Reviews in Fish Biology and Fisheries 12: 1–31, 2002.© 2003 Kluwer Academic Publishers. Printed in the Netherlands.

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The potential of fish production based on periphyton

Anne A. van Dam1,3, Malcolm C.M. Beveridge2, M. Ekram Azim1 & Marc C.J. Verdegem1

1Fish Culture and Fisheries Group, Department of Animal Sciences, Wageningen University, P.O. Box 338, 6700AH Wageningen, The Netherlands; 2FRS Freshwater Laboratory, Faskally, Pitlochry, Perthshire, Scotland, UKPH16 5LB; 3Current address: Department of Environmental Resources, IHE-Delft, P.O. Box 3015, 2601 DA Delft,The Netherlands (E-mail: avd@ihe.nl; Fax: 31-15-2122921; Phone: 31-15-2151712/2151715)

Received 5 December 2001; accepted 17 October 2002

Contents

Abstract page 1Introduction 2

BackgroundObjectives and scope of the reviewTerminology

Natural and artificial periphyton-based systems 5Natural systems with periphytonBrush-park fisheriesTraditional aquaculture systems in southeast AsiaAquaculture experimentsWater treatment with periphyton

Periphyton productivity 10Development of the periphyton assemblage and species compositionBiomass and productivityEffects of environmental factors

Fish 17Morphological and physiological adaptations to herbivoryPeriphyton ingestion by fishPeriphyton as fish feed: proximate compositionAssimilation efficiency and food conversion ratio

Potential fish production based on periphyton 21Conclusions and recommendations for further research 24

Role of periphyton in aquaculture systemsAbility of fish to utilize periphytonPotential of periphyton-based fish production

Acknowledgements 26References 26

Key words: fish ponds, herbivory, nutrients, periphyton, phytoplankton

Abstract

Periphyton is composed of attached plant and animal organisms embedded in a mucopolysaccharide matrix. Thisreview summarizes research on periphyton-based fish production and on periphyton productivity and ingestion byfish, and explores the potential of developing periphyton-based aquaculture. Important systems with periphytonare brush-parks in lagoon areas and freshwater ponds with maximum extrapolated fish production of 8 t ha−1

y−1 and 7 t ha−1 y−1, respectively. Experiments with a variety of substrates and fish species have been done,sometimes with supplemental feeding. In most experiments, fish production was greater with additional substratescompared to controls without substrates. Colonization of substrates starts with the deposition of organic substances

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and attraction of bacteria, followed by algae and invertebrates. After initial colonization, biomass density increasesto a maximum when competition for light and nutrients prevents a further increase. Often, more than 50% of theperiphyton ash-free dry matter is of non-algal origin. Highest biomass (dm) in natural systems ranges from 0 to700 g m−2 and in aquaculture experiments was around 100 g m−2. Highest productivity was found on bambooin brush-parks (7.9 g C m−2 d−1) and on coral reefs (3 g C m−2 d−1). Inorganic and organic nutrients stimulateperiphyton production. Grazing is the main factor determining periphyton density, while substrate type also affectsproductivity and biomass. Better growth was observed on natural (tree branches and bamboo) than on artificalmaterials (plastic and PVC). Many herbivorous and omnivorous fish can utilize periphyton. Estimates of periphytoningestion by fish range from 0.24 to 112 mg dm (g fish)−1 d−1. Ingestion rates are influenced by temperature, fishsize, fish species and the nutritional quality of the periphyton. Periphyton composition is generally similar to thatof natural feeds in fishponds, with a higher ash content due to the entrapment of sand particles and formationof carbonates. Protein/Metabolizable Energy (P/ME) ratios of periphyton vary from 10 to 40 kJ g−1. Overallassimilation efficiency of fish growing on periphyton was 20–50%. The limited work on feed conversion ratiosresulted in values between 2 and 3. A simple simulation model of periphyton-based fish production estimates fishproduction at approximately 2.8 t ha−1 y−1. Together with other food resources in fishponds, total fish productionwith the current technology level is estimated at about 5 t ha−1 y−1. Because grazing pressure is determined byfish stocking rates, productivity of periphyton is currently the main factor limiting fish production. We concludethat periphyton can increase the productivity and efficiency of aquaculture systems, but more research is neededfor optimization. Areas for attention include the implementation and control of periphyton production (nutrientlevels, substate types and conformations), the ratio of fish to periphyton biomass, options for utilizing periphytonin intensive aquaculture systems and with marine fish, and possibilities for periphyton-based shrimp culture.

Introduction

Background

Fish production through aquaculture is realized ina wide variety of culture systems, from extensiveseasonal ponds to intensive concrete raceways orfloating marine cages. In 1998, 53% of the 30 milliontonnes of finfish, molluscs and shrimp produced inaquaculture were predominantly cultured in extensiveto semi-intensive pond systems (mainly Chinese carpslike Hypophthalmichthys molitrix, Ctenopharyngodonidella, and Aristichthys nobilis, all Cyprinidae; com-mon carp, Cyprinus carpio, Cyprinidae; and Niletilapia, Oreochromis niloticus, Cichlidae). Ponds arealso important in terms of production value, account-ing for some 47% of the total value. Carps and the tigershrimp (Penaeus monodon, Penaeidae) are among themost important commodities (Table 1; FAO, 2001).All pond species feed low in the food chain, mostbeing filter feeders, herbivores, or omnivores.

Production in extensive pond systems is basedon the natural productivity of the pond and solarenergy. In semi-intensive systems, organic and chem-ical fertilizers and supplemental feeds are addedwhereas intensive systems are based predominantlyon high-quality complete feeds. Only 5–15% of the

nitrogen added to the ponds as fertilizer is harvestedas fish biomass (Edwards, 1993; Gross et al., 1999).In feed-driven systems, only 20–30% of the nitrogenin the feed is retained in the fish biomass (Avnimelechand Lacher, 1979; Boyd, 1985; Jiménez-Montealegre,2001). The nutrients that are not harvested as fishbiomass either accumulate in the pond sediment,volatilize, or are discharged into the environment.From economic and environmental points of view,there is a need to examine options to make aquaculturesystems more nutrient efficient.

Generally, three food pathways can be distin-guished in aquaculture systems: (1) direct feeding bythe fish on feeds; (2) the autotrophic pathway, in whichsolar energy is used by primary producers (mainlyalgae) to convert carbon dioxide into organic matterthat can be utilized by fish; and (3) the heterotrophicpathway, in which heterotrophic organisms (bacteria,protozoa, and other invertebrates) decompose organicmatter that can be utilized by the fish (Schroeder,1978). These three pathways are linked throughfluxes of organic and inorganic nutrients. In waste-fed systems, the heterotrophic pathway can be moreimportant than the autotrophic pathway, but stableisotope studies show that a large part of the micro-bial production in ponds is based on algal detritus(Schroeder, 1978; Schroeder et al., 1990). Estimates

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Table 1. Importance of pond systems in world aquaculture production of finfish, molluscs, and shrimp in 1998. Data: FAO (2001). CM =coastal marine system; P = pond; R = raceway; C = floating cage

Predominant

Volume Value production

Common name Scientific name 106 MT % 106 US$ % system

MolluscsPacific cupped oyster Crassostrea gigas 3.44 11.1 3.27 6.9 CM

Japanese carpet shell Ruditapes philippinarum 1.43 4.6 1.86 4.0 CM

Yesso scallop Pecten yessoensis 0.86 2.8 1.18 2.5 CM

Blue mussel Mytilus edulis 0.50 1.6 0.26 0.6 CM

Blood cockle Anadara granosa 0.25 0.8 0.23 0.5 CM

Mediterranean mussel Mytilus galloprovincialis 0.16 0.5 0.11 0.2 CM

ShrimpGiant tiger prawn Penaeus monodon 0.58 1.9 3.86 8.2 P

Whiteleg shrimp Penaeus vannamei 0.19 0.6 1.03 2.2 P

FinfishSilver carp Hypophthalmichthys molitrix 3.31 10.7 3.09 6.6 P

Grass carp Ctenopharyngodon idellus 2.89 9.4 2.66 5.6 P

Common carp Cyprinus carpio 2.47 8.0 2.83 6.0 P

Bighead carp Aristhichthys nobilis 1.58 5.1 1.45 3.1 P

Crucian carp Carassius carassius 1.04 3.4 0.83 1.8 P

Nile tilapia Oreochromis niloticus 0.79 2.6 0.89 1.9 P

Rohu Labeo rohita 0.75 2.4 1.94 4.1 P

Atlantic salmon Salmo salar 0.69 2.2 2.20 4.7 C

Catla Catla catla 0.63 2.0 0.55 1.2 P

Mrigal Cirrhinus mrigala 0.56 1.8 0.47 1.0 P

White Amur bream Parabramis pekinensis 0.45 1.5 0.54 1.1 P

Rainbow trout Oncorhynchus mykiss 0.44 1.4 1.36 2.9 P/R

Milkfish Chanos chanos 0.37 1.2 0.55 1.2 P

Channel catfish Ictalurus punctatus 0.26 0.8 0.42 0.9 P

Japanese eel Anguilla japonica 0.21 0.7 0.82 1.7 P

Mud carp Cirrhinus molitorella 0.16 0.5 0.16 0.3 P

Total this list 24.01 77.8 32.56 69.2

Total ponds (excluding Oncorhynchus mykiss) 16.24 52.6 22.09 46.9

Total world (finfish, molluscs and shrimp) 30.86 100.0 47.08 100.0

of the proportion of the standing stock of phyto-plankton that accumulates as sediment in the bottomrange from 20 to 50% per day (Jiménez-Montealegre,2001). Thus, a large part of the phytoplankton produc-tion is decomposed on the pond bottom and contrib-utes to the accumulation of nutrients in the sediment.Because many fish species are not able to harvestphytoplankton directly from the water column, anextra trophic level is involved in converting phyto-plankton into fish biomass. With an estimated energytransfer efficiency of 10% per trophic level (Paulyand Christensen, 1995), maximum fish yield may beno more than 1% of the energy fixed by the phyto-plankton consumed. Fish yields from extensive and

semi-intensive ponds could be up to ten times higherif primary production could be harvested directly byherbivorous fish.

Whether phytoplankton can be harvested directlyby fish depends largely on the fish species stocked.Although species like silver carp and bighead carpare capable of harvesting microalgae directly, manyspecies used in aquaculture cannot. Even for Niletilapia, generally regarded as a phytoplankton feeder,it seems questionable whether it can derive enoughenergy from exploiting phytoplankton (Dempster etal., 1993, 1995). Phytoplankton has some other dis-advantages. Nighttime respiration by phytoplanktonin ponds may lead to oxygen depletion during the

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early morning hours, causing a risk of fish mortality(Madenjian et al., 1987). Decomposition of sedi-mented phytoplankon may result in toxic decomposi-tion products (ammonia, nitrite) and increased oxygendemand. Phytoplankton blooms are unstable and maycollapse unexpectedly, resulting in a sudden drop indissolved oxygen concentrations and fish mortality(Delincé, 1992).

On the other hand, phytoplankton serves a numberof very important functions in pond aquaculture. Itis a net producer of dissolved oxygen, which isindispensable for fish growth and production (Smithand Piedrahita, 1988; Teichert-Coddington and Green,1993). It is also the most important sink of ammonia-nitrogen, which is excreted by fish and poten-tially toxic (Hargreaves, 1998; Jiménez-Montealegre,2001).

Most truly herbivorous fish species feed on larger,benthic, epilithic or periphytic algae, rather thanon phytoplankton (Horn, 1989). Such algae requiresubstrates for attachment, which are virtually absent infish ponds. In response to the high nutrient levels thatare maintained by pond fertilisation and fish excretion,high-density phytoplankton blooms usually develop.These reduce the light penetration to the pond bottom,thus preventing the development of benthic algal mats.If pond algae could be grown on substrates, morefish species may be able to harvest them, resultingin a more efficient utilization of primary production.Communities of attached algae are generally morestable than phytoplankton and the risk of collapse ismuch lower (Westlake et al., 1980). Some studiessuggest that the production of attached algae per unitwater surface area is higher than of phytoplankton(Wetzel, 1964). Horne and Goldman (1994) statedthat “it is mechanically more efficient to scrape orgraze a two-dimensional layer of periphyton thanto filter algae from a three-dimensional planktonicenvironment”. Considering all these aspects, it mightbe advantageous to develop periphyton-based pondculture.

