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Estuarine, Coastal and Shelf Science 91 (2011) 511e518

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Estuarine, Coastal and Shelf Science

journal homepage: www.elsevier .com/locate/ecss

Differences in top-down and bottom-up regulation of macroalgal communitiesbetween a reef crest and back reef habitat in Zanzibar

Gustaf Lilliesköld Sjöö*, Erik Mörk, Simon Andersson, Inger MelanderDepartment of Systems Ecology, Stockholm University, S-106 91 Stockholm, Sweden

a r t i c l e i n f o

Article history:Received 10 March 2010Accepted 2 December 2010Available online 13 December 2010

Keywords:macroalgaegrazingnutrientscoral reefswater motionEast Africa

* Corresponding author.E-mail address: gustafls@ecology.su.se (G. Lillieskö

0272-7714/$ e see front matter � 2010 Elsevier Ltd.doi:10.1016/j.ecss.2010.12.003

a b s t r a c t

Coral reef ecosystems are subjected to intense pressure from growing coastal populations and subse-quently increased nutrient loading and extraction of marine organisms. This development has alteredtop-down and bottom-up regulation of macroalgae in the reef system. The relative importance of theseregulating forces is also influenced by environmental prerequisites, such as exposure to wave action andwater motion. Thus, the present study tested the importance of top-down and bottom-up regulation, bymanipulation of nutrient availability and grazer abundance, at one reef crest- and one back reef-site inChwaka bay (Zanzibar, Tanzania). Wave action and water motion may regulate macroalgal communitiesby affecting the mobility of herbivores and availability of nutrients. The present study was conducted atthe onset of the monsoon period, with a general decline of macroalgal cover and biomass in the region;positive effects on biomass development were therefore manifested in reduced decline and not in anactual increase. The experimental study showed that both caging and fertilization had significant impactson macroalgal community composition but only caging showed any significant effects on biomassdevelopment. However, the influences of both these structuring forces were lower at the more exposedcrest-site. This period was chosen as most similar studies have been conducted during growth season,often overlooking the studied period. Such previous studies have shown that herbivore exclusionincreases macroalgal biomass, while the present study shows that it can also reduce biomass declineduring the seasonal die-off by approx 50%. Together, these results suggest an overall larger macroalgalpresence on the reef when herbivory is reduced. In general, our results propose that exposure to waveaction and water motion functions as an important regulating factor, affecting macroalgal communitiesby influencing both top-down and bottom-up regulation. In turn, these results suggest that anthropo-genic disturbances may have a greater impact on more sheltered coral reef habitats.

� 2010 Elsevier Ltd. All rights reserved.

1. Introduction

Tropical coastal ecosystems are subjected to increasing pressuresfrom anthropogenic activities, altering environmental prerequisiteswithin the seascape (Bellwood et al., 2004;Wilkinson, 2004; Downset al., 2005; Nyström et al., 2008). Growing coastal populationsincrease demands on resources within these systems (Weinsteinet al., 2007), as well as exposure to pollutants (Shahidul Islam andTanaka, 2004) and land derived nutrients (Smith et al., 2003).High dependency on coral reef resources has often resulted in over-harvesting of marine organisms and depletion of commerciallyimportant species (Sandin et al., 2008; Cinner et al., 2009). As thespecies composition and nutrient availability on the reef is changed,top-down and bottom-up forces regulating ecosystem componentsare modified, often resulting in altered benthic dominance regimes

ld Sjöö).

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and degradation of the system (Done,1992; Hughes,1994; Nyströmet al., 2000; McClanahan et al., 2002). Overexploitation of herbi-vores increases propagation of macroalgae through reduced top-down regulation (Lewis, 1986; McClanahan et al., 2003; Hugheset al., 2007; Burkepile and Hay, 2009). Furthermore, the potentialfor macroalgal development is also enhanced by increases ofbottom-up regulating resources, i.e. nutrient availability (Delgadoand Lapointe, 1994; Nielsen, 2003).

Top-down and bottom-up regulation has varying impacts ondifferent aspects of macroalgal ecology. Herbivory seems to be ofgreater importance in regulatingmacroalgal biomass, while nutrientavailability may have a stronger influence on species composition(Burkepile and Hay, 2006, 2009; Mörk et al., 2009; Sotka and Hay,2009). However, the importance of these regulating forces mayalso be affected by differences in prevailing environmental condi-tions between reef habitats. Hydrodynamic forces are influentialenvironmental factors, affectingmany aspects ofmacroalgal ecology,such as availability of dissolved inorganic carbon (Axelsson and

Crest-site

Back reef-site

i w

m

a h

c i M

s

a R

Chwaka Village

Reef crest

Unguja (Zanzibar)

1

4 3 2

0

5 km

o 39 26' E

S ' 0 1 6 o

Fig. 1. Map of field sites in the study area.

