate the influence of motorboat anchoring, running of scootersand/or trampling. And finally for the fourth treatment sedimentlayer was removed till 0.15 m depth. The removal of sediment layerrepresents disturbances due to dredging and/or ice scrape. In orderto assess the effect of the timing of disturbance half of the treatmentswere mechanically disturbed in June 2007 (timing 1) and theremaining half in July 2007 (timing 2). Sampling of benthic vege-tation was carried out monthly from June to October 2007 and in July

Fig. 2. Seasonal variation in average total macrophyte biomass�

2008 (Table 1). For each treatment three replicate biomass sampleswere collected by SCUBA diving using a 20� 20 cm frame. Each plotwas sampled only once. Samples were stored at �20 �C. In thelaboratory all species were determined to the species level. The dryweight of species was obtained after drying the individuals at 60 �Cduring two weeks.

2.3. Statistical analyses

Repeated measures ANOVA (StatSoft, 2007) was used to comparethe effect of different types of disturbances (levels: tips cut, plantsremoved, sediment mixed, sediment removed and control) and

S.E for the studied disturbance treatments in 2007–2008.

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100

70

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91

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91

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72

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72

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72

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82

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20

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200

72

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82

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72

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72

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72

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Tim

ing

1C

vsTC

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K. Torn et al. / Estuarine, Coastal and Shelf Science 87 (2010) 27–3230

timing of disturbance (levels: June 2007 and July 2007) on biomassesof macrophyte species and biomass share of charophytes amongdifferent months (from July 2007 to July 2008). The Mauchly Sphe-ricity test was used to check the assumption of equality of variance.We used the following multivariate tests to seek the statisticalsignificance of different types of experimental disturbances onvegetation biomass: Wilks’ lambda, Pillai–Bartlett trace and Hotel-ling–Lawley trace tests. These tests were used as they do not makethe strict, often unrealistic, assumptions about the structure of thecovariance matrix. As all these tests resulted in similar significances,only the output of the Wilks’ lambda test (as the most commonlyused) was reported. Post-hoc Bonferroni tests were used to analysewhich treatment levels were statistically different from each other.

3. Results

Total biomass of macroalgae in the undisturbed plots rangedbetween 9 and 227 g dw m�2. The highest biomass values wereobserved in July and the lowest values in October. A major part ofbiomass was composed by Chara aspera. Besides C. aspera theundisturbed plots contained mainly the chlorophytes Cladophoraglomerata (L.) Kutz. and Ulva intestinalis L. and the higher plantsNajas marina L. and Potamogeton pectinatus L. The higher plantsZannichellia palustris L. and Myriophyllum spicatum L. and thecharophyte Chara canescens Desv. et Loisel. in Loisel. were notfound in control treatment but were found on the disturbed plots.

The biomasses of benthic macrophytes were dependent on thetype, timing of disturbance and their interaction (Table 2). In thefirst year of the experiment the disturbed communities hadsignificantly lower biomasses compared to control communities(Fig. 2). The cutting of macrophyte tips had weakest effect whereasthe removal of algae and sediment had the strongest effect onmacrophyte biomasses (Fig. 2, Table 3). During the first year of theexperiment macrophyte community did not recover in plots weresediment was removed; only small amounts of drifting algae werefound. When macrophytes were removed at the early stage ofseasonal succession (June) a partly recovery was observed twomonths after the disturbance. Such plots were covered by smallamounts of Najas marina with the epiphytic Ulva intestinalis.However, when macrophytes were removed at the mid-stage ofseasonal succession (July) only a decrease of biomass was observedand communities did not practically recover in the first year of theexperiment. In general macrophyte removal plots were character-ized by a decreased share of charophytes and often an increasedshare of higher plants compared to control treatments.

In the second year of the experiment (2008) we could stillobserve a negative influence of disturbances on communitybiomasses (Table 4). Compared to undisturbed area charophytebiomass had been reduced considerably in areas were sediment orplants were removed (Table 5). As differences in total biomass werenot remarkable between treatments main effects were due todecreased share of charophytes under disturbance. When thecommunity was disturbed at the early stage of seasonal successionthe share of charophytes on the heavily disturbed plots (sedimentand vegetation removed) in 2008 ranged between 25 and 29%compared to the values of 80–91% in moderately and undisturbedplots (Fig. 3). The differences between heavily and moderatelydisturbed plots were less severe for the community disturbed at themid-stage of seasonal succession.

4. Discussion

Our experiment showed that mechanical disturbance directlyaffected the studied charophyte community. In general, distur-bance had a significant effect on the variability of benthic

Table 4ANOVA univariate test of significance about the effect of disturbance and timing on the biomasses of different macrophyte groups in 2008.

df Total biomass Charophytes Filamentous algae Vascular plants

MS F p MS F p MS F p MS F p

Timing 1 188.95 0.11 0.7390 6391.905 12.39 0.0023 3144.192 6.31 0.0212 74.926 0.23 0.6400Disturbance 4 3400.09 2.06 0.1268 10,632.789 20.62 0.0000 665.048 1.33 0.2935 676.220 2.04 0.1279Disturbance� Timing 4 4566.17 2.76 0.0577 4847.418 9.40 0.0002 918.709 1.84 0.1622 716.689 2.16 0.1111Intercept 1 424,673.31 256.97 0.0000 159,501.717 309.27 0.0000 39,696.785 79.65 0.0000 2770.753 8.34 0.0091

K. Torn et al. / Estuarine, Coastal and Shelf Science 87 (2010) 27–32 31

macroalgae and the extent of the impact varied among differentdisturbance levels. The treatments associated to the removal ofsediments and macrophytes appeared particularly susceptible toadverse impacts of disturbances. Similarly, the timing of distur-bance had significant effects on the charophyte community withstronger effects observed for those communities disturbed at themid-stage compared to earlier stage of macroalgal seasonalsuccession. As such our results fully agreed with our predictions.