Objectives and scope of the review

The main objective of this review is to assess thepotential of periphyton-based fish/shrimp productionin aquaculture pond systems on the basis of theavailable literature on periphyton productivity andon periphyton utilization by fish and shrimp. Wepresent an overview of data on natural and culturesystems where fish utilize periphyton and describe the

species composition of periphyton and the architec-ture and functionality of the periphyton assemblage.The productivity of periphyton in natural systems inrelation to environmental factors, substrate types andgrazing are reviewed and the potential productivity inculture sytems is estimated. We also review the qualityof periphyton as a fish feed and examine the morpho-logical and physiological adaptations of fish for util-izing periphyton. Data on periphyton grazing by fishand the effects of grazing on periphyton productivityare discussed. Based on this body of information,we estimate potential periphyton-based fish produc-tion with a simple simulation model. To conclude, weindicate knowledge gaps for developing periphyton-based aquaculture and make recommendations forfurther research.

Terminology

Throughout this paper, we will use the term “peri-phyton” to indicate the assemblage of attached aquaticplant and animal organisms on submerged substrates,including associated non-attached fauna. Several otherterms are used with regard to this assemblage. Themost general terms are “aufwuchs” (often also writtenwith a capitalized A, from the original German wordAufwuchs) and “biofilm”. Some authors prefer totalk about “attached algae”, but this disregards themany other forms that live in periphyton assemblages.Aufwuchs includes all the organisms that are attachedto, or move upon, a submerged substrate, but whichdo not penetrate into it, whereas periphyton refersto the total assemblage of sessile or attached organ-isms on any substrate (Reid and Wood, 1976; Weitzel,1979). The difference is in the unattached organismsthat are often found in association with the periphytonassemblage. Sometimes, the terms “euperiphyton”(immobile organisms attached to the substrate bymeans of rhizoids, gelatinous stalks, or other mechan-isms) and “pseudoperiphyton” or “metaphyton” (free-living, mobile forms that creep among or withinthe periphyton) are used (Weitzel, 1979). The term“biofilm” is preferred in other fields of applica-tion, such as wastewater treatment (Cohen, 2001),drinking water technology (Momba et al., 2000),food processing (Joseph et al., 2001) and dentistry(Rosan and Lamont, 2000) and is used mainly forattached bacteria and protozoa but not algae (O’Tooleet al., 2000). Other terms used to indicate periphytonindicate the substrate on which it grows: epiphyton (on

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plants), epipelon (on sediment), epixylon (on wood),epilithon (on rocks).

Natural and artificial periphyton-based systems

Natural systems with periphyton

Some of the earlier research on periphyton was carriedout in lakes, and it was shown that periphyton canhave an important share (42.4% for the lake studied)in the total annual production, especially in shallowlakes with large littoral zones (Wetzel, 1964). In fiveoligotrophic lakes, periphyton contributed 43–97% ofthe total productivity in the shallow (2–3 m) zone(Loeb et al., 1983). In the littoral zone, periphyton cangrow on rocks and sediments but also as epiphyton onmacrophytes.

In natural, unpolluted streams periphyton densityis highest in the mid-waters, where currents aremoderate and erosion and deposition are balanced.Nutrients, imported from upstream, are absorbed byperiphyton attached in locations with sufficient lightfor photosynthesis, such as rocks or the stream bed.Upstream, the current is stronger, erosional processesand allochthonous inputs are more important, nutrientsare scarce and shredders dominate the food chain. Inthe lower reaches, the currents are slow and depositionprocesses are dominant. In this nutrient-rich environ-ment phytoplankton thrives (Welcomme, 1985). Anexample of this trophic gradient was shown in a studyof a grassland stream in New Zealand, where nitrateconcentrations increased along a downstream gradientwhich was reflected in the species composition andbiomass of the periphyton (Biggs et al., 1998a, b). Thekey feature of periphyton in running water environ-ments is its ability to utilize scarce nutrients in a fixedposition favourable for photosynthesis. Once trapped,nutrients can be recycled within the periphytonassemblage. A model of periphyton biomass withnutrient concentration and water velocity as maindriving variables gave good results when comparedto field data from a river in Argentina (Saravia et al.,1998).

In marine habitats, periphyton is also found inlittoral zones (mangrove forests, estuaries) and oncoral reefs. On coral reefs, the accumulation oforganic material is facilitated by the combination ofa high primary productivity of the attached algae withnitrogen fixing by cyanophytes, the capture of N fromthe surrounding ocean and the recycling of nutri-ents within the reef. This explains how a relatively

high fish biomass can be sustained in oligotrophicwater. An important part of the primary produc-tion is transferred to the coral host in the form oforganic exudates. The main limiting factor is thesurface area available for photosynthesis by attachedprimary producers (Longhurst and Pauly, 1987). Arange of herbivores, including fish, echinoids, andother invertebrates, graze on coral reef algae. Exclu-sion experiments with cages have shown that intensegrazing by fish or sea urchins leads to reefs with aless diverse (in terms of species), lower algal biomassdominated by the smaller turfs and crustose coral-lines than ungrazed reefs (Ogden and Lobel, 1978;Hatcher, 1983; Steneck, 1988). Primary productivityin coral reefs is very high, but values probably dependa lot on the part of the reef where the measure-ment was done (depth, exposure to currents). Algalproductivity is generally believed to increase whenthe standing crop is reduced by grazing, becauseof reduced self-shading, enhanced nutrient exchangewith the water and maintenance of the plants in theexponential growth phase (Ogden and Lobel, 1978;Hatcher, 1983).

Brush-park fisheries

Brush-park fisheries are practiced in a large numberof countries and areas: West Africa, Madagascar,Sri Lanka, Mexico, Bangladesh, Cambodia, China,and Ecuador (Kapetsky, 1981). It is a traditionaltechnology that shares features of both capturefisheries and aquaculture. Research on brush-parkfisheries in the United States was done as early as the1930s (Rodeheffer, 1940; in Pardue, 1973). Currentexamples are the “katha” fishery in Bangladesh (alsocalled “jhag”, “katta” or “jhata”; Wahab and Kibria,1994), “samarahs” in Cambodia (Shankar et al., 1998),and “athkotu” in Sri Lanka (Senanayake, 1981).Kathas are constructed from the branches of treessuch as hizol (Barringtonia sp.), jamboline (Eugeniasp.) or acacia (Streblus sp.). Branches are piled upbetween a number of bamboo poles fixed in the bottomto maintain the structure and delimit the area of thekatha. Kathas are usually built in secondary riversor canals in floodplain lakes. Water hyacinth may beused to cover the katha. The whole structure can be6–9 m long, 2–6 m wide and approximately 1.25 mdeep. Kathas are usually operated for 5–7 monthseach year, during which period they are fished 3–4 times, principally between September and Marchwhen water levels recede and the water becomes cool.

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For fishing, the katha is encircled with a net and allbranches are removed. Fishing the whole katha maytake several days and usually involves 4–5 personsusing scoop nets. Harvests range from 100 to 1000kg, depending on the size of the katha. Similar fish-eries are the “kua” fishery where branches are placedin natural or excavated depressions at the beginningof the rainy season (Wahab and Kibria, 1994) and the“juk” fishery in Kaptai Lake (Ahmed and Hambrey,1999).

Much better studied are the “acadjas” in WestAfrican coastal lagoons. An acadja is an artificialreef made of tree branches (mangrove poles or some-times palm trunks) and installed in water of about1–1.5 m deep. It attracts fish and is colonized byperiphyton which serves as food for the fish. Mostimportant species in the brush-park fisheries of Beninare the blackchin tilapia (Sarotherodon melanotheron,Cichlidae) and bagrid catfish (Chrysichthys nigro-digitatus, Bagridae), but many other species arereported from other countries. After encircling theacadja with a net and removing the branches, the fishare removed, if necessary using traps or baskets. Insome areas, fishing is done by hook and line. Apartfrom attracting fish from outside, fish also reproduceinside the acadja system. Production figures reportedare high, from 4–20 t ha−1 y−1 (Welcomme, 1972;Hem and Avit, 1994).

Because of their profitability, acadjas proliferatedin West-Africa which led to resource use conflicts:competition with navigation for space in the lagoon,competition with capture fisheries for wild fish stock(although it is also claimed that brush-parks may bebeneficial to capture fisheries because fish disperseto adjacent open waters; Welcomme, 1972). Thereare also negative environmental impacts, such asincreased silting in the lagoons due to acceleratedsedimentation around the brush-parks, organic pollu-tion caused by the decaying branches in the water,increased erosion as a result of deforested catchmentareas and a net export of nutrients in areas of intenseacadja harvesting (Durand and Hem, 1996; Weinzierland Vennemann, 2001).

An experiment with the so-called “acadja-enclos”was reported by Hem and Avit (1994). They comparedthree 625 m2 enclosures in the Ebrié lagoon in IvoryCoast (salinity 0–9�): one empty, one with a 100 m2

acadja of Echinochloa pyramidalis (a floating macro-phyte), and one with a 100 m2 traditional acadjamade of the usual tree branches. Fish recruited tothese systems naturally by swimming through the 14-

mm mesh surrounding nets. After 12 months, totalbiomasses of 11.7, 18.2, and 80.5 kg, respectivelywere harvested from the three enclosures. Blackchintilapia was the dominant fish species in the enclosurewith tree branches. Subsequent trials with differentsizes of acadja-enclos (200–2500 m2) yielded onaverage 1.8 t ha−1. Because of the high requirementsfor wood, additional trials with bamboo sticks (10sticks m−2, appoximately 6 cm diameter) were done,leading to average yields of 8.3 t ha−1. The authorsexpect even higher yields if a scheme of successiveselective harvesting would be employed.

Similar experiments in Sri Lanka using differentmangrove and non-mangrove tree species to constructbrush-parks of 4-m diameter resulted in comparableyields (extrapolated: 2.3–12.9 t ha−1 y−1, assuming10 productive months per year and dependingon substrate species) of mainly green chromide(Etroplus suratensis, Cyprinidae), streaked spinefoot(Siganus javus, Siganidae), dory snapper (Lutjanusfulviflammus; Lutjanidae), prawns (Penaeus spp.,Metapenaeus dobsoni and Macrobrachium spp.) andornamental fish (Costa and Wijeyaratne, 1994).

Traditional aquaculture systems in southeast Asia

In the Philippines, Indonesia, and Taiwan, the tradi-tional culture system for milkfish (Chanos chanos,Chanidae) in coastal ponds was based on matsof benthic algae, protozoa, and detritus (in thePhilippines called “lablab”) stimulated by organicfertilization. In Indonesia, mangrove leaves (notablyAvicennia sp.) and twigs were used, whereas inthe Philippines green manures or copra slime wereapplied. Inorganic fertilization was rare. Supple-mentary feeding with rice straw, rice bran, oilcake, wheat starch, water hyacinth, or other macro-phytes was sometimes applied. In the shallow ponds(0.3–0.7 m water depth), a thick mat of algaedeveloped, consisting of cyanobacteria (e.g., Oscilla-toria, Lyngbya, Phormidium, Spirulina, Micro-coleus, Chroococcus, Gomphosphaeria) and diatoms(e.g., Navicula, Pleurosigma, Nastogloia, Stauroneis,Amphiora, Nitzschia and Gyrosigma). Other benthicflora and fauna as well as filamentous green algae werealso ingested. Apart from the target species, about20% of the harvest in Java could consist of prawns(Huet, 1986). Benitez (1984) distinguished betweenfloating lablab that contained 15% protein (ash-freedry matter basis), and benthic lablab with only 6%protein, and reports an observation by fish farmers

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that milkfish consuming filamentous green algae hada slower growth rate than fish eating lablab consistingof unicellular algae and diatoms. Nowadays, manyof these traditional systems have been replaced bydeeper milkfish ponds with higher stocking densityand supplemental feeding.

Another traditional culture system is rice-fishculture. Rice fields harbour lots of phytoplankton andfilamentous higher algae, but studies on rice fieldecology do not reveal much about periphyton (Roger,1996). Not much is known about the natural feedsconsumed by fish in these systems. Periphytic detritalaggregate was the most important item in the foodof Nile tilapia and common carp in rice fields innortheast Thailand (Chapman and Fernando, 1994).Fish feeding on periphyton on rice plants could beso vigorous that the rice plants were observed to beshaking (Chapman, 1991). Similar observations arereported from rice-fish studies in Vietnam (Rothuis etal., 1999) and in Bangladesh (Gupta et al., 1998).