G. Lilliesköld Sjöö et al. / Estuarine, Coastal and Shelf Science 91 (2011) 511e518512

Uusitalo, 1988) and reproduction (Santelices, 1990; Norton, 1992).Examples of such forces are tidal currents and wave action whichinfluence both top-down regulation through herbivory as well asbottom-up regulation through nutrient availability. It can thereby bea key determinant of macroalgal production and community struc-ture (Hurd, 2000). Tidal currents andwave action can also shape theassemblages of mobile organisms (Fulton and Bellwood, 2005) andrestrict the movements of herbivores on the reef (especially on thereef crest) (Ogden, 1976; van den Hoek et al., 1978; Morrison, 1988;Vanderklift et al., 2009) as well as inhibiting their feeding ability(Morrison,1988; Vanderklift et al., 2009), thus creating a macroalgalrefuge from grazers. Sufficient flow rate is crucial for macroalgalgrowth, as their thalli are surrounded by boundary layers thatbecome nutrient depleted, and they are therefore dependant onrenewal of resources throughwatermixing (Williams andCarpenter,1998). High flow rates result in a trade-off between maximization ofnutrient uptake through increased surface-area to volume ratio, andsusceptibility to mechanical damage from hydrodynamic forces(Stewart and Carpenter, 2003).

Biomass and community dynamics of macroalgae are seasondependent (McClanahan et al., 1996; Lirman and Biber, 2000), andinvolve both growth periods and seasonal die off (McClanahan et al.,1996; Lapointe,1997; Larned,1998), resulting in changedmacroalgalbiomass and species composition over the year (Stimson et al., 1996;Ateweberhan et al., 2006). This seasonality can be attributed tochanges in several environmental factors, such as temperature,nutrient availability, water motion and irradiance (Carpenter, 1985;Stimson et al., 1996; Ateweberhan et al., 2006) as well as herbivoreabundance and feeding intensity (Carpenter,1986; Smith, 2008). Thepresent study was conducted just prior to the monsoon period andthus covers an often overlooked part of the season, characterized byincreasing wind speeds, rainfall and wave heights along the coast ofeastern Africa (McClanahan, 1988).

The studyaimed to compare the initial response to changes in top-downandbottom-up regulationofmacroalgal communitiesbetweena crest- and a back reef-site during a period of general macroalgalbiomass decline. Althoughmany studies have investigated the effectsof top-down and bottom-up regulation, this study has a novelapproach as it includes the influence of hydrodynamic forces as wellas analyzing the effects ofmacroalgal development during a periodofgeneral decline.Wehypothesize that: (1) bothnutrient enhancementand grazer exclusion will be less effective at the site with high watermotion compared to themore sheltered site; (2) Herbivore exclusionwill positively affect macroalgal biomass, while nutrient additionmainly will influence species composition; (3) Positive effects onmacroalgal biomass will not manifest as an increase, but rather asa slower decline during the seasonal die-off.

2. Materials and methods

2.1. Study region and sites

The study was conducted in Chwaka bay (6�13e250S and39�37e58’E) on the east coast of Unguja island (Zanzibar), Tanzania(Fig. 1), which is characterized by a semi diurnal and asymmetricaltide, with strong currents. The inner bay is dominated by seagrassmeadows and, along the inner coast to the south, lays a mangroveforest. The outer rim of the bay is fringed by a coral reef consisting oflive coral patches and old coral substratum (Cederlöf et al., 1995).Along the coast of the bay there are seven villages with a combinedpopulation of 9000 whose main economic activities are fisheriesfollowed by seaweed farming (de La Torre-Castro and Rönnbäck,2004). The climate is influenced by the monsoon cycles, dividingthe year into four relatively distinctive periods (Tobisson et al.,1998).The study was conducted during a 6 week period, from March 12

until April 22, 2008, which is a transition from the dry-towards themonsoonperiod,whenhighwinds and strong currents becomemorefrequent. Furthermore, increasing cloud cover results in decreasinglight towards the end of the study period (Tobisson et al., 1998).Resulting from this climatic transition, the macroalgal communityundergoes a “die-off” period, characterized by a general reduction ofcover and biomass, as algal growth is superseded by tissue loss.

