Sunlight and sediment improve the environment of a litter ...

AQUACULTURE ENVIRONMENT INTERACTIONSAquacult Environ Interact

Vol 9 73ndash85 2017doi 103354aei00209

Published February 8

INTRODUCTION

The importance of decomposing mangrove leaf litter in providing natural food to post-larvae ofpenaeid shrimps lies mainly in the associated peri-phytic biofilm (Gatune et al 2012) The biofilm con-sists of phyto- and zoobiota which is mediated by amicrobial loop (Burford et al 2003 Azim amp Wahab2005 Pascal et al 2008) Our previous studies re -vealed that the biofilm developing on decomposinglitter possesses potential and direct nutritive value topost-larval shrimp (Gatune et al 2012 2014a 2014b)These studies also identified strategic interventiontimelines in managing mangrove litter falling intosilvominusshrimp aquaculture systems Silvo-aquacultureis an ecological shrimp culture system where theshrimp diet is naturally derived from a mangrove

copy The authors 2017 Open Access under Creative Commons byAttribution Licence Use distribution and reproduction areunrestricted Authors and original publication must be credited

Publisher Inter-Research middot wwwint-rescom

Corresponding author kgatuneyahoocom

FEATURE ARTICLE

Sunlight and sediment improve the environment ofa litter biofilm-based shrimp culture system

Charles Gatune1 Ann Vanreusel2 Marleen De Troch2

1School of Natural Resources and Environmental Studies Karatina University PO Box 1957 10101 Karatina Kenya2Biology Department Marine Biology Ghent University Campus Sterre Krijgslaan 281-S8 9000 Ghent Belgium

ABSTRACT In silvofishery where shrimp culture isintegrated with mangrove trees the mangrove leaflitter may modify the environment in these culturesystems This study tested the potential of submergedleaf litter of Rhizophora mucronata and associatedbiofilm in providing a favorable environment for post-larval shrimp Penaeus monodon Litter decompositionand assembly of microalgae and epifauna were as-sessed under exposure to sunlight or shade and pres-ence or absence of sediment Litter incubated withsediment and exposed to sunlight was rapidly decom-posed and supported the highest biomass and diver-sity of microalgae and epifauna The litter also sup-ported the highest abundance of diatoms polychaetesand nematodes during the 4th week of decompositionCyanobacteria of the genus Microcystis dominatedlitter incubated without sediment in sunlight afterdecom position for 5 wk Under shaded conditions di-atoms of the genus Navicula and the CyanobacteriaAnabaena spp and Oscillatoria spp continued togrow at high total ammonium nitrogen low dissolvedoxygen low tem perature and low pH Our study illus-trates synergy between sediment and direct sunlightin promoting diversity of microalgae and polychaetes(of dietary benefit to shrimps) inhibiting growth ofCyanobacteria and maintaining water quality atlevels favorable to culture of post-larval shrimp Ourfindings support 4 practices for a healthy environmentin fish ponds (1) locating ecological shrimp culture inless forested areas (2) promoting sediment conditionsin artificial shrimp culture systems (3) exposing litter-derived bio film within ponds to sunlight and incubat-ing with sediment to maintain favorable water qualityand control Cyanobacteria blooms and (4) minimizingthe use of pond liners and related sludge removal

KEY WORDS Shrimp culture middot Sunlight middot Sediment middotMangrove litter middot Microalgae middot Epifauna middot Biofilm

Modified shrimp pond in a mangrove mudflat at Mtwapacreek Kenya coast equipped with natural sediment andexposed to sunlight

Photo credit C Gatune Karatina University Kenya

OPENPEN ACCESSCCESS

Aquacult Environ Interact 9 73ndash85 2017

ecosystem (Primavera 1998) Ecological shrimp aqua-culture in mangrove systems has gained environ-mental support because of its tendency to conservethe mangrove forest (Primavera 1998 Fitzgerald2000) by rearing fish without clearing mangrovetrees (Primavera 1998) This integrated approachimplies that the shrimp culture system constantlyintercepts mangrove litter fall which proceeds todecompose under the influence of the microbiotapresent in the biofilm (Benner amp Hodson 1985 Rajen-dran amp Kathiresan 2007) The mangrove trees alsoshade the shrimp culture system from direct sunlighteither partially or completely Since mangrove leaflitter falling into the water eventually sinks to thebottom layers the microalgae accumulating at thewater surface or other suspended particles in thewater column further shield the litter from direct sun-light Sunlight has been demonstrated to acceleratethe rate of decomposition of leaf litter either solely byphotochemical oxidation action (Gallo et al 2009) orin combination with the accelerated extracellularenzymatic action of the associated microbial com -munities (Francoeur et al 2006) Light intensity alsoincreases algae biomass density and compositioncreating a rich energy source for shredders whichenhances the rate of plant litter decomposition bytheir grazing activity (Franken et al 2005)

In an attempt to comply with the ecological needsto reduce aquaculture activities in mangrove sys-tems shrimp culture practices are being pushed further inland However shrimp aquaculture furtherinland lacks the natural services from mangrove-based estuarine ecosystems (Kautsky et al 2001)This has caused an increase in shrimp culture sys-tems that have adopted artificial substrates to mimicnature in promoting proliferation of natural foodsources One example is the use of leaf litter to pro-mote proliferation of natural biota for maintainingwater quality (Bratvold amp Browdy 2001 Otoshi et al2006 Asaduzzaman et al 2008) Hypothetically ifthe artificial substrate used is decomposing man-grove leaf litter the growth and composition of bio-film on the decomposing leaf litter substrate maydepend on the extent of exposure to sunlight andsediment

It is essential that ecological shrimp culture sys-tems whether in mangroves or further inland support phyto- and zoobiota for maintaining waterquality and providing a quality food source for post-larval shrimp (Burford 1997 Bratvold amp Browdy2001 Thompson et al 2002) Thus it is important toassess the potential of decomposing mangrove leaflitter to support biofilm contributing to the natural

diet of post-larval shrimp when the environmentalconditions are modified In this study we hypothe-sized that water quality and the value of the naturalfood provided by the biofilm associated with decom-posing mangrove leaf litter depends on exposure todirect sunlight and sediment Environmental factorsinvestigated included light intensity water trans-parency temperature dissolved oxygen pH salinityand total ammonium nitrogen (TAN) The assemblyof the major taxa of microalgae and invertebratefauna colonizing the decomposing mangrove leaf litter of Rhizophora mucronata was also investigatedOnce isolated and identified the potential applica-tion of the various microalgae and fauna in providinga natural diet to post-larval shrimp Penaeus mon-odon was assessed by comparing with the naturalfood types commonly used in shrimp aquaculture

MATERIALS AND METHODS

Study site

The study was carried out in an integrated man-grove and shrimp culture farm at Mtwapa Creeknorthern coastal region of Kenya (3deg 57rsquo S 39deg 42rsquo E)The project area is characterized by a reforested man -grove forest dominated by Rhizophora mucronata

Experimental set-up

Senescent mangrove leaf litter (hereinafter man-grove leaf litter) which had just turned yellow-brownand dropped from the trees were carefully selectedto include leaf litter of similar surface area The leaflitter was then incubated (see lsquoLitter decompositionrsquofor details) in pond water inoculated into circularmesocosms ie open-top 200 l tanks of 075 m waterdepth at a litter loading density not exceeding 1 glminus1(Hai amp Yakupitiyage 2005) Tank water was slowlyreplenished (to avoid dislodging the biofilm) daily ata rate of 25 The tanks were not stocked withshrimps to prevent grazing on biofilm and were setto provide 4 treatments with each treatment consist-ing of 3 replicates as follows direct sunlight with sed-iment (LS) direct sunlight without sediment (LX)shaded with sediment (DS) and shaded without sedi-ment (DX) The shaded tanks were placed under thecanopy of a thick mangrove forest to prevent expo-sure to direct sunlight The sunlit tanks were placedin an area without mangrove trees with direct expo-sure to sunlight but in close proximity to the shaded

74

Gatune et al Effect of sunlight and sediment on shrimp culture

tanks The sediment treatments consisted of a 5 cmlayer of sediment obtained from the bottom of a pondwhich had previously been used to culture shrimpsThe sediment was not given any special treatment toexclude natural microbiota