Aquaculture experiments

Pardue (1973) reports two experiments from Alabamawith bluegill (Lepomis macrochirus, Centrarchidae)grown in plastic circular tanks (stocking density 2m−2, 3 m diameter, water volume 5,400 l) equippedwith yellow pine boards with surface areas equivalentto 20, 40, 60, 80 and 100% of the tank surface. Fishproduction increased linearly with increasing surfacearea, and the highest mean yield with 100% surfacearea added was 384 kg ha−1 of bluegill in 180 days(y = 243.34 + 1.408x, in which y = fish yield [kg]and x = added substrate [%]). In a subsequent exper-iment with 40 and 100% additional surface area andthree levels of fertilization, there was no differencebetween the two levels of added surface but a strongeffect of fertilization with the highest yields (mean:430 kg ha−1) achieved under complete fertilization(8-8-2 NPK at 112 kg ha−1, applied 6 times duringthe 180 days culture period). The increase in bluegillproduction was linked to the increase in macroinverte-brates on the substrates, notably Diptera, Hemiptera,Odonata, and Plecoptera.

Cohen et al. (1983) added substrates to 200-m2

ponds for freshwater prawn (Macrobrachium rosen-bergii) in Israel in an attempt to mimic the naturalconditions for prawn growth by increasing the avail-able surface area. The substrates consisted of twohorizontal layers of plastic 2-cm mesh nets withcorrugated plastic pipes attached to them (8-cm

diameter, 15–20 cm long). Each pond was stockedwith 2,000 juvenile prawns (2 g) and 15 commoncarp (100 g). The ponds were fertilized with chickenmanure and a 25% pellet feed was given during thenight. Selective harvesting of large prawns was doneto prevent suppression of growth caused by territorialbehaviour. The total marketable yield from ponds withsubstrates was 2,850 kg ha−1 in six months, against2,500 in ponds without substrates. The average finalweight of the prawns was also higher with substrates(40.3 g versus 35.8 g). There was no difference insurvival.

Another set of experiments with Macrobrachiumrosenbergii was done at Kentucky State University. Ina first experiment, substrates consisting of 3 horizontallevels of plastic mesh sheet, suspended 30 cm apart ina PVC pipe frame were placed in 400 m2 ponds. Thesubstrates increased available surface area by about20%. The substrates increased the yield of prawnsstocked at 0.33 g individual weight and 59,280 indi-viduals ha−1 from 1,060 kg ha−1 (without substrates)to 1,268 kg ha−1 in 106 days. Mean size at harvestwas also bigger (37 g against 30 g without substrates)and the number of mature females increased withsubstrates (Tidwell et al., 1998). In a similar experi-ment with two stocking densities and substrates thatadded 80% of available surface area to the ponds, thesubstrates produced an increase in yield from 1,243to 1,469 kg ha−1 in 95 days (averages for stockingdensities 60,000 and 120,000 ha−1, size at stocking =0.24 g) and a decrease in food conversion ratio from2.9 to 2.4 (Tidwell et al., 1999). In a third experi-ment, the density of the substrates was varied at afixed prawn density of 74,000 ha−1 with a stockingweight of 0.24 g. Substrates consisted of 120 cm wide,7.0×3.5 cm mesh polyethylene panels suspended hori-zontally across the ponds, 30 cm above the bottomwith 30 cm between the layers when multiple layerswere installed. Three treatments were created, corre-sponding to surface area increases of 0, 40 and 80%.There was a positive linear response of yield onsubstrate density: Y (kg/ha) = 1466.3 + 4.4604 X(% increase in surface). Feed conversion ratio wasinversely related to increase in surface area: Y (FCR)= 2.784 − 0.0052 X (% increase in surface). Therewas no significant difference in individual weight atharvest (Tidwell, 2000).

Bender et al. (1989) produced a microbial mat byapplying 32 g dm m−2 of native (Dominican Republic)grass clippings to small (30×14 cm), shallow (4.5 cm)laboratory ponds and inoculating with Oscillatoria sp.

8

The experiment was repeated with larger (13×5 m)concrete ponds and a water depth of 20 cm. Apart fromthe microbial layer growing on the grass substrate, adetrital gelatinous deposit developed on the pond sedi-ment. Weight gain of 0.5–3.5 g Nile tilapia in a 2-weekgrowth trial was higher with the silage-microbial matthan with a commercial catfish feed applied at 3% BWday−1. For the microbial mat to induce fish growth, ithad to be offered in the same pond where it was grown.Microbial mats or detrital material grown in one pondand offered to fish in another pond (either with orwithout sediment) did not induce growth in the fish. Itwas concluded that the integration of the detrital mate-rials with the biomass is crucial for the productivity ofsuch a system. Phillips et al. (1994) obtained signifi-cant differences in final individual weight of Niletilapia between ponds with and without similar micro-bial mats, but no data on mortality and total yield weregiven.

At the Asian Institute of Technology in Bangkok,Shrestha and Knud-Hansen (1994) carried out twoexperiments in concrete tanks (2.5×2×1.1 m) usingvertically suspended corrugated plastic sheets (7.7m2 extra surface area per tank) as substrates withinorganic fertilization (2.1 g N m−2 week−1). Sex-reversed all-male Nile tilapia were stocked (20 gfish−1, 3 fish m−2) for 56 days. Microscopic examina-tion of gut contents and periphyton, as well as obser-vation of feeding behaviour showed that the fish werefeeding on the periphyton. In the first experiment, netfish yields were not significantly different betweentanks with and without substrates (1.05 and 0.88 gm−2 d−1, respectively). Although there was a differ-ence in mean periphyton density between tanks withand without fish (0.78 and 0.93 mg dm cm−2, respec-tively), the difference was not statistically significant.The second experiment compared the plastic substratewith a similar surface area of bamboo poles. Fish yieldwas higher with bamboo poles than with plastic (3.43and 2.51 g m−2 d−1, respectively) and on this occa-sion, there was significantly less periphyton in tankswith fish (0.80 against 1.71 mg dm cm−2 on plasticsheets; bamboo substrates were only tested with fish).From the data on dry matter and ash-free dry matter,it can be seen that the ash content of the periphyton(appr. 50%) was consistently much higher than in thesuspended solids (consisting mainly of phytoplankton;ash appr. 20%), with the exception of periphyton onbamboo (appr. 20%).

Shankar and co-workers (Shankar et al., 1998;Ramesh et al., 1999; Umesh et al., 1999) used

bio-degradable substrates to stimulate fish produc-tion. In two preliminary experiments, productionof common carp, Mozambique tilapia (Oreochromismossambicus, Cichlidae) and rohu (Labeo rohita,Cyprinidae) in concrete tanks was 45–50% higherwith sugarcane bagasse as a substrate, compared tocontrol tanks without substrates. A subsequent biggertrial compared dried sugarcane bagasse, paddy straw,and dried water hyacinth (Eichhornia sp.) leaves,suspended as 60–90 cm bundles in 25 m2 concretetanks with soil bottoms. Substrate density was 12.5kg tank−1 (as the authors stressed the biodegradabilityof the substrates, substrate density was expressed asmass per surface area) and the tanks were fertilizedwith cow manure and urea. A mixture of common carp(2.1 g) and rohu (1.5 g) were stocked at 13 and 12 pertank, respectively. The experiment lasted 133 days andon day 70, 7.5 kg of fresh substrates were suspended.Both rohu and common carp grew best in the treat-ment with sugarcane bagasse, yielding 3,088 g tank−1,against 2,873, 2,403 and 1,865 g with paddy straw,Eichhornia and in tanks without substrate, respec-tively. In all substrate treatments, fish survival onaverage was higher than in the control (85.7–93.7%,versus 81.3%). The increased fish production could, inthe absence of major differences in dissolved oxygenand ammonia concentrations, be attributed to theperiphyton on the substrates, as shown by total platecounts of bacteria in the water and on the substrates,and by phytoplankton and zooplankton enumeration.The superior fish production with bagasse was attrib-uted to its higher fibre content and surface area,favouring better bacterial growth and subsequent fishproduction than the other two substrates. Zooplanktondensity in the water of the bagasse treatment washigher than in the other treatments. The authorsconcluded that biodegradable substrates led to betterresults than less degradable substrates like bamboo ornon-biodegradable substrates like PVC and plastic.

Bratvold and Browdy (2001) studied changes inwater quality and microbial community activity dueto AquaMatsTM substrates (3.4 m2 per m3 tank)added to polyethylene tanks stocked with Litopen-aeus vannamei postlarvae. Shrimps were fed witha commercial feed. Compared to tanks with onlysand sediment or tanks without sediment, tankswith substrates and sand sediment had a higher pHand higher total photosynthesis, lower abundance ofpelagic bacteria and phytoplankton, lower turbidity,lower ammonia and orthophosphate and higher nitrifi-cation. Shrimp production was significantly higher

9

(1.69 vs. 0.98–1.07 kg m−2 in 100 days) andfood conversion ratio (feed given/shrimp produced)was significantly lower (1.5 vs. 1.9–2.1) in thetanks with substrates compared to the tanks withoutsubstrates.

Keshavanath et al. (2001b) reported an experi-ment with different types of substrates for enhancingthe production of mahseer (Tor khudree, Cyprinidae).Bamboo poles, PVC pipes and sugarcane bagassesubstrates were placed in 25 m2 concrete tanks withmud bottoms and fingerlings of about 3 g were stockedat densities of 1, 1.5, and 2 fish per m2. After 90 days,the highest net production with bamboo substratewas 447 kg ha−1 at the highest fish density, against399 kg ha−1 with the PVC pipes. In the bagassetreatment, all fish died due to low oxygen concen-trations. In subsequent experiments (Keshavanath etal., 2002) using the same tank systems, the effectsof periphyton, supplemental feeding and their combi-nation were investigated using mahseer (3.5 g) orthe fringed lipped peninsula carp (Labeo fimbriatus,Cyprinidae) (0.73 g), both stocked at 25 per tank.Two densities of bamboo poles (98 or 196 poles per25 m2) were compared with tanks without substrates.Periphyton alone and feeding alone led to compa-rable fish yields that were significantly higher (by30–75%) than the yields obtained without periphytonor feed. There was a significant effect of substratedensity on fish survival in both species. The combi-nation of periphyton and feeding resulted in evenhigher yield increases (54–87%). The higher substratedensity improved yield only slightly without feedingand not at all with feeding, suggesting that at thefish stocking density used the carrying capacity ofthe periphyton was never exceeded. A similar exper-iment with red tilapia (Oreochromis mossambicus ×O. niloticus hybrid) gave similar results, with evenmore pronounced differences between tanks with andwithout substrates. Highest tilapia yields were 1,834g per 25 m2 without, and 2,142 g per 25 m2 withfeeding in 75 days (Keshavanath, unpublished results).Sugarcane bagasse was again used as a substrate ina farm trial. At densities of 156 bagasse bundles(about 28 kg) per 100 m2, total fish yield of catla(Catla catla, Cyprinidae), rohu, and common carp was13,104 and 14,842 g per 100 m2 in 180 days withoutand with feed, respectively, compared to 8,076 g in thecontrol without feed or periphyton (Keshavanath et al.,2001a).

At the Bangladesh Agricultural University inMymensingh, Bangladesh, research on periphyton

started with a series of monoculture experiments inwhich the performance of several fish species withperiphyton was assessed. An experiment in six 75m2 ponds compared the production of 2.1 g orange-fin labeo (Morulius calbasu, Cyprinidae) stocked at1 m−2 with and without substrates made of “kanchi”(bamboo trimmings). While no differences in waterquality were observed, survival (87–90% versus 72–77%) and fish growth were higher with substratesthan without, resulting in a net yield of 713 kg ha−1

versus 399 kg ha−1 in 120 days. These relativelylow yields could be explained by the sub-optimalwater temperatures that prevailed during the experi-ment (23.6–32.7 ◦C) (Wahab et al., 1999). Rohu (10 gat 1 m−2) and kuria labeo (Labeo gonius, Cyprinidae;4 g at 1 m−2) were then grown with bamboo substratesat 9 poles m−2 (but leaving the pond perimeter free;total substrate area was about 75 m2). Net rohu yieldwith substrate was significantly greater (1,901 kg ha−1

in 120 days) than without substrate (1,073 kg ha−1).For kuria labeo (separate experiment), yields were notsignificantly different (794 and 788 kg ha−1, respec-tively, in 120 days). The kuria labeo were neverobserved to feed actively on the periphyton whereasrohu could be clearly seen eating the periphyton (Azimet al., 2001a). It was concluded that rohu and orange-fin labeo are more suitable candidates for periphyton-based aquaculture than kuria labeo.