The two study sites are situated on the reef crest and at the backreef, at the mouth of Chwaka bay (Fig. 1), separated by c.500 m. Thesites were chosen based on their similar macroalgal cover anddominant species. Both sites consist of coral substratum (with a livecoral cover of approx.10e15%) and had an averagemacroalgal coverof approx. 30%, with Padina and Dictyota as the dominant genera.Mean algal height was equally low at both sites, with an average of3.8 cm SE �0.2 at the crest-site and 3.4 cm SE �0.2 at the back reef-site. Although the area in general is more variable, relatively similarmacroalgal communities were chosen to minimize response vari-ability, in order to isolate influence from the studied factors. Chwakabay is considered a relatively rich fishing ground, and a study byDorenbosch et al. (2005) estimated the density of commerciallyimportant (larger) herbivorous fish on reefs in Chwaka bay as 55.9ind. 100 m�2, with Scaridae, Siganidae and Acanthuridae as thedominant families. However, as no previous sea urchin data wereavailable for this area, inventorieswere conducted at both sites priorto the present study. Average water depth at the sites was about30e50 cmat spring lowand about 4m at spring high tide. The crest-site experiences stronger wave action and water motion, while theback reef-site ismore sheltered, as it is protected by several hundredmetres of reef flat, resulting in smaller waves and relatively lowerwater motion. The difference in wave exposure was manifested ina thin layer (approx.1 cm) of fine grained sediment on the shelteredback reef-site while the more exposed crest-site almost completelylacked a sediment layer. We designed a manipulative experimentwhere treatments were replicated within the two sites, leading toa lack of replication at the site level. However, the similaritiesbetween our two sites (with exception for exposure) minimize theinfluence of other factors associated with geographic replication, ase.g. precipitation, surface irradiance and background nutrientconcentration seldom differ on this spatial scale.

G. Lilliesköld Sjöö et al. / Estuarine, Coastal and Shelf Science 91 (2011) 511e518 513

2.2. Experimental design and description of treatments

At each site, 4 different treatments were conducted: unalteredcontrol treatment, fertilized, unfertilized þ exclosure of herbivoresand fertilized þ exclosure, each with 10 replicates. In addition tothe study design, semi exclosures (cage control treatment; n ¼ 10at each site) were used to verify that there were no effects of thephysical cage structure (other than excluding herbivores). Eachsite covered an area of 40 m � 40 m. All replicate plots covereda circular area of approximately 0.2 m2 and were distributedrandomly within the study site, separated by approx. 5 m.

Nutrient enhancement was conducted by application of 4 meshbags containing 10 g slow-release NPK-fertilizer pellets (ScottsOsmocote), distributed around each specified nutrient plot.A previous study from the same region has shown that tissuesamples taken from macroalgae subjected to such enhancementshow increased levels of nitrogen and phosphorous (Mörk et al.,2009). This previous study was conducted for the same length oftime and with similar cages. Fertilizer was replaced after 3 weeks.To test the effects of herbivory, reduction of grazing pressure wasachieved by exclusion of large bodied herbivores by construction ofplastic mesh cages (0.2 m2 � 50 cm high, mesh size approx.2 � 2 cm), which are robust and do not significantly alter watermotion (e.g. Jompa and McCook, 2002; Mörk et al., 2009). Thismesh-size excludes larger herbivores (i.e. larger fish and seaurchins), but not small fish and mesograzers. The cages wereanchoredwith steel U-nails andwere scrubbed every 1e2weeks, toremove biofouling organisms and sediments which would other-wise affect light penetration and water exchange. The semi exclo-sures were constructed in the same fashion as the full cages, butwith the addition of five randomly distributed openings(15 � 15 cm). Open control plots without any additives, serving asgeneral controls, were marked by four nails marking the perimeter.

2.3. Measurements and calculations

At the beginning of the experiment an inventory was carried outof the existing macroalgal community within all replicate plots,measuring cover and height of each macroalgal species. Meanheight of all occurring individualswas used for larger (free standing)species while mean stand height was used for smaller, morenumerous (stand forming) species. Cover was visually estimatedusing a length reference, placed along the substratum. Algal speciesdiversity was calculated according to the Shannon-Weiner index(H’), and evenness was calculated using Pielou’s evenness index (J’).These indices were calculated using number of macroalgal speciesand their proportion of total cover (%) within each plot. Macroalgalbiomass (g wet weight (ww)) was calculated using species volume(height (cm) � cover (cm2)) multiplied by density (g ww cm�3).Macroalgal species density values were based on earlier densitymeasurements of the regions most commonly occurring species(unpublished data). Although a certain error is added by usingstandardized species densities (as densities of some species mayvary between sites), the values can be used for comparison of thegeneral biomass development within the sites. The investigatedparameters weremonitored at the start, at the mid-point (3 weeks)and at the termination of the experiment (after 6 weeks).