Litter decomposition

Senescent mangrove leaf litter was dried in theshade to a constant weight and incubated by sus-pending it 3 cm above the bottom of the tank for a pe-riod of 7 wk Leaves were suspended vertically andabove the sediment or bottom to allow an all-rounduniform development of biofilm as the leaf litter decomposed Three decomposing leaves which hadpreviously been marked and initial weight takenwere sampled weekly and pooled from each replicatetank Biofilm on the sampled leaf litter was gentlywashed off with distilled water and pooled The bio-film and the decomposing leaves were oven-dried at70degC to a constant weight and weighed Litter decom-position was recorded as percentage weight loss of thepooled leaves after removal of the biofilm as follows

(1)

Microalgae abundance and taxa composition

Mangrove leaf litter was sampled from each tankweekly in triplicates by pooling 3 decomposing leavesper replicate Biofilm was gently washed from thesurface of the mangrove leaves with a known volumeof filtered seawater and preserved in 2 Lugolrsquosiodine solution (12 iodineiodideglacial acetic acidsolution) Microalgae were classified and counted inthe laboratory by first diluting each replicate 5minus10times Five sub-replicates of 002 ml were then examined under an inverted microscope

Epifauna abundance and taxa composition

Epifauna included both meiofauna (metazoans thatcan pass through a 1 mm sieve and are retained on a38 μm sieve) and macrofauna (organisms retained on1 mm sieve) occurring on the decomposing man-grove leaf litter

Mangrove leaf litter was sampled weekly in tripli-cates by pooling 3 decomposing leaves per replicatein a plastic bag Each group of decomposing leaves

was immediately mixed with 8 magnesium chlo-ride to shock the attached epifauna thoroughly agi-tated then sieved through 1 mm and 38 μm mesh sizesieves Sieved fauna was gently washed from the38 μm sieve with a soft spray of filtered fresh waterpreserved in 4 formaline and stained with a fewdrops of 1 solution Bengal rose Epifauna wereidentified and counted at major taxa level using abinocular microscope and densities were standard-ized towards leaf surface (ie per cm2)

Species diversity and evenness of main microalgaeand epifauna groups

The Shannon-Wiener index (H rsquo) and the equitabil-ity index (EH) were used for the estimation of micro-algae and epifauna community diversity and even-ness based on the natural log (ln) (Shannon 1948) H rsquois an accurate measure of species diversity in an areasince it not only considers the number of species butalso relative abundance of the specific species Insimple terms it considers the relationship betweenthe number of species and the number of individuals(in a given area or in a given sample) (Spellerberg ampFedor 2003) The following formulas were used

(2)

(3)

where S is the total number of species in the commu-nity and Pi is the proportion of S made up by the i th

species Species equitability or evenness (EH) wasinterpreted within the range 0minus1 with values closeto 0 signifying dominance by a single species andclose to 1 indicating many species present with equalnumbers (high evenness)

Microalgae biomass

Mangrove leaves were sampled weekly in tripli-cates consisting of 3 leaves per sample The peri-phytic biofilm was gently scraped from the surface ofthe leaves with a known volume of filtered seawaterand were GFF filtered (045 μm mesh 47 mm diam-eter) Phytopigments were extracted from the col-lected biofilm after adding 10 ml 90 acetone to thelyophylized GFF filters at 4degC in the dark and thesupernatant was analyzed for chlorophyll a accord-ing to the protocol of Granger amp Lizumi (2001)

timesInitial weight ndash Final weightInitial weight

100

rsquo lni i1

H P Pi

n

sum= minus sdot=

EHrsquo

lnH

S=

75


Environmental factors

Light intensity and water transparency were re -corded daily at noon using a Hanna HI97500 luxmeter and Secchi disk The quality of the mid-waterwas monitored by weekly measurements of tem -perature dissolved oxygen pH salinity and TANTemperature dissolved oxygen and pH were meas-ured using meters salinity was measured using arefractometer and TAN was analyzed in the labora-tory according to Eaton et al (2005) Un-ionizedammonia (NH3) toxicity was assessed using the TAN(NH4-N) to ammonia-nitrogen (NH3-N) (pH temper-ature and salinity-thermodynamic dependent) ratioas described by Spotte amp Adams (1983)

Data analysis

Repeated-measures ANOVA was performed withthe software Statistica 7 Time was the repeatedmeasure with sunlight and sediment treatments asfixed factors This statistical method was selectedbecause leaf litter and water quality parameters wererepeatedly sampled from the same tanks at eachsampling time Therefore the sampling dates weredependent on each other All data were checked fornormality and variance homogeneity requirementsfor parametric analysis Data that did not meet normality requirements after being transformedwere analyzed nonparametrically following Kruskal-Wallis ANOVA and median test Multidimensionalscaling and 2-way ANOSIM using Primer 60 soft-ware (Clarke amp Gorley 2006) were used to comparesimilarity in species distribution The Shannon-Wiener index was used to estimate thediversity and evenness of the community ofthe microalgae and epifauna colonizing thedecomposing mangrove litter at the differ-ent conditions of sunlight and sediment

RESULTS


Mangrove leaf litter incubated with sedi-ment and exposed to direct sunlight re -corded the highest percentage weight loss(mean plusmn SD 703 plusmn 23) during the 7th

week of decomposition and was signifi-cantly more decomposed compared to litterincubated without sediment and in the

shade (Tukeyrsquos HSD p lt 001) (Fig 1) Litter incu-bated in sunlight without sediment recorded the low-est mean (plusmnSD) weight loss (425 plusmn 42) and did notsignificantly differ from litter incubated in the shadeindependent of the presence or absence of sediment(Tukeyrsquos HSD p gt 005)

Microalgae biomass

Decomposing mangrove leaf litter exposed to sun-light supported significantly higher biomass of micro -algae compared to litter decomposing in the shade(Tukeyrsquos HSD p lt 0001) Compared to sediment thelight effect was the determining factor (p lt 005) andthe disparity between the sunlit and shaded treat-ments during the 4th week of leaf litter decomposi-tion greatly influenced the statistical results (sunlit9282 plusmn 6153 μg lminus1 chl a N = 3 shaded 298 plusmn138 μg lminus1 chl a N = 3 mean plusmn SD) (Fig 2)

Microalgae taxonomic composition

Nine major taxa of microalgae were identified asabundant in the periphytic biofilm present on decom-posing mangrove leaf litter diatoms Cyanobacteriadinoflagellates Zygnemophyceae ChlorophyceaeChrysophyceae flagellates Euglenozoa and Cocco -lithales Diatoms dominated the microalgae commu-nity on leaf litter decomposed for a period of lt6 wkespecially during the 4th week when the highestaverage (plusmnSD) abundance of 15 times 104 plusmn 73 times 103 cellsmlminus1 was recorded in leaf litter decomposing underdirect sunlight in the presence of sediment (Fig 3)

76

0

10

20

30

40

50

60

70

80

0 1 3 4 5 7

Per

cent

age

wei

ght

loss

Duration of decomposition (Week)

DS DX LS LX

Fig 1 Decomposition of mangrove leaf litter of Rhizophora mucronataincubated in seawater microcosms at different ambient conditionsshade with (DS) or without sediment (DX) sunlight with (LS) or without

sediment (LX) Error bars represent SD


Leaf litter decomposing under sunlight in absence ofsedi ment supported the highest abundance ofCyanobacteria (33 times 108 plusmn 28 times 108 cells mlminus1 meanplusmn SE) during the 7th week of decomposition How-ever the abundance of microalgae on leaf litterdecomposed for lt6 wk was not significantly differentin all treatments (p gt 005) except for the treatmentexposed to sunlight in the absence of sedimentwhich differed significantly during the 7th week ofdecomposition (Tukeyrsquos HSD p lt 001)

Microalgae species diversity

Among the 9 major taxa of microalgae 23 specieswere identified including 6 diatom species 5 Cyano-bacteria species 5 dinoflagellate species 1 Zygnemo -phyceae species 3 Chlorophyceae species 1 Chryso-phyceae species 1 flagellate species and 1 Cocco -lithales species The diatoms Navicula sp and Pleu-rosigma sp were the most predominant speciesNavicula sp dominated litter decomposing in theshade with a proportion of 85 and 79 in thepresence and absence of sediment respectivelyAmong the Cyanobacteria Microcystis sp domi-nated the decomposing litter exposed to sunlight inthe absence of sediment reaching a proportionalcover of 999 during the 7th week Also amongCyanobacteria Anabaena sp dominated the litterincubated in the shade without sediment whileOscillatoria sp was dominant in litter incubated inthe shade in the presence of sediment The highestmicroalgae diversity was recorded in decomposingmangrove litter exposed to sunlight in the presenceof sediment (H rsquo = 108) concomitantly with the high-

est species evenness (EH = 0092) (Table 1)The microalgae community differed signifi-cantly between all treatments (2-way crossedANOSIM light and sediment R = 0362 p =0002 and week R = 0414 p = 0001) espe-cially due to the light effect (2-way crossedANOSIM R = 0463 p = 0003) (Fig 4a)