To utilize the other food sources in the pond(plankton, detritus) as well, polyculture of rohu andcatla was investigated. With different stocking ratiosand bamboo substrate, the growth and total yields fromany combination of rohu and catla were higher by 3–40% (individual weight) and 50–300% (total yield),than those from rohu or catla in monoculture. Thecombination of 60% rohu and 40% catla was optimal,resulting in a net yield of 586 kg ha−1 70 d−1 (Azimet al., 2002a). Using this stocking ratio, another trialwith and without bamboo substrates was carried out toverify the effect of substrates with this species combi-nation. Survival, growth rate, individual weight atharvest as well as net yield of both rohu and catla,were significantly higher in the ponds with bamboosubstrates. In ponds with substrate, not only thenet yield of periphyton-feeding rohu was higher (by160%), but also that of surface-feeding catla (220%).The combined net production of the two species inponds with substrates was 180% higher (1,652 kgha−1 90 d−1 on average) than that of control ponds(577 kg ha−1 90 d−1). In the same experiment, it wasfound that the addition of 15% orange-fin labeo to the

10

optimum mix of catla and rohu further increased totalproduction by 40% (2,306 kg ha−1 90 d−1) (Azim etal., 2001b).

Water treatment with periphyton

Some investigators have attempted to use fish andperiphyton for removing nutrients from wastewater.The nutrients acccumulated in the periphyton areremoved by harvesting the periphyton. This can bedone manually or mechanically, but fish can also beused. Drenner et al. (1997) used Mozambique tilapiaand central stoneroller (Campostoma anomalum,Cyprinidae) for harvesting periphyton grown incircular tanks fed with mock wastewater treatmentplant effluent. Maximum removal rates were 48.4mg total phosphorous (removed in sediments and fishbiomass) per m−2 water surface per day.

Periphyton productivity

Development of the periphyton assemblage andspecies composition

Development of a periphyton layer on a clean surfacegenerally starts with the deposition by electrostaticforces of a coating of dissolved organic substances(mainly mucopolysaccharides), to which bacteria areattracted by hydrophobic reactions (Hoagland et al.,1982; Cowling et al., 2000). The presence of free-floating organic micro-particles in eutrophic watersstimulates this process. Bacteria actively attach usingmucilaginous strands. This can take a week, but insome studies this was observed within days and evenwithin a matter of hours. It is not clear whetherbacterial colonization is a prerequisite for subsequentattachment of other organisms, or what the exactrole of the bacteria is in this process (Hoaglandet al., 1982). In the days that follow, algae startto grow. Low-profile diatoms appear first, followedby small pennate diatoms, short-stalked and longerstalked species and then by diatoms with rosettesand mucilage pads. In the final stages of develop-ment, species of green algae with upright filamentsor long strands can grow (Hoagland et al., 1982;Horne and Goldman, 1994). On plants, the periphytoncommunity is attached on gelatinous stalks of algaland bacterial mucus interspersed with deposits ofcalcium carbonate (Wetzel, 1975).

In their study with grass silage, Bender etal. (1989), using colony counts of nitrogen-fixingbacteria, microscopic identification of species andcharacterization of chemotactic response on agarplates, showed that a chemotactic response to the lacticand acetic acid in the silage from bacteria in the sedi-ments was the first step in the colonization of the grasssubstrates. The bacteria bloomed in the water andproduced slimy exudates that annealed the mirobesto the silage after which cyanobacteria invaded thesubstrates and caused a further increase in biomass.Using microprobes, it was shown that within the mat,different heterogeneous micro-environments existedwith oxic and anoxic zones.

Periphyton organisms have various ways ofattaching to the substrate: stalks with sticky ends(e.g. ciliates), sticky capsules (bacteria and bluegreenalgae), cushions of filaments (seaweeds, algae andaquatic mosses), muscular suction pads (snails),glue (barnacles) or simply clinging to the substrate(e.g., insect larvae). Attachment to sediment canbe achieved by rooting (especially higher plants),rhizoids (seaweeds on corals), and with a muscularfoot (clams) (Reid and Wood, 1976).

During the development of the periphyton layer,conditions for growth of the various algal specieschange drastically. As the density of organismsincreases, there is more competition for substratesurface area and this affects the composition of theperiphyton community. The organisms also competefor carbon dioxide, nutrients and light. This explainsthe development of the periphyton layer away from thesubstrate, resulting in something that can be comparedto the canopy of a terrestrial forest (Hoagland etal., 1982; Figure 1). Another strategy for ensuringoptimal nutrient and light conditions is shown bypennate diatom and cyanobacterial cells that can movearound the substrate. They “glide” by excreting apolysaccharide mucilage that sticks to the substrate(diatoms) or by using contractile fibrils in their cellwalls (cyanobacteria). In this way, they can moveaway from areas where light or nutrients have becomelimiting (Horne and Goldman, 1994). It is prob-ably also a way to escape being covered by sedi-ment deposits (Hutchinson, 1975). Some diatomsremain at the base of the periphyton assemblagethroughout its development, withstanding extremelylow light conditions, while other species move aroundthe periphyton layer looking for the best conditionsavailable (Johnson et al., 1997).

11

Figure 1. Range of vertical structure in the periphyton community. Drawn to scale, ×400. From: Hoagland et al., 1982. Reproduced withpermission, Botanical Society of America.

Coral reef algae can be classified as “algalturf” (1–10 mm), macroalgae or “fleshy algal pave-ment” (larger than 10 mm) and “crustose algae”(encrusting noncalcified algae or calcareous, crustosecorallines) (Steneck, 1988). The epilithic algalcommunity (EAC) of coral reefs generally consistsof a mixture of turf and crustose algae (Klumppand McKinnon, 1992). Species diversity within theperiphyton assemblage can be high. Planas et al.(1989) found on average 41 different species inperiphyton on ceramic tiles. Wahab et al. (1999)encountered 12 genera of Bacillariophyceae, 25 ofChlorophycaea, 10 of Cyanophyceae, 4 of Eugleno-

phyceae, 1 of Rhodophyceae and 5 of zooplankton inperiphyton, as well as a variety of macrobenthic organ-isms, notably chironomid larvae on scrap bamboosubstrates in fishponds in Bangladesh. Lam and Lei(1999) found 81 algal species in periphyton on glassslides in the Lam Tsuen River, Hong Kong. Konan-Brou and Guiral (1994) found 24 species of algae inthe periphyton community on bamboo substrates inacadjas in Cote d’Ivoire.

Often, one or a few species of algae dominate theassemblage. The EAC of coral reefs is often domi-nated by filamentous Chlorophytes and Rhodophytes(Klumpp and McKinnon, 1992). On plastic substrates

12

in tilapia cages in Bangladesh, filamentous Chloro-phyceae and Myxophyceae dominated the periphytonbefore fish stocking, whereas after stocking of thefish diatoms became more important. Diatoms couldbe attached directly to the substrate but were alsofound as epiphytes on larger filamentous algae. Inaddition, freshwater oligochaetes, Protozoa, Rotifera,and coelenterate Hydrozoa were observed (Huchetteet al., 2000). Dominant species in the periphyton ofthe acadjas were the filamentous algae Rhizocloniumriparium (Chlorophyceae) and Lyngbia (Cyano-bacteria) in the surface layers, and Audouinelladaviesii (Rhodophyceae) in the deeper layers. Diatomsof the genera Nitzschia and Melosira grew on thefilamentous algae (Guiral et al., 1993; Konan-Brouand Guiral, 1994). In eutrophic Lake Valencia,Venezuela, the basis of the “periphytic detritalaggregate” (PDA) growing on macrophytes (Potamo-geton sp.) consisted of filamentous cyanophytes,which were also the dominant phytoplankton in thelake. Diatoms, bacteria, and amorphous detritus werethe main components of the periphyton attached to thecyanophyte matrix (Bowen, 1979).

The composition, biomass, and productivity of theperiphyton community vary with season, year, loca-tion, and grazing pressure. On coral reefs, the structureof the community is often different depending onwhether it is located on the reef flats, the inner orouter shelf, windward or leeward side, and shallowor deep parts and slopes (Klumpp and McKinnon,1992). Within a single water body, there can bea considerable overlap in species between phyto-plankton and peripyton (Havens et al., 1996). In fish-ponds in Bangladesh, 23 of the 39 genera found in theperiphyton were common to the phytoplankton (Azimet al., 2001a).

The algal contribution to the dry matter can beestimated from the ratio of ash free dry matter topigment, called the autotrophic index (AI, mg ash freedry matter/mg chlorophyll a on a given surface area;APHA, 1998). Huchette et al. (2000) reported that AIswere between 150 and 300 in ungrazed conditions andremained stable around 300 when grazed. Azim et al.(2002b) reported AI values ranging from 189 to 346 infreshwater fertilized ponds without fish, depending onsubstrate. The values decreased with time, indicatingthat ash-free dry matter of non-algal origin dominatedin young periphyton. In general, 1 mg chlorophyll a isequivalent to 65–85 mg algae (Dempster et al., 1993;APHA, 1998), so more than 50% of the periphytonash-free dry matter is not of algal origin.

Biomass and productivity

Table 2 gives an overview of the standing crop ofperiphyton found on different substrates in variouskinds of natural and culture systems. Because ofthe wide variation in methods used, environments,and species composition it is difficult to comparethe biomass figures directly. The biomasses foundin natural systems (streams, lakes, and coral reefs)can be greater than those found in brush-parks andculture systems (tanks and ponds). In a comparison ofperiphyton biomass in a wide range of natural systems,biomasses of up to 2350 mg m−2 chlorophyll a werereported (Westlake et al., 1980). The main reasons forthis are probably the higher fish densities and asso-ciated grazing intensity in culture systems, althoughbiomasses in culture systems without fish were stilllower than those in, for example, coral reefs. Likely,there is a strong effect of the algal species composi-tion, with especially high biomasses attained by thefleshy macroalgae that make up the algal assemblageon lightly grazed coral reefs. Furthermore, substratetype has a strong effect on the density of periphyton, asshown by the differences between different substratetypes in experiments in India and Bangladesh (Azimet al., 2002b; Keshavanath et al., 2001b).

Table 3 shows data on periphyton productivity.Again, comparisons are difficult, but the productivityof the acadja systems was the highest (7.9 g Cm−2 d−1). In this study, not only area-specific butalso chlorophyll-specific productivity was higher inperiphyton than in phytoplankton (highest contrastmeasured on one day was 22.5 and 5.9 mg C (mgchla)−1 h−1 for periphyton and phytoplankton, respec-tively) (Guiral et al., 1993). Coral reefs are alsovery productive, with net productivity of up to 3g m−2 d−1 (see Table 3). Productivity measure-ments were much lower in temperate lakes. An inter-mediate estimate (±1.7 g C m−2 d−1) was made ina pond in Bangladesh (Azim et al., 2002b), basedon the periphyton biomass after the first two weeksof colonization on clean bamboo substrates. Theother measurements were made using UV-transparentrespiration chambers.

Effects of environmental factors

NutrientsInorganic nutrients can have a strong effect onperiphyton biomass, as shown by numerous enrich-ment studies in both natural and artificial systems

13

Tabl

e2.

Peri

phyt

onbi

omas

s(s

tand

ing

crop

)in

vari

ous

natu

ral

and

artifi

cial

syst

ems.

Bio

mas

sis

expr

esse

das

gas

h-fr

eedr

ym

atte

r(A

FDM

),or

asm

gch

loro

phyl

la

(Chl

-a)

per

m2

ofsu

bstr

ate

area

Syst

emty

peSu

bstr

ate

type

AFD

MC

hl-a

Rem

arks

Ref

eren

ce

(gm

−2)

(mg

m−2

)

Stre

am/r

iver

Nat

ural

ston

es0–

48.4

Gla

cial

stre

am,A

ntar

ctic

aIz

agui

rre

and

Piza

rro,

1998

Cel

lulo

se-a

ceta

te0.