Our results also demonstrated that under the most severedisturbances (removal of sediment and macrophytes) the char-ophyte community did not recover in a period of one year. Although,the biomasses did not statistically differ among treatments, theshare of charophytes was significantly reduced compared to controltreatments. It is known that benthic communities with three-dimensional structure (i.e. dominated by canopy-forming vegeta-tion) are sensitive to mechanical stress. Soft bottom areas areparticularly vulnerable to trampling and anchoring (Eriksson et al.,2004) where the canopy-forming vegetation could be easilydestroyed (Milazzo et al., 2002b). Areas with high level of tourism orwaterfowl grazing vegetation are highly threatened (Eckrich andHolmquist, 2000; Milazzo et al., 2002a; Eriksson et al., 2004). Ingeneral, other macrophytes were less severely affected bymechanical disturbance as their recoveries were much faster. Suchrapid recovery potential is expected due to the short generation timeand fast growth of filamentous algae and higher plants (King andSchramm, 1976).

The result of the present study indicates that the moderate levelof herbivory (removal of macrophyte tips) had negligible effect oncharophytes. However, under the severe herbivory (removal of allvegetation) significant effects were observed even in the followingvegetation period. Earlier experiments have also shown that recov-eries are related to the intensity of disturbance (Eckrich and Holm-quist, 2000; Milazzo et al., 2002b). Depending on the availability ofalternate food source herbivorous birds either consume part of thevegetation closest to the surface or destroy the whole vegetationwith roots and rhizomes (Nacken and Reise, 2000; Hori et al., 2006).

Several factors are known to affect the processes of macrophyterecolonization. The size of the disturbed area and timing of thedisturbance can influence the sequence of recovery (Kim and

Table 5Bonferroni adjusted p-values for multiple comparison among treatments of theunivariate ANOVA in 2008 (C – control, TC – tips cut, VR – vegetation removed,SM – sediment mixed, SR – sediment removed).

Total biomass Charophytes Filamentous algae Vascular plants

Timing 1C vs TC ns ns ns nsC vs VR ns <0.01 ns nsC vs SM ns ns ns nsC vs SR ns <0.01 ns ns

Timing 2C vs TC ns ns ns nsC vs VR ns <0.05 ns nsC vs SM ns ns ns nsC vs SR ns <0.05 ns ns

DeWreede, 1996). In our case the size of the sediment removal plotwas relatively small (2.25 m2) and regenerated layer of thesubstrate was likely transported from adjacent areas by storms inautumn and winter. Together with a recovery of sediment structurethe pool of hibernating material of the vegetation was also recov-ered, although the share of charophytes in vegetation was signifi-cantly lower compared to undisturbed plots. Lower share ofcharophytes can be explained by the competitive interactions at theearly stage of macroalgal succession. The efficiency of recovery isspecies-specific (Eckrich and Holmquist, 2000). Namely, higherplants are known to have earlier seedling and better competitionfor light giving them advantages compared to charophytes in thehabitat recovery process (Van den Berg et al., 1998).

Charophytes can hibernate as oospoores, vegetatively as bulbilsor parts of overwintering thalli (Martin et al., 2003). The impor-tance of oospores as hibernacles is poorly known e.g. only someobservations in the Baltic Sea (Nielsen, 2003). The above-groundsections of Chara aspera usually degrade already in early autumn(Martin et al., 2003; Kotta et al., 2004) and the overwintering matsof detached charophyte are only irregularly and locally observed(personal observation). Thus, it has been suggested that C. asperamainly hibernates as bulbils i.e. bulb-shaped body usuallyproduced for asexual reproduction (Idestam-Almquist, 2000). Suchoverwintering strategy may explain why the share of charophytesin the following growth season was high under treatments wherebulbils were not removed by disturbance (i.e. cutting the tips off,mixing of the sediment surface layer). The influence of cutting ofmacrophytes and trampling on the vertical structure of sediment isweaker than removing of vegetation or sediment.

To conclude the results of our experiment indicated that thelargest impact on the shallow soft bottom charophyte communityis observed under the disturbances associated with mechanicalremoval of vegetation or sediment. Disturbances that only partlydamage the plants have minor effects and communities are

Fig. 3. Biomass share of charophytes, filamentous algae and higher plants for thestudied disturbance treatments in 2008.

K. Torn et al. / Estuarine, Coastal and Shelf Science 87 (2010) 27–3232

characterized by fast recovery. The timing of disturbance hadsignificant effects on the charophyte community with strongereffects when disturbed at mid-season compared to early season.The observed recovery patterns are likely explained by thedisturbance of the prevailing hibernacles of charophytes i.e.vegetative bulbils.

Acknowledgements

The work was supported by target financed projectSF0180013s08 of the Estonian Ministry of Education and Researchand the Estonian Science Foundation grants 6015 and 7813.

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