Epifauna abundance and diversity

Eighteen major taxa of epifauna were iden-tified in the meiofauna fraction RotiferaCopepoda Foraminifera Polychaeta Nema-toda Insecta Cnidaria Gastropoda Oligo -chaeta Turbellaria Amphipoda MysidaOstra coda Bivalvia Oikopleura TanaidaceaKinorhyncha and Cumacea

The epifauna colonizing decomposing mangroveleaf litter differed significantly between differenttreatments across the week groups especially dueto the effect of light (2-way crossed ANOSIM R =0426minus0704 p = 0001) (Fig 4b) Decomposing man-grove litter exposed to sunlight supported signifi-cantly higher abundance of epifauna compared to litter incubated in the shade (p = 0002) The abun-dance of epifauna in the shade increased after the 4th

week of litter decomposition During Weeks 5 and 7decomposing litter exposed to sunlight in the pres-ence of sediment supported the highest mean abun-dance of epifauna (22 plusmn 11 ind cmminus2 mean plusmn SD)which significantly differed (Tukeyrsquos HSD p lt 005)from litter incubated in the shade especially withsediment which supported the lowest abundance ofepifauna (04 plusmn 03 ind cmminus2) (Fig 5)

Rotifera and Copepoda dominated the shadedmangrove litter decomposing in the absence of sedi-ment with a proportion of 34 and 55 respec-tively whereas Polychaeta preferred conditions re -ceiving direct sunlight Nematoda preferred condi-tions with sediment Litter decomposing in the pres-ence of sediment supported the highest diversityand an evenly distributed assembly of the differentclasses of epifauna regardless of light conditions(Table 2)


A significantly higher light intensity was recordedfor the sunlight treatments (97 053 plusmn 7093 lux mean plusmnSD) than the shaded treatments (2224 plusmn 703 lux) (p lt005) All treatments recorded water transparency of

77

0

20

40

60

80

100

120

140

160

180

DS DX LS LX

Treatment

Alg

al b

iom

ass

(chl

a micro

g lndash

1 ) Wk 1 Wk 3 Wk 4 Wk 5 Wk 7

Fig 2 Biomass of microalgae in biofilm developing on mangrove leaf lit-ter of Rhizophora mucronata incubated in seawater microcosms at differ-ent time intervals and different ambient conditions shade with (DS)or without sediment (DX) sunlight with (LS) or without sediment (LX)

Error bars represent SD


not less than the set-up water depth of 075 m Thewater in the tanks supporting decomposing mangrovelitter exposed to sunlight had high dissolved oxygentemperature and pH but low levels of TAN The con-centration of dissolved oxygen in the sunlight treat-ments ranged between 65 plusmn 08 and 30 plusmn 05 mg lminus1

(mean plusmn SD) whereas it was significantly lower (p lt

005) in the shade treatments ranging between 29 plusmn04 and 02 plusmn 01 mg lminus1 (Fig 6a) Although there wasno statistical difference in terms of temperature (p gt005) and pH (p gt 005) between the sunlight andshade treatments temperature and pH were generallylow in the shade treatments (Fig 6bc) The lowest pH(54 plusmn 01) was recorded in the shaded tanks without

78

0

1000

2000

3000

4000

5000

6000

7000

8000 Week 3

DS

DX

LS

LX

DS

DX

LS

LX

0

1000

2000

3000

4000

5000

6000

DS

Week 1

DX

LS

LX

0

5000

10000

15000

20000

25000 Week 4

0

2000

4000

6000

8000

10000

12000 Week 5

DS

DX

LS

LX

Ab

und

ance

of m

icro

alga

e (c

ells

mlndash

1 )

Microalgae taxa

a

c

b

d

6 x 108

5 x 108

4 x 108

3 x 108

2 x 108

1 x 108

DS

Week 7

D

LS

LX

Microalgae taxa

e

05000

10000150002000025000

Fig 3 Abundance of different microalgae taxa colo-nizing biofilm developing on mangrove leaf litter ofRhizophora mucronata incubated in seawater micro-cosms at different ambient conditions shade with (DS)or without sediment (DX) sunlight with (LS) or with-out sediment (LX) at (a) Week 1 (b) Week 3 (c) Week4 (d) Week 5 and (e) Week 7 Error bars represent SD


sediment during the 4th week of lit-ter decomposition During thesame period the tank without sed-iment had an increase in TANwhich progressed to a much higherconcentration of 00078 plusmn 00055mg lminus1 (mean plusmn SD) during the 5th

week of decomposition Howeverthe highest levels of TAN (0038 plusmn0006 mg lminus1) were re corded in theshade treatments with sedimentduring the 1st week of litter decom-position but then declined overtime (Fig 6d)

DISCUSSION


The ecological approach ofshrimp aquaculture in mangroveforests implies that mangrove leaflitter falls into the shrimp pondand plays a potentially impor -tant function in the ecological processes within the pond Theseprocesses may be limited by theexposure of decomposing man-grove leaf litter to sunlight due toshading by mangrove trees andcontact with sediment

In our present study we ob -served that mangrove leaf litter

79

DS DX LS LX

Microalgae taxaDiatoms Guinardia sp 00 00 00 3 times 10minus5

Nitzschia sp 00 004 00 3 times 10minus5

Navicula sp 8495 7857 6587 0004Rhizosolenia sp 00 00 00 00Pleurosigma sp 581 146 2066 9 times 10minus5

Coscinodiscus sp 089 046 008 8 times 10minus5

Fragilaria sp 030 00 00 00Striatella unipunctata sp 015 00 00 00

Cyanobacteria Anabaena sp 015 593 315 51 times 10minus4

Pseudo-anabaena sp 00 00 024 00Oscillatoria sp 417 029 065 00Microcystis sp 00 246 621 9999Spirulina sp 149 072 040 13 times 10minus4

Dinoflagellates Gyrodinium sp 00 00 008 00Protoperidinium sp 134 132 008 8 times 10minus5

Prorocentrum sp 015 014 00 00Ostreopsis sp 00 014 00 5 times 10minus5

Peridinium sp 015 00 00 00

Flagellates Choanoflagellate sp 00 00 008 1 times 10minus5

Coccolithales Coccolithus sp 00 00 008 00

Zygnemophyceae Cosmarium sp 00 804 024 00

Chlorophyceae Scenedesmus sp 00 014 00 1 times 10minus5

Dunaliella sp 015 00 202 7 times 10minus5

Chloromonas sp 00 00 00 8 times 10minus5

Chrysophyceae Dinobryon sp 030 029 016 00

Diversity and evennessDiversity index (H rsquo) 06824 08953 10841 00007Species evenness (EH) 00614 00803 00924 31 times 10minus5

Table 1 Proportional assemblage of microalgae in biofilm developing on man-grove leaf litter of Rhizophora mucronata incubated in seawater microcosms at dif-ferent ambient conditions shade with (DS) or without sediment (DX) sunlight with(LS) or without sediment (LX) and species diversity and evenness Microalgae

data are percentages calculated from all weeks pooled together

DSTreatment DX LS LX

2D stress 013 2D stress 015a b

Fig 4 Multidimensional scaling plot of similarity in (a) microalgae and (b) epifauna colonizing biofilm on decomposing man-grove leaf litter of Rhizophora mucronata incubated in seawater microcosms at different ambient conditions shade with (DS)

or without sediment (DX) sunlight with (LS) or without sediment (LX)


exposed to sunlight in the presence of sedimentdegraded faster than litter decomposing in the shadeAlthough sunlight has been observed to directlyenhance the rate of decomposition of plant leaf litterthrough photo degradation (Gallo et al 2009) otherstudies have observed decomposition as being medi-ated by associated macrobiota (Franken et al 2005)

microbiota (Francoeur et al 2006) andadsorption of nutrients by sediment(Avnimelech amp Gad 2003)