2.4. Environmental conditions

In order to control for unwanted caging artifacts, light pene-tration and water motion were monitored, within and outside thecages. Irradiance was measured during midday, using an Interna-tional Light Photometer model IL 1400 A. All irradiance measure-ments were conducted on the same day, at the initiation of the

study. Temperature was measured at midday during each samplingoccasion (at both sites). Water motion at both sites, as well ascomparisons between inside and outside the cages was estimatedby the submergence of 10 plaster clods for 24 h during spring tide,with a tidal amplitude of 3.7 m. After drying, the clods werereweighed and the amount of eroded weight (g) was calculated.Mean weight reduction of plaster clods was then used to comparewater motion between sites (McClanahan et al., 2005).

2.5. Tissue nutrient analysis

To test the availability of added nutrients, actively growing tipsof Eucheuma denticulatum (Burman) were collected from a seagrassarea within the bay, and attached to all caged treatments (bothfertilized and unfertilized) from which small fragments weresampled at the initiation, after 3 and 6 weeks, respectively. Thetissue nutrient content (% dw) was used as an indicator of relativeambient nutrient levels at the sites as well as measurements ofnutrient binding within the different treatments (Lilliesköld Sjööand Mörk, 2009).

To determine C, N and P content, air-dried algaewere ground intoa fine powder, and dried again to constant weight at 60 �C. Theanalyseswere performed using a Leco CHNS-932 elemental analyzer(combustion temperature 950 �C), which gives the percentage massof N and C in the tissues. The phosphorus analyses were conductedby combustion of samples for 2 h at 500 �C before digestion in per-sulfate solution (50 g þ 30 ml H2SO4 l-1) for 1 h at 120 �C. Theresultant orthophosphate was then analyzed colorimetrically usinga segmented flow system (ALPKEM O I Analytical).

2.6. Data analyses

Differences between sites, treatments and environmentalparameters were tested using one- and two-way ANOVA, depend-ing on the number of tested factors. ANOVA assumptions weretested using: Cochran’s C-test for homogeneity of variances, plot ofresiduals were used to test if data were normally distributed anda regression between variances and means to test for correlations.When all ANOVA assumptions were fulfilled, Tukey’s HSD-test(HSD) was used to detect differences between treatments. ANOVAand post-hoc analyses were conducted using the software STATIS-TICA 9. Multivariate analyses of macroalgal community composi-tion, based on species coverwithin each replicate plot and samplingoccasion, were conducted using “partial Canonical CorrespondenceAnalysis” (pCCA). The constraint involved removing (“partiallingout”) the variance contributed by differences in time. This analysistested the effects of herbivore exclusion and fertilization on thecommunity composition at the two sites. Prior to pCCA the datawere examined for gradient length, arch- and edge-effects, as wellas the variance inflation factors. These pCCA data were furthertested using multivariate ANOVA and goodness-of-fit. Thesemultivariate analyses were conducted in the software R. ANOSIM-analysis were used to analyse differences in macroalgal communitycomposition between sites, using all treatments at the initiation ofthe study. Finally, the individual species contribution to the differ-ences in species compositionwas calculated with SIMPER-analyses.Both ANOSIM and SIMPER-analyses were conducted using thesoftware PAST 1.83.

3. Results

3.1. Environmental conditions at the two sites

The temperature was the same at both sites at each occasion,decreasing from 31 �C at the start to 26 �C at the end of the study.

Start Week 3 Week 60

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±SE Mean Cover

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±SE Mean P content Mean N content

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%(tn

etno

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Start Week 3 Week 60.9

1.0

1.1

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)´H(

ytisrevidseicepS

Mean diversity

±SE Mean species no.

.on

seic

epS

3.0

3.5

4.0

4.5

5.0

5.5

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6.5

7.0c

ns ns

ns

***

Fig. 2. Mean macroalgal biomass (g ww m�2) and cover (%). (a) Eucheuma tissue N andP content (% dw). (b) and algal species diversity (H0) and species no. (c) in the studyarea during the study period. Data represents pooled control plots from both sites (asthe sites did not differ regarding any of these traits). All values denote means � SE.Stars denote level of significance compared to initial values (* ¼ <0.05; ** ¼ <0.01;*** ¼ <0.001) (n ¼ 20).