8–20

7.1–

46A

maz

onri

ver,

depe

ndin

gon

zone

Putz

,199

7

Woo

d7–

3313

–42

Bill

abon

g(l

entic

syst

em),

onE

ucal

yptu

sca

mal

dule

nsis

Scho

lzan

dB

oon,

1993

Lak

e/re

serv

oir

Sedi

men

t76

.8–3

97N

utri

ent-

poor

vs.e

nric

hed

site

s,N

orth

ern

Oza

rks,

Mis

sour

i(U

SA)

Loh

man

etal

.,19

92

X-r

aypl

ates

0.4–

33.1

Olig

otro

phic

lake

with

trou

tfar

m,P

atag

onia

,Arg

entin

a.H

ighe

rB

affic

oan

dPe

droz

o,19

96

valu

esne

arfis

hfa

rm

Nat

ural

ston

es3–

502–

100

10la

kes

ofva

ryin

gtr

ophy

,Que

bec,

Can

ada

Cat

tane

o,19

87

Dea

dre

edst

ems

5–50

Olig

o-m

esot

roph

icla

ke,N

ethe

rlan

ds.L

owbi

omas

sin

sum

mer

,M

eule

man

san

dH

eini

s,19

83

high

inw

inte

r

Cor

alre

efC

oral

rock

132–

683

Dep

endi

ngon

alga

ltyp

e,B

onai

re(N

ethe

rlan

dsA

ntill

es)

Bru

ggem

an,1

995

Cor

alro

ck40

0–70

060

0–12

00M

acro

alga

e,G

reat

Bar

rier

Ree

fH

atch

eran

dL

arku

m,1

983

Cor

alro

ck16

0–24

0bM

ainl

ycr

usto

sean

dtu

rfal

gae,

Gre

atB

arri

erR

eef.

Klu

mpp

and

McK

inno

n,19

92

Bru

sh-p

ark

Bam

boo

0.2–

382.

5–15

4D

epen

ding

onde

pth

and

loca

tion

Ebr

ieL

agoo

n,C

ote

Kon

an-B

rou

and

Gui

ral,

1994

d’Iv

oire

Bam

boo

7.2–

254.

1–16

7aD

epen

ding

onde

pth

and

salin

ity/s

easo

n,E

brie

Lag

oon,

Cot

ed’

Ivoi

reA

rfiet

al.,

1997

Cul

ture

syst

emPl

astic

shee

ts3.

3–9.

55

m2

conc

rete

tank

s,A

sian

Inst

itute

ofTe

chno

logy

,Ban

gkok

Shre

stha

and

Knu

d-H

anse

n,19

94

Bam

boo,

kanc

hi,h

izol

19–1

1312

5–22

875

m2

fishp

onds

Mym

ensi

ngh,

Ban

glad

esh

Azi

met

al.,

2002

b

Bag

asse

,bam

boo,

PVC

7–18

60–3

00a

25m

2co

ncre

teta

nks,

Man

galo

re,I

ndia

.Hig

her

valu

esw

ithou

tfish

Kes

hava

nath

etal

.,20

01b,

2002

Wat

ertr

eatm

ent

Gla

ss,s

and

disk

,70

–100

Bio

film

onbi

olog

ical

reac

tors

with

laye

rof

subs

trat

e,va

lue

Api

lane

zet

al.,

1998

syst

emA

ctiv

eca

rbon

depe

ndin

gon

subs

trat

e

a Tota

lpig

men

t(ch

loro

phyl

la+

pheo

phyt

on).

bC

onve

rted

from

gca

rbon

byas

sum

ing

48%

Cin

afdm

.

14

Table 3. Net productivity of periphyton in various natural and culture systems. Productivity is expressed as g C m−2 d−1 and was convertedto these units assuming 50% C in dm and 12 hours active feeding per day

System type Substrate type Net productivity Remarks Reference

(g C m−2 d−1)

River Cellulose-acetate 0.082–1.04 Amazon river, depending on zone Putz, 1997

Lake 0.02–0.20 Littoral zone, 5 oligotrophic lakes, California/Nevada Loeb et al., 1983

USA

Reed stems 0.14–0.72 Littoral zone, oligo-mesotrophic lake, Netherlands Meulemans and Heinis, 1983

Debris and plants 0.73 Whole-lake estimate, large shallow lake Wetzel, 1964

Coral reef Coral rock 0.6–1.1 Great Barrier Reef. Lower on slopes, higher on flats Klumpp and McKinnon, 1992

Coral rock 1.79–2.15 Great Barrier Reef. Damselfish territories Klumpp and Polunin, 1989

Coral rock 1.98–2.00 Papua New Guinea, turf algae Polunin, 1988

Coral rock 1.8–3.1 Virgin Islands Carpenter, 1986

Coral rock 2.16–4.80 Several Pacific benthic reef communities Marsh, 1976

Coral rock 0.64–2.00 Fringing coral reef, Bonaire Van Rooij et al., 1998

Brush-park Bamboo 7.9 Guiral et al., 1993

Fishpond Bamboo 1.7 Estimated from increase in total biomass on clean Azim et al., 2002b

substrates

Fishpond Grass silage 7.5 Bender et al., 1989

(e.g., Aizaki and Sakamoto, 1988; Lohman et al.,1992; Ghosh and Gaur, 1994). Periphyton biomassand productivity can thus be used as indicators ofeutrophication in natural waters (e.g., Mattila andRaeisaenen, 1998). In a fertilization experiment inponds, a quadratic relationship between periphytonbiomass and fertilization level was established, witha maximum periphyton biomass (mean biomass over6 weeks) of 3.3 mg cm−2 dry matter realized withfertilization rates of 4,500, 150, and 150 kg ha−1

of cow manure, urea, and TSP, respectively (equiva-lent to 1.5 times the standard rate for fishpondsin Bangladesh). Phytoplankton biomass increasedlinearly with increasing fertilization rate up to 2 timesthe standard rate (Azim et al., 2001c).

Investigative studies of nutrient limitation showmixed results. In most freshwater studies, phos-phorous was identified as the limiting nutrient (e.g.,Ghosh and Gaur, 1994; Vymazal et al., 1994), butnitrogen (Barnese and Schelske, 1994), carbon(Sherman and Fairchild, 1989) and silica can also belimiting, depending on the algal species and on otherenvironmental factors such as hardness and acidity.High Si:P and N:P ratios favoured diatoms, and lowN:P and Si:P ratios favoured cyanophytes in a reser-voir in Patagonia (Baffico and Pedroso, 1996). Simi-larly, high Si:N or Si:P ratios favoured diatoms, low

N:P ratios favoured cyanophytes and high N:P ratiosfavoured chlorophytes in periphyton of the Baltic Sea(Sommer, 1996).

Whether or not nutrient enrichment stimulatesperiphyton productivity also depends on the type ofsubstrate. Benthic periphyton has an advantage overphytoplankton because it is closer to the nutrient-richsediment and the interstitial pore water, or in the caseof epiphytes to macrophyte nutrients. In a series ofwhole-lake experiments, it was shown that periphytonon sediments utilized the nutrients in the sedimentpore water and therefore, responded much less toenrichment than periphyton growing on wood in thesame lake (Blumenshine et al., 1997). Epilithic algaeare more likely to become nutrient-limited becausethey have to absorb nutrients from the water (Sand-Jensen and Borum, 1991).

Lower nutrient concentrations do not necessarilymean lower biomass and productivity. In an experi-ment with an artificially created upstream-downstreamgradient, there were large differences in nutrientconcentrations between upstream and downstreamparts of the stream, but differences in periphytonbiomass were poorly related to gradient. More nutrientrecycling took place downstream (Mulholland et al.,1995). Similarly, in a modelling study of nutrientenrichment in seven New Zealand streams, biomass

15

levels in the area studied were lower than predictedusing the calibrated model. This was ascribed todifferences in other factors such as increased grazing,shading, or differences in substrate characteristics(Welch et al., 1992).

Apart from the impact of enrichment onperiphyton, periphyton has an effect on the nutrientconcentration in the overlying water. Periphytonlowered the phosphorous of the overlying water(Hansson, 1989; Bratvold and Browdy, 2001) andsediment (Hansson, 1989). By lowering the nutrientconcentration of the water, periphyton can affectthe growth of the phytoplankton, as was shownin a study in Swedish lakes (Hansson, 1990). Inaquaculture experiments with periphyton, ammoniaconcentrations in tanks with periphyton were lowerthan in control tanks, indicating a stimulating effectof the periphyton on nitrification (Langis et al.,1988; Ramesh et al., 1999; Bratvold and Browdy,2001).

Organic nutrients are also important for the hetero-trophic components of the periphyton. The activityof ectoenzymes in a Mediterranean river was higherduring periods of high dissolved organic matterconcentrations (Romaní and Sabater, 2000). Suchenzymes are retained in the periphyton layer bythe extracellular polysaccharide matrix (Thompsonand Sinsabaugh, 2000). Similarly, the organic loadcaused by decomposing salmon carcasses led toincreased stream periphyton growth (Fisher-Woldand Hershey, 1999). Pulses of highly availablecarbon created a change in the composition ofthe biofilm from chemoautotrophic to heterotrophicorganisms, and biofilms adapted their metabolism tothe prevailing environmental conditions (Battin et al.,1999; Butturini et al., 2000). The algae from theperiphyton are important suppliers of organic matter tothe heterotrophs. In river biofilms, maximum enzymeactivity was seen with an algal biomas that wastwo to three times as high as the bacterial biomass.Bacteria are likely to utilize the algal exudates andlysis products, as well as photosynthetically producedoxygen, whereas algae utilize the inorganic carbonproduced by the heterotrophs (Kuehl et al., 1996;Romaní and Sabater, 2000). Organic matter qualityaffects the rate at which it is processed, as shown bydifferences in turnover times between two rivers withdifferent sources of organic matter (Romaní, 2000).Dissolved organic matter may play a role in deter-mining the structure of the periphyton. Periphytoncommunities treated experimentally with dissolved

organic carbon contained less mucilage than untreatedcontrols (Wetzel et al., 1997).

GrazingGrazing is the most important determinant ofperiphyton biomass. On coral reefs, algal communitiescan be grazed down completely by fish or echinoids(e.g. Hixon and Brostoff, 1981; Hay, 1981). Exclusionand removal experiments on coral reefs showed thatalgal standing crop could increase 1.5 to 15-fold whengrazers were excluded (Hatcher and Larkum, 1983).Not all components of the periphyton assemblage areequally susceptible to grazing. Diatoms belonging tothe overstory of the periphyton layer were removedby grazing snails while more prostrate basal cells(e.g., Stigeoclonium sp.) were unaffected by grazing(McCormick and Stevenson, 1991; Hill et al., 1992;Steinman et al., 1992). Generally, periphyton algaldiversity is lower when grazed (Jacoby, 1987; Horn,1989; Swamikannu and Hoagland, 1989).

Most studies of grazing have been done withinvertebrate grazers such as snails and insect larvaewhile studies with fish are much less common.Huchette et al. (2000) compared the species composi-tion of grazed (four weeks) and ungrazed periphytoncommunities on plastic substrates in tilapia cages in aBangladesh river. Four weeks after stocking with fish,the filamentous algae were reduced to short colonylengths and other species such as Ankistrodesmusbecame more important in the periphyton. Grazingalso resulted in a size reduction of epiphytic diatoms.Grazing tilapia preferred the larger-sized diatoms(Melosira spp., Cycotella spp.) as shown by a largerproportion of these species in the stomachs. The fishwere not grazing on the periphyton only, as shownby a higher diversity of diatom species in the fishstomachs than in the periphyton and the presence ofnanoplankton in the fish stomachs. Grazing resulted ina much lower standing biomass of periphyton than inthe ungrazed treatment. Similarly, periphyton biomasswas 60% lower on nets in cages stocked with Karibatilapia (Oreochromis mortimeri, Cichlidae), redbreasttilapia (Tilapia rendalli, Cichlidae) and Nile tilapiathan in unstocked cages (Norberg, 1999). However,in a study with redear sunfish (Lepomis microlophus,Centrarchidae) and snails, it was shown that thefish had a positive effect on periphyton biomass byreducing the grazing on the periphyton by snails.Nutrient concentrations in the water were also higherwith fish, but this did not affect the periphyton much(McCollum et al., 1998). In streams in the Ozark

16

Mountains (Missouri, USA), stones were coveredby cyanobacteria (Calothrix sp.) when exposed tograzing by fish and invertebrates. Once protected fromgrazing, diatoms would overgrow the cyanobacteriawithin four to ten days. Grazing minnows could stripthe diatom layer in a matter of minutes, after whichregeneration of the cyanobacteria happened in 11 days(Power et al., 1988). Predators of grazing fish can alsoaffect the density of periphyton layers, as shown bya study in streams in Panama where bands of highperiphyton biomass occurred in the top water layer(<20 cm deep) which is avoided by the fish for fearof predation (Power et al., 1989).