In our study litter exposed to sunlightseem to be characterized by a higherabundance of microalgae and epifaunacompared to litter incubated in theshade Francoeur et al (2006) observedthat the extracellular enzyme activity inmicrobial communities colonizing natu-ral organic substrata is stimulated bylight and photosynthesis which is com-mon in microbial communities associ-ated with natural decaying plant litter inwetlands Sediment also has a signifi-cant tendency in promoting proliferationof microfauna (Avnimelech amp Gad 2003)By stimulating microbial activities ex po -

sure to sunlight and sediment is therefore an impor-tant physical parameter influencing the microbiallymediated decomposition of mangrove leaf litter inecological shrimp culture systems The effect of sunlight on abundance and activities of the epifaunain litter decomposition is an indirect process asexplained by Franken et al (2005) Light intensityfirst influences algal biomass density and composi-tion which in turn positively influence the growth ofepifauna some of which are efficient shredders ofthe decomposing leaf litter

The higher decomposition of mangrove leaf litterexposed to sunlight and in the presence of sedimentsuggests a synergistic effect of light sediment andthe associated organisms in enhancing the decompo-sition of submerged mangrove leaf litter Accordingto Avnimelech amp Gad (2003) the concentrations ofnutrients including organic carbon compounds inthe shrimp pond bottom soil are higher than thosefound in the water column Hence the bottom be -comes the favorable site for microbial developmentdue to the availability of organic matter In the pres-ent study the sediment was not sterilized The rapiddecomposition of mangrove leaf litter incubated withsediment may be due to the higher microbial loadcontributed by the sediment Although the sedimentgrain size was not measured the sediment used inthe study was obtained from the shrimp pond bottomwhich is characterized by small grain size (Burford etal 1998) The smaller sediment grain size may havealso influenced a high microbial load (Burford et al1998) Mangrove leaf litter exposed to sunlight inthe absence of sediment seems to have decomposedslowly defying the potential photodegradation influ-ences of sunlight The possible influence of the pre-

80

0

05

1

15

2

25

3

35

4

0 1 3 4 5 7

Ab

und

ance

of e

pifa

una

(no

cm

ndash2)

Duration of litter decomposition (Week)

DS DX LS LX

Fig 5 Abundance of epifauna in biofilm developing on mangrove leaf litterof Rhizophora mucronata incubated in seawater microcosms at differentambient conditions shade with (DS) or without sediment (DX) sunlight

with (LS) or without sediment (LX) Error bars represent SD

DS DX LS LX

Epifauna taxaRotifera 1098 3421 2103 4030Copepoda 4074 5508 3306 1109Foraminifera 1479 030 243 023Polychaeta 581 459 1450 1557Nematoda 2399 353 2454 3081Insecta 012 004 001 000Cnidaria 018 000 006 031Gastropoda 018 030 047 041Oligochaeta 012 004 000 000Turbellaria 190 143 356 119Amphipoda 000 004 001 000Mysida 006 000 000 000Ostracoda 025 019 028 009Bivalvia 000 000 001 000Oikopleura 000 000 001 000Tanaidacea 012 019 002 000Kinorhyncha 012 000 000 000Cumacea 072 008 000 000

Diversity and evennessDiversity index (H rsquo) 159 109 158 138Species evenness (EH) 021 013 017 015

Table 2 Proportional assemblage of epifauna on biofilmdeveloping on mangrove leaf litter of Rhizophora mucronataincubated in seawater microcosms at different ambient con-ditions shade with (DS) or without sediment (DX) sunlightwith (LS) or without sediment (LX) and species diversityand evenness Epifauna data are percentages calculated from

all weeks pooled together


dominant Cyanobacteria on the slow decompositioncannot be connected to a possible disruption of theshredding effect of the epifauna This is because theabundance of the epifauna community was similar tothat on the fast-decomposing mangrove leaf litter inthe presence of sediment Further analysis is requiredto assess the biochemical interaction of the Cyano-bacteria with the various decomposition processes ofmangrove leaf litter in the absence of sediment

Effect of direct sunlight on natural food supply

The exposure of pond water to sunlight is crucial inpromoting primary production which is the baselinefor energy transfer to higher trophic levels in the pondfood web The relevance of this pathway dependson the nutritional value of the primary producer to theimmediate (primary) or secondary consumers In ourpresent study decomposing mangrove litter exposedto sunlight supported the largest biomass of micro-algae compared to litter decomposing in the shadeThis was expected since sunlight is essential for photosynthesis and thus for primary productivity Thesynergy in the combination of sunlight and sediment

in promoting the diversity of epifauna was clearlydemonstrated This ecological condition is beneficialin promoting natural food sources in shrimp culturesystems The absence of sediment seems to favor pro-liferation of a dominant species of microalgae Thiscould be a result of a modification of environmentalconditions Sediment therefore seems to complementsunlight in the shrimp pond food web which thereforesuggests it is an important condition in maintainingthe ecological stability of the shrimp culture system

The dominating presence of polychaetes on litterdecomposing in sunlight suggests the importanceof placing shrimp culture systems outside mangrovecanopy to promote growth of polychaetes which area potential natural food for post-larvae of penaeidshrimps (Nunes amp Parsons 2000) In addition the im -portance of sediment was observed in the im provedproliferation of diatoms especially Navicula andPleurosigma spp which are of nutritional impor-tance in supporting ecological shrimp aquaculture(Bombeo-Tuburan et al 1993 Abu Hena amp Hisha -muddin 2012) Litter decomposing in the absence ofsediment supported only Cyanobacteria dominatedby Microcystis spp Microcystis is known to pro-duce a potent hepatotoxin a microcystin that is also

81

00005001

0015002

0025003

0035004

0045005

0 1 3 4 5 75

55

6

65

7

75

8

85

0 1 3 4 5 7

26

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0 1 3 4 5 7

DS DX

Tem

per

atur

e (deg

C)


LS LX

0

1

2

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0 1 3 4 5 7

Dis

solv

ed o

xyg

en (m

g lndash

1)

Tota

l am

mon

ium

nitr

ogen

(mg

lndash1 )

pH

a b

c d

Fig 6 Water quality parameters (a dissolved oxygen b temperature c pH d total ammonium nitrogen) of seawater in mi-crocosms with decomposing mangrove leaf litter of Rhizophora mucronata at different ambient conditions shade with (DS) or

without sediment (DX) sunlight with (LS) or without sediment (LX) Error bars represent SD


produced by a number of planktonic Cyanobacteriagenera such as Anabaena Anabaenopsis Nostocand Planktothrix (Oscillatoria) (Amado amp Monserrat2010) and other bioactive metabolites with potentialto degrade the nutritional status of aquaculture spe-cies (inhibitors of proteases and grazer deterrents)(Schrader et al 1998 Smith et al 2008)

Diatoms especially Navicula spp continued togrow in the shade although in lower abundancescompared to sunlight conditions and could be thereason behind the continued growth of copepods onlitter decomposing in the shade The diatoms Navic-ula and Nitzschia spp are capable of growing in theshade since they can adopt a heterotrophic mode offeeding (Lewin 1953 Admiraal amp Peletier 1979) TheCyanobacteria Anabaena and Oscillatoria were alsofound to thrive on litter decomposing in the shadeThe filamentous nitrogen-fixing A variabilis is capa-ble of heterotrophic growth in complete darkness(Mannan amp Pakrasi 1993) Nevertheless our presentstudy revealed reduced abundance of Cyanobacteriaon litter decomposing in the presence of sediment asfurther demonstrated by elevated growth of Cyano-bacteria in bare sunlight treatments during the 7th

week of litter decomposition This observation eluci-dates the importance of coupling sediment and sun-light in enabling the decomposing mangrove litter tosupport the growth of high-quality food microalgaein ecological shrimp culture systems Application ofsubstrates to promote growth of biofilm in shrimpculture systems without sediment should thereforebe approached with caution since the low food-quality Cyanobacteria may dominate Sediment playan important role in providing a whole range of nutri-ents required for the growth of different types ofmicroalgae (Avnimelech amp Gad 2003) The concen-trations of nutrients in sediment are higher thanthose recorded in pond water (Avnimelech amp Gad2003) Sediment accumulated in shrimp culture sys-tems is typically highly enriched in nitrogen andphosphorous (Boyd et al 1994) which are importantnutrients in supporting proliferation of microalgae