G. Lilliesköld Sjöö et al. / Estuarine, Coastal and Shelf Science 91 (2011) 511e518514

Watermotion differed (ANOVA F1¼7.00, p< 0.05) between the twosites, with 88% (SE �0.03) plaster clod erosion at the crest-site,compared to 76% (SE �0.04) at the more sheltered back-reef site.Sea urchin biomass was similar at the two sites, 502 g SE�55 at theback reef-site and 376 g SE �77 at the crest-site (ANOVA F2 ¼ 1.93,p ¼ 0.18) as was the species composition (ANOSIM p ¼ 0.9,R ¼ �0.07). Both sites were dominated by Echinometra sp. andEchinotrix sp.

3.2. General development at the two sites

Macroalgal community composition differed between the twosites (ANOSIM R ¼ 0.16, p < 0.001), comparing all plots prior to theinitiation of the study (n ¼ 50). However, there were no differencesbetween sites regarding the development of macroalgal biomass,cover, species diversity or tissue nutrient content, within controlplots (Appendix 1). Hence, controls from both sites were pooled todescribe the general development in the studied area. Both algalbiomass (ANOVA F2 ¼ 25.64, p < 0.001) and cover (ANOVAF2 ¼ 24.25, p < 0.001) decreased over time (Fig. 2a). Eucheumatissue nutrient content, on the other hand increased during thestudy period (Nitrogen ANOVA F2 ¼ 29.02, p < 0.001; PhosphorusANOVA F2 ¼ 30.00, p < 0.001) (Fig. 2b). Algal tissue N contentincreased from w0.7% dw to w1.1% dw, and P content increasedfrom w0.06% dw to w0.08% dw. Algal species diversity increased(ANOVA F2 ¼ 13.09, p < 0.001) by w28% over the study period,while species number did not show any change (Fig. 2c). Evennessshowed a similar development as diversity, increasing by w25%(ANOVA F2 ¼ 61.66, p < 0.001) during the study.

3.3. Differences between treatments

Therewere no differences between treatments at the start of thestudy, concerning macroalgal cover, biomass, species number anddiversity (see Appendix 1 for two-way ANOVA values; HSDp ¼ 0.23e0.99).

Water motion was not different inside herbivore exclosurescompared to outside (Appendix 1), where clods inside herbivoreexclosures experienced a 75 and 81% weight reduction (SE �0.02and 0.03) and clods in open plots were reduced by 76 and 88% (SE�0.3 and 0.4) at the back reef and crest-site respectively. Thedifference in light intensity inside and outside the cages was smallwith a 5.4% light reduction inside cages which may be negligible ina shallow tropical environment where algae often are light satu-rated at irradiances well below natural daylight (e.g. Arnold andMurray, 1980; Littler et al., 1988). Neither were there any effectsof cage controls compared to controls (Appendix 1), suggesting thatthe physical structure of cages did not affect algal cover, biomass,species number or diversity.

At the crest site, increase of tissue nutrient content in Eucheumadid not differ between cages (N ¼ 42% SE �6; P ¼ 44% SE �6) andfertilized cages (N¼ 43% SE�5; P¼ 48% SE�4) (Appendix 1). At theback reef-site however, increase of tissue nutrient content washigher, regarding both N (ANOVA F1 ¼ 12.03, p < 0.01) and P(ANOVA F1¼9.09, p< 0.05), in fertilized (N¼ 36% SE�5; P¼ 33% SE�5) compared to unfertilized cages (N ¼ 9% SE �6; P ¼ 9% SE �5).

There were no effects of treatments on algal biomass change atthe crest-site (Appendix 1), whereas the back reef-site showeda 50% smaller biomass decrease (two-way ANOVA TreatmentF3 ¼ 7.5, p < 0.001) in grazing exclosures than in controls (bothfertilized HSD p < 0.01, and unfertilized HSD p < 0.001) during thestudy period (Fig. 3). The same pattern was found for algal cover,which was not affected by treatments at the crest site (Appendix 1),but at the back reef site (two-way ANOVA Treatment F3 ¼ 12.7,p < 0.001). The decrease in algal cover was 70% lower in the caged

treatments (HSD p< 0.05) at this site. Fertilization did not influencealgal cover, biomass, species number or diversity in neither openplots or with herbivores excluded, at either of the two sites(Appendix 1).

Algal diversity (H’ ¼ 1.6 SE �0.02) and species richness (6.0 SE�0.15) were similar at the two sites and there were no effectsof treatments in either the crest-site or the back reef-site(Appendix 1).