Although grazing diminishes biomass, algalproductivity is enhanced by grazing because self-shading and competition for nutrients are reduced(Hatcher, 1983; Carpenter, 1986; McCormick andStevenson, 1989). Grazing removes dead or senescentalgae and keeps the algal assemblage in a productive,early-successional stage. Coral reef algae grazed bysea urchins had a lower biomass than ungrazed algaebut production was not reduced, indicating a positiveeffect of grazing on the productivity of the algae(Carpenter, 1986). Norberg (1999), using transparentincubation chambers, measured a fourfold increase inperiphyton specific productivity in grazed periphytoncompared to ungrazed controls. Apart from the directeffect of reduced competition, there is also theindirect effect of excreted nutrients that can benefitthe periphyton. Rudd (Scardinius erythrophthalmus,Cyprinidae) grazing on macrophytes increased thephosphorous content in water and periphyton, asshown by a 33PO4 tracer experiment (Hansson et al.,1987).

Some algae have developed defenses againstgrazing. Seaweeds have chemical defenses againstgrazing (chemical compounds that determine palata-bility for certain species of grazers) that may bechanged by e.g. desiccation or exposure to light(Cronin and Hay, 1996). The foliaceous red algaIridaea cordata is protected from predation by someherbivores (isopod Idotea) by its cuticle. Other herbi-vores (chiton, sea urchin, limpet) eat Iridaea in allits stages, and yet others (Lacuna, snail), while notdeterred by the cuticle, do not eat infertile Iridaeaanyway (Gaines, 1985).

LightThe importance of self-shading in mature perihytonassemblages has already been mentioned and illus-trates the importance of light for the productivity

of periphyton. Periphyton standing stock is reducedat greater depths because of reduced light incidence(Konan-Brou and Guiral, 1994; Azim et al., 2002a).Irradiance induced more differences in epilithicbiomass than differences in hydrology in labora-tory streams, with higher levels of irradiance leadingto a higher biomass and changes in the taxonomiccomposition of the epilithic assemblage (DeNicolaand McIntire, 1999). Light is less important for thenon-algal components of the periphyton, althoughnon-algal periphyton probably benefits from organicexudates produced by the algal components (Kuehlet al., 1996; Romaní and Sabater, 2000). Photo-adapation was observed in coral reef algae, such thatchanges in irradiance were compensated by changesin the photosynthetic efficiency and maximum rateof photosynthesis (Klumpp and McKinnon, 1992).Periphyton productivity was not suppressed at highlight intensities, which normally inhibit phytoplanktonproductivity (Loeb et al., 1983).

The effects of changes in irradiance on acadjaswere investigated by Arfi et al. (1997). Ninety-fivepercent of the variation in periphyton dry matterin an acadja in the Ebrié lagoon was due to threevariables: photosynthetically active radiation, phyto-plankton chlorophyll a, and the discharge volumeof the river into the lagoon. In the rainy season,river discharge and cloud cover increase, leading toa reduced salinity in the lagoon and a decrease inradiation and photosynthesis. These environmentalchanges lead to a decrease in phytoplankton settling onthe substrates and an overall reduction in periphytonproduction and biomass.

Substrate typeThe seasonal changes of epiphyton in natural systemsare affected by the seasonal changes in the vegetationupon which it grows (Horne and Goldman, 1994).Apart from aquatic vegetation, inorganic substratessuch as rocks and sand are important in naturalsystems.

In aquaculture, a variety of materials can beused: PVC pipes (Keshavanath et al., 2001b), plasticsheets (Shrestha and Knud-Hansen, 1994; Tidwellet al., 1998) and custom-designed materials such asAquamatsTM (Bratvold and Browdy, 2001). Livingsubstrates are not common in aquaculture but occurin integrated cultures of (semi-) aquatic crops likerice with fish, where periphyton grows on plant stems(Chapman, 1991; Chapman and Fernando, 1994).Dead organic materials such as bamboo poles, tree

17

branches, jute sticks, or bundles of sugarcane bagasseare likely to become more important in pond aquacul-ture. In periphyton research, a variety of other mate-rials is used including ceramic tiles, glass fibre filters,and glass slides. For sampling microbial periphytoncommunities, and especially protozoa, polyurethanefoam has been recommended (Cairns et al., 1979).

Substrate type has a distinct effect on periphytongrowth. A comparison of periphyton growing onnatural (leaves) and artificial (glass slides) substratesin a Malaysian river, totals of 37 and 35 species,respectively, were found of which 25 were commonto both substrate types (Nather Khan et al., 1987).In a study in Swedish lakes, glass tubes supportedgreater numbers and a more diverse periphytoncommunity than wood substrates, whereas plasticsubstrates supported only a layer of bacteria (Danilovand Ekelund, 2001). In studies in India andBangladesh, bamboo resulted in greater maximumdensities of periphyton than PVC pipes or sugarcanebagasse bundles (Keshavanath et al., 2001b; Azimet al., 2002b). The reasons for these differences areunknown, but they may be attributable to leaching ofnutrients or toxic substances from the substrates, ordifferences in surface roughness. Similarly, the densityof biofilms of Salmonella sp. on plastic, cement,and steel surfaces was found to differ by an orderof magnitude, probably due to differences in hydro-phobicity of the materials (Joseph et al., 2001). Mostmicroorganisms are hydrophilic and probably adsorbmore strongly to hydrophobic surfaces (Cowling etal. 2000). Generally, plastic and PVC also performedworse in terms of fish production than bamboo ortree branches (Shrestha and Knud-Hansen, 1994;Keshavanath et al., 2001b).

InteractionsGrazing has an overriding effect on biomass whilethe effect of nutrients is not discernible or muchless apparent due to the ability of the periphytonto recycle nutrients and to utilize nutrients from thesubstrate (Steinman et al., 1992; Hill et al., 1992;Pan and Lowe, 1994). Greater nutrient levels lead togreater grazer biomass, indicating that the nutrientsare effectively passed on to higher trophic levels. Lownutrient concentrations limit periphyton biomass butwhen nutrient supply increases, competition for light,both within the periphyton and with other primaryproducers, becomes more important. In lakes, phyto-plankton can contribute to shading at high nutrientconcentrations (Hansson, 1992).

Fish

Morphological and physiological adaptations toherbivory

Although animal components constitute an importantpart of periphyton layers, periphyton is best util-ized by fishes that are adapted to herbivorous diets.These adaptations reflect their evolution from carni-vores to herbivores. Specialization towards a plantdiet required adaptation of the teeth (from graspingto cropping teeth), a grinding apparatus (a pharyngealmill or a gizzard-like stomach), a less acidic stomach(because plant cell walls are destroyed mechanicallyand acidity possibly interferes with the ingestion ofcarbonates from coral substrates or sand), and alonger gut length to increase the residence time, thusensuring better digestion (Horn, 1989). Fishes gener-ally possess the enzymes to digest the contents of plantcells, but lack the enzymes capable of disrupting cellwalls by digesting the beta-linked polymers, such ascellulase (Lobel, 1981). Cellulase activity in fish gutscan probably be ascribed to microorganisms coloniz-ing the fish gut contents (Stickney and Shumway,1974). Many important pond aquaculture speciespossess some of these adaptations to herbivory and areprobably able to utilize periphyton. However, someother species that seem to be adapted to a herbivorousdiet do not utilize periphyton well (e.g., catla; Azim etal., 2002a). The reason for this is not clear, but it seemslikely that they lack the ability to crop the attachedvegetative part of the periphyton. Detritivorous tilapiasare exceptional in the sense that they use low stomachpH (as low as 1.4) to digest cell walls (Beveridge andBaird, 2000).

Periphyton ingestion by fishMost of the quantitative data on periphyton grazingis from coral reef studies and deals with species thatare not of direct interest for aquaculture. For white-spotted devil (Plectroglyphidodon lacrymatus, Poma-centridae) of 62.7 mm mean standard length, a grazingrate of 304.3 g C (g fish)−1 y−1 was measured onshallow fringing reefs in Papua New Guinea (Poluninand Brothers, 1989). For the same species in a coastallagoon in Papua New Guinea, mean consumption wasestimated at 1.57 g dm d−1 for a 14 g fish (Polunin,1988). For another damselfish species, the Australiangregory (Stegastes apicalis, Pomacentridae) on theGreat Barrier Reef, ingestion rates of 773–1433 mgC fish−1 d−1 were measured (mean body weight 63

18

g; Klumpp and Polunin, 1989). For herbivorous reeffish, Van Rooij et al. (1998) estimated an allometricrelationship between carbon intake (g d−1) and bodyweight (g) from several literature sources: C intake =0.0342W0.816 (r2 = 0.946, n = 13, W = 10–100 g).

In a study in a West-African lagoon, Pauly (1976)found that a 20 g blackchin tilapia consumed 1.5 gdetritus dm day−1. Dempster et al. (1993) measuredthe ingestion of algae by Nile tilapia fingerlings (47mm mean standard length), both of planktonic Micro-cystis aeruginosa and from a periphytic assemblageconsisting mainly of Oscillatoria sp. Mean ingestionrate when only periphyton was offered was about 1.8mg dm (g fish)−1 h−1 (measured during a 4-hourperiod). In a second experiment with periphyton densi-ties ranging from 10 to 40 g m−2, ingestion rate wasindependent of periphyton density (mean: 3.68 mgdm g−1 h−1). In a study with indigenous carps inBangladesh, periphyton grazing rates of 0.5–1.2 (kurialabeo), 0.2–0.79 (rohu) and 0.2–1.1 mg dm fish−1

h−1 (orange-fin labeo) were measured (Rahmatullahet al., 2001). Azim et al. (2003) measured periphytonconsumption in three size groups (7, 25 and 150 g)of Nile tilapia in the laboratory and found ingestionrates of 0.90, 0.18 and 0.02 mg dry matter g−1 h−1,respectively. Ingestion rate of Nile tilapia increasedwhen periphyton density on the glass plates increased.

A comparison of these observations after conver-sion to the same unit (mg dm [g fish]−1 d−1; Table4) shows that ingestion rates estimated for coral reeffish are generally higher than those measured in thelaboratory. Information on grazing by fishes can beobtained from observations of ingestion (number ofbites during a defined time period) in relation to gutfullness, through exclusion experiments in the naturalhabitat (using cages to exclude fish from certain areas,after which grazing rates follow from biomass differ-ences between areas with and without cages) or bymeasuring biomass differences on artificial substratesin the laboratory before and after grazing. Advantageof the observation and exclusion methods is thatthe measurements are relatively unaffected by hand-ling stress, while laboratory studies often involveshort study periods that are hard to extrapolate tolonger periods of time. Laboratory conditions (solitaryfish, sometimes unialgal diets, various sources ofstress) strongly affect the natural feeding behaviourof fish, which probably leads to underestimationsof periphyton consumption with these experiments(Horn, 1989; Azim, unpublished results).

Apart from fish weight, temperature is important.A linear relationship between the number of bitesper hour and temperature was observed in damselfish(whitespotted devil), with the mean number of bitesdoubling when water temperature increased from 26to 32 ◦C (Polunin and Brothers, 1989). There arealso differences between species. For some species,periphyton is simply not a preferred food. Yields ofthe indigenous kuria labeo in ponds with periphytonin Bangladesh were not different from control pondswithout substrates, suggesting that this labeo didnot eat the periphyton (Azim et al., 2001a). Simi-larly, catla were not observed to feed on periphytongrowing on bamboo substrates in ponds (Azim et al.,2002a). Common carp were observed to lose weightin tanks with periphyton substrates while Nile tilapiagained weight by utilizing the periphyton (Van Dam,unpublished).