Effect of sunlight on environmental conditions

Sunlight is capable of influencing the dynamics ofvarious water quality parameters and therefore playsan important role in determining the ecologicalhealth of a shrimp pond in a mangrove forest In thepresent study tanks with decomposing litter in theshade were low in dissolved oxygen compared tothose exposed to sunlight Sunlight promotes photo-

synthesis whereby CO2 is absorbed and oxygen isreleased as a result (Dawes 1998) This process canoxygenate the sediment at the pond bottom (Avnim-elech amp Gad 2003) According to Avnimelech amp Gad(2003) algae produce oxygen during the day leadingto oxygen enrichment of the water column especiallythe top layer Although the diffusion of oxygen to thesediment is slow wind and mechanically drivenwater currents mix the water column and bring someof the oxygen to the bottom layers The importance ofmicroalgae in promoting oxygen in water dependson the type of algae Cyanobacteria is not a preferredfood by epifauna and shrimp (Preston et al 1998)This microalgae is therefore likely to bloom in thebiofilm and then collapse Subsequent decomposi-tion of dead Cyanobacteria by bacteria would con-sume a lot of dissolved oxygen from the water On theother hand diatoms are preferred food for epifaunaand shrimp (Brown amp Jeffrey 1995 Borowitzka 1997De Troch et al 2010) Diatoms would therefore nottend to bloom in the biofilm if grazing by the epi-fauna is adequate Epifauna and shrimp feeding ondiatoms would consume less oxygen than bacteriaresulting in a positive oxygen balance When Cyano-bacteria die they float and form a layer on the watersurface and thus cut off sunlight to the pond waterreducing the amount of photosynthesis in the waterDead diatoms would remain attached to the litter orsink (Smetacek 1985) to the bottom of the pond Thewater above would remain clear and exposed to sun-light allowing photosynthesis to continue In thepresence of sediment diatoms would therefore con-tribute as the net producers of oxygen and as poten-tial regulators of water quality whereas Cyanobac-teria would not

In the absence of adequate sunlight the bottomsediment and decomposing mangrove litter providelarge amounts of organic matter which are favorableconditions for microbial development (Avnimelech ampGad 2003) Bacteria consume large amounts of oxy-gen (Avnimelech amp Gad 2003) and with no oxygenproduction due to the absence of photosyntheticactivity the water and the sediment become anoxicIn our present study litter decomposing in the shadein the presence of sediment was characterized by relatively higher TAN especially during the earlystages of decomposition as observed in Weeks 1 and3 and low dissolved oxygen levels In case of deple-tion of oxygen denitrification occurs in the organicmatter with nitrate as an electron acceptor (Reddy etal 1986) Due to microbial metabolism of nitrogenouscompounds an increase of ammonium in the watercan be expected (Chien 1992) Another pathway of

82


ammonium accumulation is when sulfate is used asan electron acceptor and sulfide is released (Chien1992) The released sulfide inhibits nitrification(Joye amp Hallibaugh 1995) These reactions couldhave largely contributed to the increased levels ofTAN in the tanks with mangrove leaf litter decom-posing in the shade even more than in the presenceof sediment

Potential toxicity to post-larval shrimp

The water quality in shaded tanks has the potentialto build a toxic environment for macroinvertebratesincluding post-larval shrimp When oxygen is de-pleted other terminal electron acceptors such as ni-trate iron manganese sulfate and CO2 can be usedto mediate microbial decomposition of organic matter(Reddy et al 1986) This could lead to the productionof reduced and potentially toxic compounds such asnitrite un-ionized ammonia reduced divalent man-ganese hydrogen sulfide organic acids and methane(Nix amp Ingols 1981 Chien 1992 Boyd 1998 Avnim-elech amp Gad 2003) Another important reaction underanaerobic conditions is the fermentation of organicsubstrates by fermenting bacteria releasing reducedacids alcohols CO2 and hydrogen which produce offensive odors and some are toxic to shrimp (Mori-arty 1997) The potential to produce re duced acidsCO2 hydrogen sulfides and hydrogen ions could havecontributed to the reduced levels of pH in the tankswith mangrove litter decomposing in the shade

Litter decomposing in the shade was characterizedby pH values as low as 54 Low pH (lt60) can stressshrimp and cause limited calcification and poor survival (Kater et al 2006) It increases nitrite toxicityto fish and has similar effects on shrimp (Kater et al2006) The combined toxicity of both TAN (NH4-N)and ammonia-nitrogen (NH3-N) occurs at pH lt 83(Kater et al 2006) Un-ionized ammonia (NH3) is themore toxic form of ammonia to post-larvae of penaeidshrimps and occurs at elevated temperature and pHgt 83 (Chien 1992) The safe level of un-ionizedammonia for post-larvae of Penaeus monodon aged 6to 25 d is 01 mg lminus1 (Chien 1992) or 111 mg lminus1 TANat pH 82 295degC and a salinity of 34 (Spotte amp Adams1983) In our experiment the levels of TAN werelower than the allowable upper limit However theslightly higher TAN levels observed in the shadedtreatments especially with sediment suggest an in -creased potential of TAN toxicity if the incidence ofsunlight is limited Low pH levels as observed in theshaded tanks can increase the fraction of un-ionized

hydrogen sulfide (H2S) which is toxic to post-larvalshrimp (Chien 1992)

The above observations demonstrate the importanceof exposing decomposing mangrove leaf litter to sun-light and sediment especially in situations whereecological shrimp culture systems may be under adense canopy of mangrove trees The use of multiplelayers of leaf litter shading each other should also beavoided Some observations have been made indica-ting that a moderate load not exceeding 1 g lminus1 ofmangrove litter could play an important role in pro-moting shrimp growth and survival in aerobic condi-tions (Hai amp Yakupitiyage 2005) In this respect ourstudy demonstrates the additional advantage of sunlight and sediment in enhancing the proliferationof high-quality natural food from the decomposingmangrove leaf litter

CONCLUSION

This study highlights the synergistic effect betweensediment and sunlight in maintaining a high diver-sity of microalgae and good water quality favorablefor the culture of post-larval shrimp In the presenceof sunlight a lack of sediment enhances the growthof Cyanobacteria (Microcystis spp) on mangrove litter decomposed for a period gt5 wk Howevershading cannot be relied upon as a deterrent sinceCyanobacteria (especially Anabaena spp and Oscil-latoria spp) may continue to colonize mangrove litterdecomposing in the shade with considerable successFurthermore shading of decomposing mangrove litterinhibits growth of polychaetes which are potentialfood for post-larval shrimp

This study supports promoting an environmentallyfriendly system of culturing shrimps in less forestedareas In case a situation arises where leaf litter mustbe used to promote biofilm as natural food for shrimpthen complete shading of the culture system shouldbe avoided This study demonstrated synergy in thecombination of sunlight and sediment in promotingthe proliferation of high-quality natural food forpenaeid shrimps moderating water quality and con-trolling blooms of Cyanobacteria The findings mayalso provide an important economic insight into thedesign and management of liner-based shrimp cul-ture systems The synergy between sunlight and sediment in maintaining a stable environment canbe em ployed to limit the use of pond liners and re -duce the frequency of removing sludge which tendsto accumulate at the bottom of lined ponds for theculture of both crustaceans and finfish

83


Acknowledgements CG thanks the Flemish InterUniver-sity Council (VLIRUOS) for the financial support Deeply feltthanks to KMFRI laboratory technicians Kilonzi MagaraMkonu Onduso Adungosi Okemwa Ogola and the youthand community members of the Majaoni silvofishery pro-ject Kenya for their field assistance

LITERATURE CITED

Abu Hena MK Hishamuddin O (2012) Food selection pref-erence of different ages and sizes of black tiger shrimpPenaeus monodon Fabricius in tropical aquacultureponds in Malaysia Afr J Biotechnol 11 6153minus6159

Admiraal W Peletier H (1979) Influence of organic com-pounds and light limitation on the growth rate of estuar-ine benthic diatoms Br Phycol J 14 197minus206

Amado LL Monserrat JM (2010) Oxidative stress genera-tion by microcystins in aquatic animals why and howEnviron Int 36 226minus235

Asaduzzaman M Wahab MA Verdegem MCJ Huque SSalam MA Azim ME (2008) CN ratio control and substrate addition for periphyton development jointlyenhance freshwater prawn Macrobrachium rosenbergiiproduction in ponds Aquaculture 280 117minus123

Avnimelech Y Gad R (2003) Shrimp and fish pond soils processes and management Aquaculture 220 549minus567