As mentioned above, the sites had similar macroalgal cover andwere dominated by the same species at the start of the study, butdiffered regarding community composition so the latter at each site

Start Week 3 Week 6-100

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Fertilized cages

a

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Mean ±SE

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Controls

Fertilized cages

***

**

b

Fig. 3. Mean algal biomass change (% �SE) in the different treatments at the crest-site.(a) and the back reef-site. (b) after 3 and 6 weeks (n ¼ 10). Stars indicate the level ofsignificance compared to controls (* ¼ <0.05; ** ¼ <0.01; *** ¼ <0.001). The lines inthe figure have been adjusted horizontally to better display the variation.

Table 1Inertia in the two pCCA, as well as eigenvalues for the two constrained main axes.The table also shows the contribution of the two factors (fertilization and caging) toeach axis, tested using goodness of fit.

Inertia Rank

Crest-SiteTotal 3.3519Conditional 0.3063 1Constrained 0.0564 2Unconstrained 2.9892 25

Back reef-SiteTotal 2.9417Conditional 0.2894 1Constrained 0.0949 2Unconstrained 2.5575 27

Factor Axis 1 Axis 2 r2 p

Crest-SiteEigenvalues forconstrained axes

0.0337 0.0227

Fertilization �0.3030 �0.9530 0.1533 <0.001Caging 0.9469 �0.3216 0.1895 <0.001

Back reef-SiteEigenvalues forconstrained axes

0.0595 0.0355

Fertilization �0.6743 0.7384 0.2040 <0.001Caging 0.6664 0.7456 0.2633 <0.001

Table 2SIMPER-analysis showing mean abundance (% cover) and % contribution to theobserved difference between sites, for the 10 most influential species at week 1and 6.

Week 1 Contribution(%)

Cumulative(%)

Crest-site Back reef-site

Mean abund.

TaxonPadina boergesenii 36.9 36.9 6.6 14.5Dictyota sp. 23.23 60.13 10.8 9.8Caulerpa elongata 8.07 68.2 2.24 1.06Laurencia sp. 7.64 75.84 1.9 0.48Caulerpa mexicana 3.66 79.5 0.8 0.8Stoechospermumpolypodioides

3.03 82.53 0.56 0.34

Filamentous green 2.42 84.95 0.24 0.62Halimeda discoidea 1.93 86.88 0.18 0.44Halimeda renschii 1.79 88.67 0.38 0.16Sargassum aquifolium 1.53 90.2 0.46 0

Week 6Laurencia sp. 11.19 11.19 1.9 2.02Caulerpa elongata 10.98 22.17 2.74 0.7Avrainvillea sp. 9.08 31.25 2.1 0.24Dictyota sp. 7.75 39 1.74 0.76Lyngbya sp. 7.47 46.47 1.68 0.18Galaxura sp. 5.99 52.46 0.12 1.42Gracilaria sp. 5.55 58.01 0.52 1.08Padina boergesenii 5.18 63.19 0 1.28Halimeda discoidea 5.18 68.37 0.34 1.06Filamentous green 4.73 73.1 0.32 1.02

G. Lilliesköld Sjöö et al. / Estuarine, Coastal and Shelf Science 91 (2011) 511e518 515

was analyzed separately with respect to impacts of herbivoreexclusion and fertilization. Eigenvalues for constrained axes in thepCCA-analysis showed that a larger part of the total inertia wasrelated to herbivore and nutrient manipulations in the back reef-site than in the crest-site (Table 1). Multivariate ANOVA analysisshowed that the pCCA distribution was statistically significant forboth sites (p < 0.05). Goodness-of-fit analysis showed that bothcaging and fertilization influenced the observed distribution(p < 0.001 for both factors and sites). At the crest-site, the eigen-values show that caging had the strongest contribution to the mainaxis, while in the back reef-site both factors were of similarimportance (Table 1).

SIMPER-analyses revealed that both sites were initially domi-nated by the genera Padina and Dictyota. During the study period,cover of both these dominant genera declined substantially andthey has almost disappeared towards the end of the study, in alltreatments and at both sites. While these two genera declined, thereduced algal cover was partially replaced by other, previously

more inconspicuous genera, such as Caulerpa, Laurencia andGracilaria (Table 2).

4. Discussion

Environmental factors such as wind, temperature and precipi-tation, that regulate macroalgal community dynamics, are seasonalin Chwaka bay (Tobisson et al., 1998) and may explain most of theobserved decline of macroalgal biomass and cover in the presentstudy, as it was conducted during the die-off period just prior to the

Start Week 3 Week 6-100

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Control Mean ±SE

Exclosure

Large- bodiedHerbivores

OtherFactors

Fig. 4. Mean algal biomass change (% �SE) in caged (both fertilized and unfertilized)and control treatments at the back reef-site after 3 and 6 weeks.