Periphyton nutritional quality also plays a role indetermining ingestion rates. Fish feeding on algae,macrophytes or detritus ingest larger quantities tocompensate for the low energy content. To compensatefor low protein content, they selectively feed onthe components with the highest protein content,thus maximizing the dietary protein to metaboliz-able energy (P/ME) ratio (Horn, 1989; Bowen etal., 1995). Stoplight parrotfishes (Sparisoma viride,Scaridae) on Carribean reefs spend 70–90% of the dayforaging, ingesting huge amounts (sometimes morethan 60% of their own body mass per day) of low-quality food (P/ME ratios ranging from 5–8 mg kJ−1)(Bruggemann, 1995).

Periphyton as fish feed: proximate composition

The composition of natural food for pond fishes hasbeen reviewed by Hepher (1988). Except for macro-vegetation and some algae, most natural food typesare rich in protein. Fluctuations in composition aremainly caused by differences in ash content. Thecomposition of detritus is highly variable and dependsa lot on the source material. Generally, periphytoncomposition is similar to other natural food types. Onedifference is the high organic matter content of theperiphyton assemblage due to the mucopolysaccharidematrix. Nielsen et al. (1997) determined the composi-tion of biofilms and found that the extracellular poly-meric substances accounted for 50–80% of the totalorganic matter. Protein was the largest fraction of theextracellular substance, despite the emphasis that isususally put on polysaccharides. Periphyton can also

19

Table 4. Comparison of periphyton ingestion rates from different experiments. Data were converted to mg dm (g fish)−1 d−1

Species Location Fish size Grazing rate Source

(g fw) (mg dm g−1 d−1)

Sarotherodon melanothron Lagoon, Ghana 20 75 Pauly, 1976

Plectroglyphidodon lacrymatus Shallow fringing reef, Papua New Guinea 16.9c 98.8a,b Polunin and Brothers, 1989

Stegastes apicalis Great Barrier Reef, Australia 63 24.5–45.5b Klumpp and Polunin, 1989

Plectroglyphidodon lacrymatus Coastal lagoon, Papua New Guinea 14 112.1 Polunin, 1988

Oreochromis niloticus Laboratory, periphyton on glass plates 3.7d 21.6–44.2e Dempster et al., 1993

Oreochromis niloticus Laboratory, periphyton on glass plates 7 10.8e Azim et al., 2003

Oreochromis niloticus Laboratory, periphyton on glass plates 25 2.16 Azim et al., 2003

Oreochromis niloticus Laboratory, periphyton on glass plates 150 0.24 Azim et al., 2003

Labeo gonius Laboratory, periphyton on glass plates ±10–100 6–14.4e Rahmatullah et al., 2001

Labeo calbasu Laboratory, periphyton on glass plates ±10–100 2.4–13.2e Rahmatullah et al., 2001

Labeo rohita Laboratory, periphyton on glass plates ±10–100 2.4–9.5e Rahmatullah et al., 2001

Assumptions: aAssuming 365 days in one year. bAssuming 50% C in dm. cCalculated with L-W relationship from same publication.dCalculated with L-W relationship for O. niloticus from Fishbase (Froese and Pauly 2001). eAssuming diurnal feeding (12 h day−1).

trap exogenous organic matter from the water column,which may account for a large part of the “bio”-mass(Sansone et al., 1998). Organic compounds adsorbto particulate and colloidal calcium carbonate that isformed during photosynthesis (Wetzel, 1975).

Table 5 compares the composition of a numberof natural pond foods with that of periphyton.Characteristics of natural foods are the low drymatter content, and variable protein, energy and ashcontents. Periphyton grazed from coral reefs, mixedwith sediment material, had the lowest protein andenergy content, whereas bacteria, zooplankton andinsects had the highest nutritional quality. Generally,periphyton has a high ash content compared to othernatural feeds. Partly, this is due to the high contentof carbonates that are formed (Wetzel, 1975) andthe entrapment of inorganic particles. We estimatedthe P/ME-ratios of the various food types, assumingthat metabolizable energy is 60% of gross energy(see Table 5). P/ME-ratios ranged from about 6 inperiphyton ingested by parrotfish and in calcareous redalgae to more than 60 in bacteria, with the majorityof values between 10 and 40 kJ g−1. Values esti-mated for periphyton grown on different substratetypes in aquaculture ponds ranged from 15.6 to 25.5kJ g−1. There seemed to be an effect of substratetype on the nutritional quality of the periphyton, withbamboo substrates giving better quality periphytonthan jutestick and branches of the hizol tree (Azimet al., 2002b). P/ME ratios for natural feeds rangetypically range from 1 to 30 mg kJ−1 (Bowen et al.,1995).

There is little information on other indicators ofperiphyton nutritional quality. Phillips et al. (1994)analyzed the amino acid profile of proteins from amicrobial mat grown on grass silage. A comparisonwith the essential amino acid requirements of severalfish species shows that the microbial mat was onlydeficient in valine.

Assimilation efficiency and food conversion ratio

Montgomery and Gerking (1980) measured assimi-lation efficiency in cortez damselfish (Eupomacentrusrectifraenum, Pomacentridae) and giant damselfish(Microspathodon dorsalis, Pomacentridae) from BajaCalifornia, Mexico feeding on various species ofmarine algae. There was a large difference between theproximate composition of the periphyton mat (81.6%ash, 1.7% protein in dm) and the stomach contents ofcortez damselfish (50.2% ash, 26.1% protein), whichwas attributed to selective feeding. The giant damsel-fish fed non-selectively on algal turf consisting solelyof the red alga Polysiphonia. The assimilation effici-ency on a biomass basis was 20–24% and for protein57–67%. A digestibility study with periphyton matsgrown on grass silage showed a dry matter digesti-bility of 62% and 60%, and protein digestibility of81% and 75%, for Nile tilapia and silver carp, respec-tively. Drying significantly lowered the digestibility ofthe material to less than 50% on a dry matter basis(Ekpo and Bender, 1989; Bender et al., 1989). Table6 summarizes data on assimilation efficiency (AE, ordigestibility) of fish feeding on periphyton and some

20

Tabl

e5.

Com

pari

son

ofpe

riph

yton

nutr

ition

alqu

ality

with

othe

rty

pes

ofna

tura

lfoo

ds.P

/ME

-rat

ios

wer

ees

timat

edby

usas

sum

ing

that

met

abol

izab

leen

ergy

is60

%of

gros

sen

ergy

for

allf

ood

type

s

Food

type

Subt

rate

type

Dry

mat

ter

Prot

ein

Lip

ids

Car

bohy

drat

esA

shE

nerg

yP/

ME

-rat

ioa

Sour

ce

(%)

(%dm

)(%

dm)

(%dm

)(%

dm)

(kJ

g−1)

(mg

kJ−1

)

Bac

teri

a(P

seud

omon

assp

.)–

80.4

1.7

16.9

20.5

65.3

Mat

tyan

dSm

ith,1

978

Bac

teri

a–

5.4

19.7

45.7

Hep

her,

1988

Alg

ae(S

piru

lina

sp.)

–53

.82.

511

.119

.6M

atty

and

Smith

,197

8

Alg

ae–

14.1

–21.

717

.6–3

1.3

3.7–

9.9

26.9

–46.

79.

3–15

.832

.7H

ephe

r,19

88

Mac

roph

ytes

–15

.814

.64.

513

.916

.314

.9H

ephe

r,19

88

Zoo

plan

kton

–7.

3–35

.041

.5–6

4.3

19.0

–26.

49.

2–28

.25.

1–19

.620

.1–2

3.8

40.1

Hep

her,

1988

Inse

cts

–14

.8–2

6.0

34.7

–68.

84.

9–18

.620

.1–2

2.5

3.7–

11.8

20.5

–23.

639

.1H

ephe

r,19

88

Mol

lusc

s–

32.2

39.5

7.8

7.5

32.9

16.3

40.5

Hep

her,

1988

Det

ritu

s–

91.5

12.4

19.7

Hep

her,

1988

Ave

rage

natu

ralf

ood

–14

.252

.17.

727

.37.

7H

ephe

r,19

88

Gre

enal

gae

Bra

nitic

boul

ders

10.2

4.5

59.9

25.4

13.8

12.4

Mon

tgom

ery

and

Ger

king

,198

0

Bro

wn

alga

eG

rani

ticbo

ulde

rs8.

34.

855

.731

.311

.711

.7M

ontg

omer

yan

dG

erki

ng,1

980

Red

alga

eG

rani

ticbo

ulde

rs7.

72.

151

.938

.310

.412

.4M

ontg

omer

yan

dG

erki

ng,1

980

Cal

care

ous

red

alga

eG

rani

ticbo

ulde

rs1.

21.

715

.581

.63.

36.

1M

ontg

omer

yan

dG

erki

ng,1

980

Alg

alm

atG

rani

ticbo

ulde

rs1.

72.

114

.681

.61.

716.

1M

ontg

omer

yan

dG

erki

ng,1

980

Peri

phyt

on+

sedi

men

tC

oral

rock

0.35

–2.6

66.6

–95.

60.

9–4.

26.

5–10

.4B

rugg

eman

n,19

95

Peri

phyt

onB

ambo

o22

–30

2.0–

5.5

15–2

917

–20

29.1

–32.

6A

zim

etal

.,20

02b;

2002

c

Peri

phyt

onK

anch

i19

–28

3.0

14–2

919

23.4

–25.

4A

zim

etal

.,20

02b;

2002

c

Peri

phyt

onH

izol

24.8

9.2

4120

.420

.3A

zim

etal

.,20

02b

Peri

phyt

onJu

test

ick

12.7

2.8

3113

.615

.5A

zim

etal

.,20

02c

21

Table 6. Assimilation efficiency (AE, or digestibility) in fish feeding on periphyton and other natural foods

Food type Fish species Total Organic AE (%) Carbo- Lipids Source

matter protein hydrate

Thalassa testudineum Sparisoma radians 50 66 Targett et al., 1995

Lobophora variegata S. radians 40–49 63–71 Targett et al., 1995

Lobophora variegata S. chrysopterum 48 65 75 Targett et al., 1995

Padina gymnospora S. chrysopterum 25 45 66 Targett et al., 1995

Cladophora glomerata Oreochromis niloticus 72.3 Appler and Jauncey, 1983

Hydrodictyon reticulatum O. niloticus 70.9 Appler, 1985

Hydrodictyon reticulatum Tilapia zillii 75.7 Appler, 1985

Bluegreen algae O. niloticus 64–72 34–50 50–62 Getachew, 1988

Marine algae Eupomacentrus rectifraenum 24.2 67 44 56.4 Montgomery and Gerking, 1980

Marine algae Microspathodon dorsalis 20.1 57.4 37.1 46.3 Montgomery and Gerking, 1980

Algal mat on silage O. niloticus 62.1 80.7 Ekpo and Bender, 1989

Algal mat silage Hypophthalmichthys molitrix 59.7 75.0 Ekpo and Bender, 1989

other natural foods. Overall AE ranged from 20 to50%, but protein AE was generally higher (57–80%).

Very little work on feed conversion efficiency ofperiphyton into fish biomass has been done. In somestudies, algae were fed to fish to determine the feedconversion ratio (FCR, reported here as g dm feeddivided by g fresh fish gain). Stanley and Jones(1976) fed the cyanobacterium Spirulina platensis tobigmouth buffalo (Ictiobus cyprinellus, Catostomidae;53.1 g initial weight, 29.1 g kg−1 d−1 for 28 days,21–25 ◦C) and blue tilapia (Oreochromis aureus,Cichlidae; 23.8 g initial weight, 28.4 g kg−1 d−1

for 36 days), and obtained FCRs of 2.0 for bothspecies. Grass carp fed at 21–27 g kg−1 d−1 did notperform well with FCR values of 9.7–11.4. The FCRfor Nile tilapia fed on a diet containing Cladophoraglomera meal as the sole protein source was 2.33(Appler and Jauncey, 1983). Appler (1985) formulateddiets incorporating varyious amounts of the greenfilamentous alga Hydrodictyon reticulatum. The dietcontaining the alga as the only protein source gaveFCRs of 3.6 for Nile tilapia and 3.9 for redbelly tilapia(Tilapia zillii, Cichlidae) (initial weight 1 g, 50 daysculture period, 26 ◦C, feeding level 5% body weightper day). Azim et al. (2003) fed 7–8 g (individualweight) Nile tilapia with periphyton grown on glasssubstrates in a greenhouse in The Netherlands. Despitethe high ash content of the periphyton (55% on drymatter basis), the fish grew and the FCR was 2.81.