Azim ME Wahab MA (2005) Periphyton based pond poly-culture In Azim ME Verdegem MCJ van Dam AABeveridge MCM (eds) Periphyton ecology exploita-tion and management CABI Publishing Wallingfordp 207minus222

Benner R Hodson RE (1985) Microbial degradation of theleachable and lignocellulosic components of leaves andwood from Rhizophora mangle in a tropical mangroveswamp Mar Ecol Prog Ser 23 221minus230

Bombeo-Tuburan I Guanzon NG Jr Schroeder GL (1993)Production of Penaeus monodon (Fabricius) using fournatural food types in an extensive system Aquaculture112 57minus65

Borowitzka M (1997) Microalgae for aquaculture opportu-nities and constraints J Appl Phycol 9 393minus401

Boyd CE (1998) Pond water aeration systems Aquacult Eng18 9minus40

Boyd CE Tanner ME Madkour M Masuda K (1994) Chem-ical characteristics of bottom soils from freshwater andbrackishwater aquaculture ponds J World Aquacult Soc25 517minus534

Bratvold D Browdy CL (2001) Effects of sand sediment andvertical surfaces (Aquamats) on production water qual-ity and microbial ecology in an intensive Litopenaeusvannamei culture system Aquaculture 195 81minus94

Brown MR Jeffrey SW (1995) The amino acid and grosscomposition of marine diatoms potentially useful for mar-iculture J Appl Phycol 7 521minus527

Burford MA (1997) Phytoplankton dynamics in shrimpponds Aquacult Res 28 351minus360

Burford MA Peterson EL Baiano JCF Preston NP (1998)Bacteria in shrimp pond sediments their role in mineral-izing nutrients and some suggested sampling strategiesAquacult Res 29 843minus849

Burford MA Thompson PJ McIntosh RP Bauman RH Pearson DC (2003) Nutrient and microbial dynamics inhigh-intensity zero-exchange shrimp ponds in BelizeAquaculture 219 393minus411

Chien YH (1992) Water quality requirements and manage-ment for marine shrimp culture In Wyban J (ed) ProcSpec Sess Shrimp Farming World Aquaculture SocietyBaton Rouge LA p 144minus156

Clarke KR Gorley RN (2006) PRIMER v6 user manualtutorial PRIMER-E Plymouth

Dawes CJ (1998) Marine botany 2nd edn John Wiley ampSons New York NY

De Troch M Cnudde C Willems A Moens T Vanreusel A(2010) Bacterial colonization on fecal pellets of Harpacti-coid copepods and on their diatom food Microb Ecol 60 581minus591

Eaton AD Clesceri LS Rice EW Greenberg AE FransonAH (eds) (2005) Standard methods for the examination ofwater and wastewater American Public Health Associa-tion (APHA-AWWA-WEF) Washington DC

Fitzgerald WJ Jr (2000) Integrated mangrove forest andaquaculture systems in Indonesia In Primavera JH Gar-cia LMB Castranos MT Surtida MB (eds) Mangrove-friendly aquaculture Proceedings of the workshop onmangrove-friendly aquaculture SEAFDEC AquacultureDepartment January 11ndash15 1999 Iloilo City p 21minus34

Francoeur SN Schaecher M Neely RK Kuehn KA (2006)Periphytic photosynthetic stimulation of extracellularenzyme activity in aquatic microbial communities associ-ated with decaying Typha litter Microb Ecol 52 662minus669

Franken RJM Waluto B Peeters ETHM Gardeniers JJPBeijer JAJ Scheffer M (2005) Growth of shredders onleaf litter biofilms the effect of light intensity FreshwBiol 50 459minus466

Gallo ME Porras-Alfaro A Odenbach KJ Sinsabaugh RL(2009) Photoacceleration of plant litter decompositionin an arid environment Soil Biol Biochem 41 1433minus1441

Gatune C Vanreusel A Cnudde C Ruwa R Bossier P DeTroch M (2012) Decomposing mangrove litter supports amicrobial biofilm with potential nutritive value to penaeidshrimp post larvae J Exp Mar Biol Ecol 426minus427 28minus38

Gatune C Vanreusel A Ruwa R Bossier P De Troch M(2014a) Growth and survival of post-larval giant tigershrimp Penaeus monodon feeding on mangrove leaf litter biofilms Mar Ecol Prog Ser 511 117minus128

Gatune WC Vanreusel A Ruwa R Bossier P De Troch M(2014b) Fatty acid profiling reveals a trophic link be -tween mangrove leaf litter biofilms and the post-larvaeof giant tiger shrimp Penaeus monodon Aquacult Envi-ron Interact 6 1minus10

Granger S Lizumi H (2001) Water quality measurementmethods for seagrass habitat In Short FT Coles RG(eds) Global seagrass research methods Elsevier ScienceAmsterdam p 402minus404

Hai TN Yakupitiyage A (2005) The effects of the decompo-sition of mangrove leaf litter on water quality growthand survival of black tiger shrimp (Penaeus monodonFabricius 1798) Aquaculture 250 700minus712

Joye SB Hallibaugh JT (1995) influence of sulfide inhibitionof nitrification on nitrogen regeneration in sedimentsScience 270 623minus625

Kater BJ Dubbeldam M Postma JF (2006) Ammonium toxi-city at high pH in a marine bioassay using Corophiumvolutator Arch Environ Contam Toxicol 51 347minus351

Kautsky N Folke C Roumlnnbaumlck P Troell M Beveridge MPrimavera J (2001) Aquaculture In Levin SA (ed) Ency-clopedia of biodiversity Vol 1 Elsevier New York NYp 185minus198

Lewin JC (1953) Heterotrophy in diatoms J Gen Microbiol

84


9 305minus313Mannan RM Pakrasi HB (1993) Dark heterotrophic growth

conditions result in an increase in the content of photo-system II units in the filamentous cyanobacterium Ana -baena variabilis ATCC 29413 Plant Physiol 103 971minus977

Moriarty JW (1997) The role of micro-organisms in aqua -culture ponds Aquaculture 151 333minus349

Nix J Ingols R (1981) Oxidized manganese from hypolim-netic water as a possible cause of trout mortality inhatcheries Prog Fish-Cult 43 32minus36

Nunes AJP Parsons GJ (2000) Effects of the Southern brownshrimp Penaeus subtilis predation and artificial feedingon the population dynamics of benthic polychaetes intropical pond enclosures Aquaculture 183 125minus147

Otoshi CA Montgomery AD Matsuda EM Moss SM (2006)Effects of artificial substrate and water source on growthof juvenile Pacific white shrimp Litopenaeus vannameiJ World Aquacult Soc 37 210minus213

Pascal P Dupuy C Richard P Rzeznik-Orignac J Niquil N(2008) Bacterivory of a mudflat nematode communityunder different environmental conditions Mar Biol 154 671minus682

Preston NP Burford MA Stenzel DJ (1998) Effects of Tricho -desmium spp blooms on penaeid prawn larvae Mar Biol131 671minus679

Primavera JH (1998) Tropical shrimp farming and its sustainability In De Silva S (ed) Tropical maricultureAcademic Press New York NY p 257minus289

Rajendran N Kathiresan K (2007) Microbial flora associated

with submerged mangrove leaf litter in India Rev BiolTrop 55 393minus400

Reddy KR Feijtel TC Patrick WH Jr (1986) Effect of soilredox conditions on microbial oxidation of organic mat-ter In Chen Y Avnimelech Y (eds) The role of organicmatter in modern agriculture Martinus Nijhoff Publish-ers Dordrecht p 117minus156

Schrader KK de Regt MQ Tidwell PR Tucker CS Duke SO(1998) Selective growth inhibition of the musty-odor producing cyanobacterium Oscillatoria cf chalybea bynatural compounds Bull Environ Contam Toxicol 60 651minus658

Smetacek VS (1985) Role of sinking in diatom life-historycycles ecological evolutionary and geological signifi-cance Mar Biol 84 239minus251

Smith JL Boyer GL Zimba PV (2008) A review of cyanobac-terial odorous and bioactive metabolites impacts andmanagement alternatives in aquaculture Aquaculture280 5minus20

Spellerberg IF Fedor PJ (2003) A tribute to Claude Shannon(1916-2001) and a plea for more rigorous use of speciesrichness species diversity and the lsquoShannon-WienerrsquoIndex Glob Ecol Biogeogr 12 177minus179