G. Lilliesköld Sjöö et al. / Estuarine, Coastal and Shelf Science 91 (2011) 511e518516

monsoon. The two study sites were chosen as they represent twotypes of reef habitats with different exposure to wave action andwater motion, while having relatively similar macroalgal cover atthe start of the study. Nevertheless, an ANOSIM-analysis revealedthat community composition differed between sites when testedmultivariately. The sites clearly differed in exposure to hydrody-namic forces, even though the plaster clod test only showed a 10%higher dissolution at the crest-site. We believe that this is anunderestimation of the actual difference inwater motion as the testonly spans over 24 h and dissolution is not linearly related to watermotion when comparing different flow regimes (Porter et al.,2000). The more sheltered position of the back reef-site, pro-tected by an extensive reef flat, is shown by a sediment layer, whichis lacking at the crest-site. Furthermore, the hydrodynamic forces atthe crest-site were evident when working there, as they made itmore strenuous to put out and maintain the cages. Macroalgalcover and biomass were similarly developed on both sitesthroughout the study, whereas the response to exclusion ofherbivores and nutrient loading differed between the sites. Herbi-vore exclusion resulted in a slower decrease of macroalgal biomassat the back reef-site, whereas there were no such effects at thecrest-site although this is unlikely to be related to herbivoreabundance as sea urchin biomass and composition were similar atboth sites. Larger herbivorous fish should be able to move freelybetween the two sites as they only are separated by 500 m ofcoherent reef, thus resulting in similar fish communities. However,previous studies (e.g. Ogden, 1976; van den Hoek et al., 1978;Morrison, 1988; Clemente and Hernández, 2008) have shown thatgrazing pressure may be generally lower at a site with relativelyhigher hydrodynamic forces, presumably resulting from restrictedherbivore mobility and inhibited feeding. Thus further reductionsof grazing pressures may have a relatively smaller effect in suchareas.

It has frequently been shown that herbivore exclusion mayincrease macroalgal biomass (e.g. McClanahan et al., 2003;Burkepile and Hay, 2006, 2009; Sotka and Hay, 2009) but suchstudies are often conducted during periods of general macroalgalgrowth. A related study from the same region, using the sameherbivore exclusion method, showed a 77% increase in macroalgalbiomass within cages during the growth season (Mörk et al., 2009).However, as the present study was conducted at the onset of themonsoon, herbivore exclusion reduced the rate of macroalgalbiomass decline. An enhanced macroalgal biomass accumulationduring the growth season in combination with a slower declineduring the seasonal die off period would result in an overall largerbiomass of macroalgal standing stock throughout the whole season.In turn, more macroalgae on the coral reef will influence thecompetition for benthic cover, and may affect the starting point forthe coming macroalgal growth season. According to the differencein biomass decline in the back reef-site, between the caged (bothfertilized and unfertilized) and control treatments, large bodiedherbivores (which were excluded through caging) seem tocontribute substantially to removal of macroalgal biomass. Based onthis difference, large bodied herbivores seem to account for c.50% ofthe observed decline while the remaining biomass loss may beascribed to other factors (e.g. consumption by smaller herbivores ormechanical removal through waves or water motion) (Fig. 4).Hatcher and Larkum (1983) proposed that although grazing by largebodied herbivores has a clear influence on macroalgal biomassaccumulation, it is only a good predictor of macroalgal standingstock within limited temporal and spatial scales. They also suggestthat whenever macroalgal growth exceeds grazing losses, the algalstanding stock is no longer primarily controlled by grazing. Instead,growth characteristics of the dominant algal species and otherexternal factors, such as light, temperature or nutrient availability,

may regulate macroalgae during periods of biomass increase(Hatcher and Larkum, 1983). This agrees with the results from thepresent study as herbivory by large bodied herbivores only accountsfor c.50% of the algal biomass reduction, at the back reef-site (Fig. 4).During the present study period, light and temperature decreasedwhile nutrient availability increased so the remaining biomass lossmay at least partly be attributed to these reductions in light andtemperature, which affects the macroalgal growth negatively.

General macroalgal species diversity in the study area increasedduring the study period, even though species number remainedstable. The observed diversity development is instead explained bya cover reduction of the two dominant genera (Padina and Dic-tyota), and a partial cover replacement by less dominant genera(Table 2), as is also shown by the observed increase in evenness.This suggests that the use of a diversity index may be inadequatefor understanding the development of the algal community if theunderlying cause of diversity development is not properly scruti-nized (for further discussion on the use of diversity indices seereview by Jost (2006)).