Potential fish production based on periphyton

To estimate the potential fish production fromperiphyton-based pond aquaculture systems, weconstructed a simple dynamic simulation modeland incorporated values found in the literaturefor periphyton productivity, maximum periphytonbiomass, ingestion rate and conversion efficiency.The model (Figure 2) consists of two state variables,periphyton biomass (PB; g) and fish biomass (FB;g), and two rate variables, net periphyton growth rate(PBgrowth; g d−1) and periphyton conversion rate tofish (PBconversion; g d−1). PBgrowth is defined with theequation:

PBgrowth = K · PB · (1 − PB/PBmax) (1)

in which K is the relative growth rate of periphyton(d−1) and PBmax is the maximum periphyton biomass(g). Equation (1) results in a curve where theperiphyton biomass increases with time to a plateau(PBmax) where PBgrowth = 0 (see broken line “a” inFigure 3). This is the theoretical periphyton densitywhere self-shading and/or nutrient limitation preventa further increase in density, and productivity andmortality are balanced. In the model, maximumperiphyton growth occurs when PB = 0.5 PBmax.

PBconversion is calculated by assuming that the fishconsume periphyton at a constant rate (q, in d−1)equivalent to a percentage of their biomass:

PBconversion = q · FB (2)

The grazing by the fish reduces the periphytonbiomass, keeping it from reaching its maximum

22

Figure 2. Relational diagram of simple simulation model for periphyton-based fish production. K and PBmax are parameters of the periphytongrowth rate equation. PB is the actual periphyton biomass (g). PBdens is the periphyton density in g per m2 of substrate surface area. SAI is thesurface area index (m2 of substrate area per m2 of pond area). FB is the fish biomass. PBconversion is the rate at which periphyton is consumedby fish, which is calculated as a fixed percentage (q) of fish biomass. FCR is the conversion ratio of periphyton to fish biomass. FBdens is thefish biomass density in g fish per m2 pond surface area. For further explanation, see text.

biomass and maintaining its productivity. In themodel, it was assumed that the periphyton had aminimum biomass (PBmin) before fish were stockedand that fish grazing would cease whenever thebiomass of the periphyton would be lower than thatminimum biomass.

This simple model was implemented in Stella�

6.0 and run with a time-step of 0.05 day. Parametervalues were derived from the present review. Weassumed a maximum periphyton density of 100 g dmm−2 (Table 2). PBmax was derived from this valueby multiplying with the substrate area. Minimumdensity was assumed to be 10 g m−2. Net periphytonproductivity was set at 1.5 g C m−2 d−1 or 3 g dm

m−2 d−1 (assuming 50% C in dm) (see Table 3),which converts into a value of K = 0.12 (this followsfrom rewriting equation (1) and substituting PB =0.5·PBmax). Ingestion rate was assumed to be 5% offish biomass d−1 (q = 0.05; based on Bowen et al.,1995 and Van Rooij et al., 1998) and the conversionefficiency of periphyton dry matter to fish biomass wasassumed to be 50% (FCR = 2). Fish stocking densitywas assumed to be 1 m−2 and initial fish weight was5 g (resulting in an initial fish density of 5 g m−2,which is typical for pond culture). Substrate densitywas assumed to be 1 m2 per m2 of pond surface (inthe model, this is called the surface area index orSAI).

23

Figure 3. Simulation of periphyton and fish production with 1 fish m−2 (5 g individual weight) and periphyton productivity of 3 g dm m−2

d−1. For model description and simulation conditions, see text. A: fish and periphyton biomass. Broken lines indicate simulated periphytonbiomass without fish (a) and with higher (1.5 m−2) fish stocking density. B: rates of periphyton production and consumption. C: ratio offish:periphyton biomass throughout the simulation. Straight dotted lines indicate the time of maximum periphyton productivity (1) and themoment when periphyton production and consumption by fish are equal (2). For further explanation, see text.

24

The results of the simulation are shown in Figure3. All results are reported per m2 of pond surface(note that because SAI = 1, periphyton densities perm2 substrate area are the same as per m2 pond surfacearea). Simulated periphyton biomass increased from10 g m−2 initially to a maximum of 90 g m−2 after52 days. Before day 52, periphyton productivity wasgreater than the consumption of the periphyton by fish.Maximum periphyton productivity was achieved onday 22. After day 58, fish grazing exceeded periphytonproductivity as a result of the increased fish biomass(about 20 g m−2 on day 58) and periphyton biomassdecreased steadily until reaching a value of about 50g m−2 on day 120. The model computes a net fishproduction of 948 kg ha−1 in 120 days, and with threecrops per year the production of fish due to periphytonwould be 2,844 kg ha−1 y−1.

The model does not account for the many interac-tions that would occur in a periphyton-based fishpond.In reality, other food resources in the pond wouldcontribute to fish production, and fishes may switchbetween different food resources depending on thedensity of the resource and feeding preferences. Themodel demonstrates that the ratio of fish to periphytondensity is very important. In the beginning of theculture period, fish density is low, the periphytonremains under-exploited and productivity is limited.Towards the end of the culture period, fish densityis much higher which results in increased grazingpressure and lower periphyton density. The highestperiphyton productivity occurred between days 20 and60, when the ratio of fish to periphyton biomass was0.18–0.24. When designing periphyton-based culturesystems, this should be taken into account. Multiplecropping and partial harvesting of fish may be usedto keep the fish:periphyton biomass ratio at optimallevels.

Conclusions and recommendations for furtherresearch

Role of periphyton in aquaculture systems

Periphyton is a complex mixture of autotrophicand heterotrophic organisms and cannot simply beregarded as an attached equivalent of phytoplankton,although it certainly performs similar functions inponds, such as oxygen production and the uptake ofinorganic nutrients. There is an intense exchange ofinorganic and organic nutrients between autotrophic

and heterotrophic components of the periphytonassemblage, which probably results in less accumu-lation of detritus of periphyton origin on the bottomof the ponds in comparison to a phytoplankton-dominated system. In addition, suspended organicmaterial is trapped and processed by the periphytonlayer. Thus, in a periphyton-based system the biomassproduced remains in the aerobic layers of the pondwhere decomposition is faster and where it is moreaccessible to grazing by fish. In this way, periphytonprobably contributes to making pond systems morenutrient efficient. Adding substrates to experimentalponds in Bangladesh led to an 54–64% increasein nitrogen use efficiency (N in fish/N in inputs)but overall nitrogen efficiency remained quite low(8.7% with bamboo substrates) (Azim et al., 2002c).Several studies show a positive effect of periphytonon nitrification, leading to lower ammonia concen-trations. Maximum periphyton production can beachieved at lower nutrient levels than those needed forphytoplankton. Nutrient concentrations in the watercolumn may be poor indicators of conditions forperiphyton close to the substrate, where steep nutrientgradients exist. The methodology needed to studythese processes is still developing (Sand-Jensen andBorum, 1991; Bott et al., 1997). Periphyton doesindeed seem to be more stable than phytoplankton,as a result of which the risk of community collapseand water quality deterioration is much smaller.However, for improved management and manipulationof periphyton layers in fishponds, more knowledgeabout the basic processes in the periphyton assemblageis needed.

Ability of fish to utilize periphyton

Although not all fish species are suitable for culturein periphyton-based systems, success in such systemsis not limited to specialist (macro)herbivores. Moregeneral detritus and benthos feeders can also thriveon periphyton. Some species (e.g., catla and commoncarp) are not able to utilize periphyton directly butmay play an important role in periphyton-based poly-culture systems. Not enough is known about themechanisms for exploiting periphyton and the selec-tion of food from periphyton assemblages by fish,or about the relationship between periphyton densityand the ability of different fish species to harvestperiphyton (functional response types). Experimentsto investigate this are extremely difficult to design,as periphyton density is affected by environmental

25

Figure 4. Number of substrate poles needed to install periphyton substrates in a 200 m2 pond at different pole diameters and SAI’s.

factors and changes rapidly with time. Because ofthis, observation periods are short which leads to largeextrapolation errors. In addition, invertebrate grazersconfound the effect of fish grazing. Nevertheless, moreknowledge about these basic processes is needed ifprogress in system design is to be made.

Potential of periphyton-based fish production

A considerable amount of experimental work onperiphyton-based fish production systems has beendone but it is difficult to compare studies becauseof the wide variety in culture systems, substratetypes, fish species and environments used. Never-theless, there is enough evidence that ponds withsubstrates can produce more fish than identical pondswith the same fertilization/feeding regime, but withoutadditional substrates. The main factors affecting thesuccess of periphyton-based systems are the choice ofspecies, the choice of substrate material, the densityof substrate material in relation to pond surface area(SAI), and the density of fish in relation to periphytondensity.

There are clear indications that biofilms andperiphyton develop better on natural than on artifi-cial materials, probably because of differences in thehydrophilic characteristics of these materials. Also,

the presence of organic matter is important for theinitiation of bacterial processes that are the start oflayer formation. Bamboo seems to be especially suit-able as it not only yields more, but also higher qualityperiphyton. Certainly, biodegradable substrates favourthe growth of bacteria and more research is needed tolook into the potential of their use in fishponds. Onthe other hand, they do pose the danger of fish killsif the decomposition processes are so rapid that theyconsume all the oxygen (Keshavanath et al., 2001b).

More research must be devoted to the relation-ship between substrate area and pond surface area.In the studies we reviewed, SAI ranged from 0.02–1.54, and the few studies that investigated differentsubstrate densities showed that increasing SAI beyonda certain value did not lead to further increases infish production. This critical value depends stronglyon the type of substrate used. On the one hand,research should focus on the possibility of increasingSAI because periphyton production rather than theability to harvest the periphyton seems to limit fishproduction. Can nutrient and light limits be shifted bymanipulating the numbers and diameters of substratematerial used without negatively affecting the physicalspace requirements of the fish (see Figure 4)? Maybeother, more efficient substrate conformations can bedesigned.

26

The extent to which periphyton can be usedin intensive aquaculture systems is not clear. Itmay be possible to use specially designed substratesthat leach nutrients in the right mix for optimalperiphyton growth. Periphyton may be combined withfeeds by stocking two fish species: a high-value,carnivorous fish that utilizes the feed and anotherspecies that utilizes the periphyton. Much more workis needed to determine optimum combinations andpossibly special feed formulations for periphyton-based systems. Perhaps periphyton systems can beused for a specific part of the culture cycle, e.g. infingerling production. The positive effect of substrateson fish survival, probably related to stress reduction,points in this direction.

With regard to the culture of marine fish, verylittle experimental work is reported. Although someinitial work on periphyton was done in coastal lagoonsin West Africa, most of the other work reportedwas done in extensive and semi-intensive freshwaterponds. Mullets (Mugilidae) are probably very suit-able for growing in marine periphyton-based systemsbecause of their feeding habits, but hardly any workwith mullets and periphyton has been done so far(Eskinazi-Leça et al., 1980). Another interestingoption is to culture marine shrimp in periphytonbased systems. Most of the work done on the use ofsubstrates and freshwater prawns was geared towardsproviding shelter and preventing territorial behaviour.It is not clear whether periphyton attached to artifi-cial substrates can be harvested by shrimp. Substratesmay enhance the formation of periphyton-detritusassemblages that can be utilized by shrimp, thuspreventing the accumulation of decomposing organicmatter and adverse environmental conditions on thepond bottom.

Experimental work in fishponds shows thatperiphyton substrates can roughly double the yield offish in ponds with no supplemental feeding (Azimet al., 2001a, 2002a; Keshavanath et al., 2002).Based on our simple model and the productivity ofperiphyton, we estimate that the potential fish yieldwith periphyton is around 5 tonnes ha−1 y−1 with thecurrent technology. Assuming that the fish:periphytonbiomass ratio would be maintained in the optimumrange, further increases in production can come fromincreasing periphyton productivity, e.g., by manipu-lating nutrient levels, identifying substrate materialsthat facilitate periphyton growth, or increasing the SAI(provided that no nutrient or light limitation occurs).

Acknowledgements

The authors would like to thank J.M. van Rooij,M.A. Wahab, P. Keshavanath and D.J. Baird for theircontributions to this study. This review was writtenwith financial support from the European Commission(Grant INCO-DC IC18-CT97-0196) and the Inter-disciplinary Research and Education Fund (INREF) ofWageningen University.

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