Spotte S Adams G (1983) Estimation of the allowable upperlimit of ammonia in saline waters Mar Ecol Prog Ser 10 207minus210

Thompson FP Abreu PC Wasielesky W (2002) Importanceof biofilm for water quality and nourishment in intensiveshrimp culture Aquaculture 203 263minus278

85

Editorial responsibility Marianne Holmer Odense Denmark

Submitted May 17 2016 Accepted December 5 2016Proofs received from author(s) January 20 2017


ecosystem (Primavera 1998) Ecological shrimp aqua-culture in mangrove systems has gained environ-mental support because of its tendency to conservethe mangrove forest (Primavera 1998 Fitzgerald2000) by rearing fish without clearing mangrovetrees (Primavera 1998) This integrated approachimplies that the shrimp culture system constantlyintercepts mangrove litter fall which proceeds todecompose under the influence of the microbiotapresent in the biofilm (Benner amp Hodson 1985 Rajen-dran amp Kathiresan 2007) The mangrove trees alsoshade the shrimp culture system from direct sunlighteither partially or completely Since mangrove leaflitter falling into the water eventually sinks to thebottom layers the microalgae accumulating at thewater surface or other suspended particles in thewater column further shield the litter from direct sun-light Sunlight has been demonstrated to acceleratethe rate of decomposition of leaf litter either solely byphotochemical oxidation action (Gallo et al 2009) orin combination with the accelerated extracellularenzymatic action of the associated microbial com -munities (Francoeur et al 2006) Light intensity alsoincreases algae biomass density and compositioncreating a rich energy source for shredders whichenhances the rate of plant litter decomposition bytheir grazing activity (Franken et al 2005)

In an attempt to comply with the ecological needsto reduce aquaculture activities in mangrove sys-tems shrimp culture practices are being pushed further inland However shrimp aquaculture furtherinland lacks the natural services from mangrove-based estuarine ecosystems (Kautsky et al 2001)This has caused an increase in shrimp culture sys-tems that have adopted artificial substrates to mimicnature in promoting proliferation of natural foodsources One example is the use of leaf litter to pro-mote proliferation of natural biota for maintainingwater quality (Bratvold amp Browdy 2001 Otoshi et al2006 Asaduzzaman et al 2008) Hypothetically ifthe artificial substrate used is decomposing man-grove leaf litter the growth and composition of bio-film on the decomposing leaf litter substrate maydepend on the extent of exposure to sunlight andsediment

It is essential that ecological shrimp culture sys-tems whether in mangroves or further inland support phyto- and zoobiota for maintaining waterquality and providing a quality food source for post-larval shrimp (Burford 1997 Bratvold amp Browdy2001 Thompson et al 2002) Thus it is important toassess the potential of decomposing mangrove leaflitter to support biofilm contributing to the natural

diet of post-larval shrimp when the environmentalconditions are modified In this study we hypothe-sized that water quality and the value of the naturalfood provided by the biofilm associated with decom-posing mangrove leaf litter depends on exposure todirect sunlight and sediment Environmental factorsinvestigated included light intensity water trans-parency temperature dissolved oxygen pH salinityand total ammonium nitrogen (TAN) The assemblyof the major taxa of microalgae and invertebratefauna colonizing the decomposing mangrove leaf litter of Rhizophora mucronata was also investigatedOnce isolated and identified the potential applica-tion of the various microalgae and fauna in providinga natural diet to post-larval shrimp Penaeus mon-odon was assessed by comparing with the naturalfood types commonly used in shrimp aquaculture

MATERIALS AND METHODS

Study site

The study was carried out in an integrated man-grove and shrimp culture farm at Mtwapa Creeknorthern coastal region of Kenya (3deg 57rsquo S 39deg 42rsquo E)The project area is characterized by a reforested man -grove forest dominated by Rhizophora mucronata

Experimental set-up

Senescent mangrove leaf litter (hereinafter man-grove leaf litter) which had just turned yellow-brownand dropped from the trees were carefully selectedto include leaf litter of similar surface area The leaflitter was then incubated (see lsquoLitter decompositionrsquofor details) in pond water inoculated into circularmesocosms ie open-top 200 l tanks of 075 m waterdepth at a litter loading density not exceeding 1 glminus1(Hai amp Yakupitiyage 2005) Tank water was slowlyreplenished (to avoid dislodging the biofilm) daily ata rate of 25 The tanks were not stocked withshrimps to prevent grazing on biofilm and were setto provide 4 treatments with each treatment consist-ing of 3 replicates as follows direct sunlight with sed-iment (LS) direct sunlight without sediment (LX)shaded with sediment (DS) and shaded without sedi-ment (DX) The shaded tanks were placed under thecanopy of a thick mangrove forest to prevent expo-sure to direct sunlight The sunlit tanks were placedin an area without mangrove trees with direct expo-sure to sunlight but in close proximity to the shaded

74





(1)









(2)

(3)



Microalgae biomass



100

rsquo lni i1

H P Pi

n

sum= minus sdot=

EHrsquo

lnH

S=

75




Data analysis


RESULTS





Microalgae biomass




76

0

10

20

30

40

50

60

70

80

0 1 3 4 5 7

Per

cent

age

wei

ght

loss


DS DX LS LX















77

0

20

40

60

80

100

120

140

160

180

DS DX LS LX

Treatment

Alg

al b

iom

ass

(chl

a micro

g lndash

1 ) Wk 1 Wk 3 Wk 4 Wk 5 Wk 7







78

0

1000

2000

3000

4000

5000

6000

7000

8000 Week 3

DS

DX

LS

LX

DS

DX

LS

LX

0

1000

2000

3000

4000

5000

6000

DS

Week 1

DX

LS

LX

0

5000

10000

15000

20000

25000 Week 4

0

2000

4000

6000

8000

10000

12000 Week 5

DS

DX

LS

LX

Ab

und

ance

of m

icro

alga

e (c

ells

mlndash

1 )

Microalgae taxa

a

c

b

d

6 x 108

5 x 108

4 x 108

3 x 108

2 x 108

1 x 108

DS

Week 7

D

LS

LX

Microalgae taxa

e

05000

10000150002000025000





DISCUSSION




79

DS DX LS LX































80

0

05

1

15

2

25

3

35

4

0 1 3 4 5 7

Ab

und

ance

of e

pifa

una

(no

cm

ndash2)


DS DX LS LX



DS DX LS LX











81

00005001

0015002

0025003

0035004

0045005

0 1 3 4 5 75

55

6

65

7

75

8

85

0 1 3 4 5 7

26

27

28

29

30

31

32

0 1 3 4 5 7

DS DX

Tem

per

atur

e (deg

C)


LS LX

0

1

2

3

4

5

6

7

8

0 1 3 4 5 7

Dis

solv

ed o

xyg

en (m

g lndash

1)

Tota

l am

mon

ium

nitr

ogen

(mg

lndash1 )

pH

a b

c d











82








CONCLUSION



83



LITERATURE CITED



































84




















85







(1)









(2)

(3)



Microalgae biomass



100

rsquo lni i1

H P Pi

n

sum= minus sdot=

EHrsquo

lnH

S=

75




Data analysis


RESULTS





Microalgae biomass




76

0

10

20

30

40

50

60

70

80

0 1 3 4 5 7

Per

cent

age

wei

ght

loss


DS DX LS LX















77

0

20

40

60

80

100

120

140

160

180

DS DX LS LX

Treatment

Alg

al b

iom

ass

(chl

a micro

g lndash

1 ) Wk 1 Wk 3 Wk 4 Wk 5 Wk 7







78

0

1000

2000

3000

4000

5000

6000

7000

8000 Week 3

DS

DX

LS

LX

DS

DX

LS

LX

0

1000

2000

3000

4000

5000

6000

DS

Week 1

DX

LS

LX

0

5000

10000

15000

20000

25000 Week 4

0

2000

4000

6000

8000

10000

12000 Week 5

DS

DX

LS

LX

Ab

und

ance

of m

icro

alga

e (c

ells

mlndash

1 )

Microalgae taxa

a

c

b

d

6 x 108

5 x 108

4 x 108

3 x 108

2 x 108

1 x 108

DS

Week 7

D

LS

LX

Microalgae taxa

e

05000

10000150002000025000





DISCUSSION




79

DS DX LS LX































80

0

05

1

15

2

25

3

35

4

0 1 3 4 5 7

Ab

und

ance

of e

pifa

una

(no

cm

ndash2)