Fertilization increased the tissue nutrient content at the backreef-site, but not at the crest-site, a feature possibly due to rapiddilution of added nutrients, resulting from the higher flow. Suchdilution may be an artefact of our small-scale experimental nutrientaddition, whereas large-scale eutrophication would result inenhanced nutrient delivery at the crest site as a result of increasedmass transfer (Sanford and Crawford, 2000) and disruption ofboundary layers (Wheeler, 1980; Hurd, 2000). Regardless of theincreased tissue nutrient levels at the back reef-site, fertilization didnot influence the development ofmacroalgal cover, biomass, speciesnumber or diversity, at either of the sites. These results suggest thatnutrients are a relatively weaker regulating factor of these param-eters. Growth dilution is not likely to explain the observed lack ofresponses in tissue nutrient content as growth did not increase infertilized treatments. The pCCA-analysis showed that both herbi-vore exclusion and fertilization affected the macroalgal communitycomposition at both sites but also that the effect of treatment wasstronger at the back reef-site. This shows that although none of themeasured parameters responded to treatment at the crest-site,treatments still affected the species-specific responses within thecommunity. Many species were affected by these factors, but thegenus Laurencia showed the strongest response to herbivoreexclusion, whereas the genus Caulerpa responded strongest tofertilization. In both cases the response manifested in an increase of

Macroalgae

Nutrient availability

Herbivory s e c r o f

c i m

a n y d o r d y

H

Top-down regulation

Bottom-up regulation

Physical regulation

Fig. 5. Conceptual model showing interactions between the studied regulating factors.Black arrows indicate direct effects while gray arrows indicate indirect influence on themacroalgal community.

G. Lilliesköld Sjöö et al. / Estuarine, Coastal and Shelf Science 91 (2011) 511e518 517

cover, where cover of Laurenciawas three times higher inside cagesand Caulerpa had twice as high cover in fertilized treatments.Despite the general decrease inmacroalgal cover and biomass, somespecies (such as the genera above) may increase their cover asa response to alterations of top-down and bottom-up regulation iftheir biomass budget becomes positive. Such increases of previouslyinconspicuous species may be a result of reduced competition fromthe dominant species. However, manipulations of herbivory andnutrient loading explained more variation at the back reef-site thanat the crest-site. These observed differences in response to alter-ations of top-down and bottom-up regulation could be attributed tothe differences in exposure between the two sites. The lack ofresponse to herbivore exclusion and fertilization at the crest-sitemay be a result of a larger influence of wave action and watermotion at this site. Exposure to hydrodynamic forces can thus beconsidered as a third regulating factor of macroalgal communitydynamics (in addition to top-down and bottom-up regulation),which may directly affect algal morphology and growth throughphysical regulation (stimulation/disturbance). It could also affectmacroalgal communities indirectly, as it may have a direct influenceon the other two regulating factors, either by hampering herbivoremovement or affecting nutrient availability. Hydrodynamic forcescan therefore be considered to exert an overarching influence onmacroalgal communities, without itself being affected by the otherstudied regulatory factors (Fig. 5).

5. Conclusions

The present study suggests that exposure to hydrodynamicforces influences the effects of top-down and bottom-up regula-tion. A reduction of large herbivores reduced the rate of macroalgaldecline during the die-off period with c.50%, at the more protectedback reef-site, but not at the exposed crest-site. Together withprevious studies showing increases of algal biomass during growthperiods, our results suggest that algal presence on the reef isenhanced throughout both growth and die-off seasons when thereare fewer larger herbivores. Nutrients did not influence cover,biomass, species number or diversity, but affected species compo-sition, with the strongest influence at the more sheltered back reef-site. As the effects of herbivore exclusion and fertilization werereduced in the more exposed site, it can be concluded that hydro-dynamic forces may be an important regulating factor, possiblyinfluencing the consequences of overfishing and eutrophication.

Acknowledgements

We thank SIDA/SAREC (Swedish Agency for Research Coopera-tion with Developing Countries) for funding of the project. We

would also like to thank N. Jiddawi (Institute of Marina Science,University of Dar es Salaam) for valuable help with facilitation ofthe project. Furthermore, we would like to thank. L. Kautsky,M. Troell and N. Kautsky for valuable input and advice on themanuscript.

Appendix. Supplementary data

Supplementary data associated with this article can be found inthe online version, at doi:10.1016/j.ecss.2010.12.003

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