DS DX LS LX



DS DX LS LX











81

00005001

0015002

0025003

0035004

0045005

0 1 3 4 5 75

55

6

65

7

75

8

85

0 1 3 4 5 7

26

27

28

29

30

31

32

0 1 3 4 5 7

DS DX

Tem

per

atur

e (deg

C)


LS LX

0

1

2

3

4

5

6

7

8

0 1 3 4 5 7

Dis

solv

ed o

xyg

en (m

g lndash

1)

Tota

l am

mon

ium

nitr

ogen

(mg

lndash1 )

pH

a b

c d











82








CONCLUSION



83



LITERATURE CITED



































84




















85






Data analysis


RESULTS





Microalgae biomass




76

0

10

20

30

40

50

60

70

80

0 1 3 4 5 7

Per

cent

age

wei

ght

loss


DS DX LS LX















77

0

20

40

60

80

100

120

140

160

180

DS DX LS LX

Treatment

Alg

al b

iom

ass

(chl

a micro

g lndash

1 ) Wk 1 Wk 3 Wk 4 Wk 5 Wk 7







78

0

1000

2000

3000

4000

5000

6000

7000

8000 Week 3

DS

DX

LS

LX

DS

DX

LS

LX

0

1000

2000

3000

4000

5000

6000

DS

Week 1

DX

LS

LX

0

5000

10000

15000

20000

25000 Week 4

0

2000

4000

6000

8000

10000

12000 Week 5

DS

DX

LS

LX

Ab

und

ance

of m

icro

alga

e (c

ells

mlndash

1 )

Microalgae taxa

a

c

b

d

6 x 108

5 x 108

4 x 108

3 x 108

2 x 108

1 x 108

DS

Week 7

D

LS

LX

Microalgae taxa

e

05000

10000150002000025000





DISCUSSION




79

DS DX LS LX































80

0

05

1

15

2

25

3

35

4

0 1 3 4 5 7

Ab

und

ance

of e

pifa

una

(no

cm

ndash2)


DS DX LS LX



DS DX LS LX











81

00005001

0015002

0025003

0035004

0045005

0 1 3 4 5 75

55

6

65

7

75

8

85

0 1 3 4 5 7

26

27

28

29

30

31

32

0 1 3 4 5 7

DS DX

Tem

per

atur

e (deg

C)


LS LX

0

1

2

3

4

5

6

7

8

0 1 3 4 5 7

Dis

solv

ed o

xyg

en (m

g lndash

1)

Tota

l am

mon

ium

nitr

ogen

(mg

lndash1 )

pH

a b

c d











82








CONCLUSION



83



LITERATURE CITED



































84




















85















77

0

20

40

60

80

100

120

140

160

180

DS DX LS LX

Treatment

Alg

al b

iom

ass

(chl

a micro

g lndash

1 ) Wk 1 Wk 3 Wk 4 Wk 5 Wk 7







78

0

1000

2000

3000

4000

5000

6000

7000

8000 Week 3

DS

DX

LS

LX

DS

DX

LS

LX

0

1000

2000

3000

4000

5000

6000

DS

Week 1

DX

LS

LX

0

5000

10000

15000

20000

25000 Week 4

0

2000

4000

6000

8000

10000

12000 Week 5

DS

DX

LS

LX

Ab

und

ance

of m

icro

alga

e (c

ells

mlndash

1 )

Microalgae taxa

a

c

b

d

6 x 108

5 x 108

4 x 108

3 x 108

2 x 108

1 x 108

DS

Week 7

D

LS

LX

Microalgae taxa

e

05000

10000150002000025000





DISCUSSION




79

DS DX LS LX































80

0

05

1

15

2

25

3

35

4

0 1 3 4 5 7

Ab

und

ance

of e

pifa

una

(no

cm

ndash2)


DS DX LS LX



DS DX LS LX











81

00005001

0015002

0025003

0035004

0045005

0 1 3 4 5 75

55

6

65

7

75

8

85

0 1 3 4 5 7

26

27

28

29

30

31

32

0 1 3 4 5 7

DS DX

Tem

per

atur

e (deg

C)


LS LX

0

1

2

3

4

5

6

7

8

0 1 3 4 5 7

Dis

solv

ed o

xyg

en (m

g lndash

1)

Tota

l am

mon

ium

nitr

ogen

(mg

lndash1 )

pH

a b

c d











82








CONCLUSION



83



LITERATURE CITED



































84




















85







78

0

1000

2000

3000

4000

5000

6000

7000

8000 Week 3

DS

DX

LS

LX

DS

DX

LS

LX

0

1000

2000

3000

4000

5000

6000

DS

Week 1

DX

LS

LX

0

5000

10000

15000

20000

25000 Week 4

0

2000

4000

6000

8000

10000

12000 Week 5

DS

DX

LS

LX

Ab

und

ance

of m

icro

alga

e (c

ells

mlndash

1 )

Microalgae taxa

a

c

b

d

6 x 108

5 x 108

4 x 108

3 x 108

2 x 108

1 x 108

DS

Week 7

D

LS

LX

Microalgae taxa

e

05000

10000150002000025000





DISCUSSION




79

DS DX LS LX































80

0

05

1

15

2

25

3

35

4

0 1 3 4 5 7

Ab

und

ance

of e

pifa

una

(no

cm

ndash2)


DS DX LS LX



DS DX LS LX











81

00005001

0015002

0025003

0035004

0045005

0 1 3 4 5 75

55

6

65

7

75

8

85

0 1 3 4 5 7

26

27

28

29

30

31

32

0 1 3 4 5 7

DS DX

Tem

per

atur

e (deg

C)


LS LX

0

1

2

3

4

5

6

7

8

0 1 3 4 5 7

Dis

solv

ed o

xyg

en (m

g lndash

1)

Tota

l am

mon

ium

nitr

ogen

(mg

lndash1 )

pH

a b

c d











82








CONCLUSION



83



LITERATURE CITED



































84




















85






DISCUSSION




79

DS DX LS LX































80

0

05

1

15

2

25

3

35

4

0 1 3 4 5 7

Ab

und

ance

of e

pifa

una

(no

cm

ndash2)


DS DX LS LX



DS DX LS LX











81

00005001

0015002

0025003

0035004

0045005

0 1 3 4 5 75

55

6

65

7

75

8

85

0 1 3 4 5 7

26

27

28

29

30

31

32

0 1 3 4 5 7

DS DX

Tem

per

atur

e (deg

C)


LS LX

0

1

2

3

4

5

6

7

8

0 1 3 4 5 7

Dis

solv

ed o

xyg

en (m

g lndash

1)

Tota

l am

mon

ium

nitr

ogen

(mg

lndash1 )

pH

a b

c d











82








CONCLUSION



83



LITERATURE CITED



































84




















85









80

0

05

1

15

2

25

3

35

4

0 1 3 4 5 7

Ab

und

ance

of e

pifa

una

(no

cm

ndash2)


DS DX LS LX



DS DX LS LX











81

00005001

0015002

0025003

0035004

0045005

0 1 3 4 5 75

55

6

65

7

75

8

85

0 1 3 4 5 7

26

27

28

29

30

31

32

0 1 3 4 5 7

DS DX

Tem

per

atur

e (deg

C)


LS LX

0

1

2

3

4

5

6

7

8

0 1 3 4 5 7

Dis

solv

ed o

xyg

en (m

g lndash

1)

Tota

l am

mon

ium

nitr

ogen

(mg

lndash1 )

pH

a b

c d











82








CONCLUSION



83



LITERATURE CITED



































84




















85









81

00005001

0015002

0025003

0035004

0045005

0 1 3 4 5 75

55

6

65

7

75

8

85

0 1 3 4 5 7

26

27

28

29

30

31

32

0 1 3 4 5 7

DS DX

Tem

per

atur

e (deg

C)


LS LX

0

1

2

3

4

5

6

7

8

0 1 3 4 5 7

Dis

solv

ed o

xyg

en (m

g lndash

1)

Tota

l am

mon

ium

nitr

ogen

(mg

lndash1 )

pH

a b

c d











82








CONCLUSION



83



LITERATURE CITED



































84




















85











82








CONCLUSION



83



LITERATURE CITED



































84




















85










CONCLUSION



83



LITERATURE CITED



































84




















85





LITERATURE CITED



































84




















85






















85



Sunlight and sediment improve the environment of a litter ...

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