Reviews in Fish Biology and Fisheries 12: 1–31, 2002. © 2003 Kluwer Academic Publishers. Printed in the Netherlands.
1
The potential of fish production based on periphyton Anne A. van Dam1,3 , Malcolm C.M. Beveridge2 , M. Ekram Azim1 & Marc C.J. Verdegem1 1 Fish
Culture and Fisheries Group, Department of Animal Sciences, Wageningen University, P.O. Box 338, 6700 AH Wageningen, The Netherlands; 2 FRS Freshwater Laboratory, Faskally, Pitlochry, Perthshire, Scotland, UK PH16 5LB; 3 Current address: Department of Environmental Resources, IHE-Delft, P.O. Box 3015, 2601 DA Delft, The Netherlands (E-mail:
[email protected]; Fax: 31-15-2122921; Phone: 31-15-2151712/2151715)
Received 5 December 2001; accepted 17 October 2002
Contents Abstract Introduction Background Objectives and scope of the review Terminology Natural and artificial periphyton-based systems Natural systems with periphyton Brush-park fisheries Traditional aquaculture systems in southeast Asia Aquaculture experiments Water treatment with periphyton Periphyton productivity Development of the periphyton assemblage and species composition Biomass and productivity Effects of environmental factors Fish Morphological and physiological adaptations to herbivory Periphyton ingestion by fish Periphyton as fish feed: proximate composition Assimilation efficiency and food conversion ratio Potential fish production based on periphyton Conclusions and recommendations for further research Role of periphyton in aquaculture systems Ability of fish to utilize periphyton Potential of periphyton-based fish production Acknowledgements References
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Key words: fish ponds, herbivory, nutrients, periphyton, phytoplankton
Abstract Periphyton is composed of attached plant and animal organisms embedded in a mucopolysaccharide matrix. This review summarizes research on periphyton-based fish production and on periphyton productivity and ingestion by fish, and explores the potential of developing periphyton-based aquaculture. Important systems with periphyton are 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 substrates compared to controls without substrates. Colonization of substrates starts with the deposition of organic substances
2 and attraction of bacteria, followed by algae and invertebrates. After initial colonization, biomass density increases to a maximum when competition for light and nutrients prevents a further increase. Often, more than 50% of the periphyton ash-free dry matter is of non-algal origin. Highest biomass (dm) in natural systems ranges from 0 to 700 g m−2 and in aquaculture experiments was around 100 g m−2 . Highest productivity was found on bamboo in 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 stimulate periphyton production. Grazing is the main factor determining periphyton density, while substrate type also affects productivity and biomass. Better growth was observed on natural (tree branches and bamboo) than on artifical materials (plastic and PVC). Many herbivorous and omnivorous fish can utilize periphyton. Estimates of periphyton ingestion by fish range from 0.24 to 112 mg dm (g fish)−1 d−1 . Ingestion rates are influenced by temperature, fish size, fish species and the nutritional quality of the periphyton. Periphyton composition is generally similar to that of natural feeds in fishponds, with a higher ash content due to the entrapment of sand particles and formation of carbonates. Protein/Metabolizable Energy (P/ME) ratios of periphyton vary from 10 to 40 kJ g−1 . Overall assimilation efficiency of fish growing on periphyton was 20–50%. The limited work on feed conversion ratios resulted in values between 2 and 3. A simple simulation model of periphyton-based fish production estimates fish production at approximately 2.8 t ha−1 y−1 . Together with other food resources in fishponds, total fish production with the current technology level is estimated at about 5 t ha−1 y−1 . Because grazing pressure is determined by fish stocking rates, productivity of periphyton is currently the main factor limiting fish production. We conclude that periphyton can increase the productivity and efficiency of aquaculture systems, but more research is needed for optimization. Areas for attention include the implementation and control of periphyton production (nutrient levels, substate types and conformations), the ratio of fish to periphyton biomass, options for utilizing periphyton in intensive aquaculture systems and with marine fish, and possibilities for periphyton-based shrimp culture.
Introduction Background Fish production through aquaculture is realized in a wide variety of culture systems, from extensive seasonal ponds to intensive concrete raceways or floating marine cages. In 1998, 53% of the 30 million tonnes of finfish, molluscs and shrimp produced in aquaculture were predominantly cultured in extensive to semi-intensive pond systems (mainly Chinese carps like Hypophthalmichthys molitrix, Ctenopharyngodon idella, and Aristichthys nobilis, all Cyprinidae; common carp, Cyprinus carpio, Cyprinidae; and Nile tilapia, Oreochromis niloticus, Cichlidae). Ponds are also important in terms of production value, accounting for some 47% of the total value. Carps and the tiger shrimp (Penaeus monodon, Penaeidae) are among the most important commodities (Table 1; FAO, 2001). All pond species feed low in the food chain, most being filter feeders, herbivores, or omnivores. Production in extensive pond systems is based on the natural productivity of the pond and solar energy. In semi-intensive systems, organic and chemical fertilizers and supplemental feeds are added whereas intensive systems are based predominantly on high-quality complete feeds. Only 5–15% of the
nitrogen added to the ponds as fertilizer is harvested as fish biomass (Edwards, 1993; Gross et al., 1999). In feed-driven systems, only 20–30% of the nitrogen in the feed is retained in the fish biomass (Avnimelech and Lacher, 1979; Boyd, 1985; Jiménez-Montealegre, 2001). The nutrients that are not harvested as fish biomass 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 aquaculture systems more nutrient efficient. Generally, three food pathways can be distinguished in aquaculture systems: (1) direct feeding by the fish on feeds; (2) the autotrophic pathway, in which solar energy is used by primary producers (mainly algae) to convert carbon dioxide into organic matter that can be utilized by fish; and (3) the heterotrophic pathway, in which heterotrophic organisms (bacteria, protozoa, and other invertebrates) decompose organic matter that can be utilized by the fish (Schroeder, 1978). These three pathways are linked through fluxes of organic and inorganic nutrients. In wastefed systems, the heterotrophic pathway can be more important than the autotrophic pathway, but stable isotope studies show that a large part of the microbial production in ponds is based on algal detritus (Schroeder, 1978; Schroeder et al., 1990). Estimates
3 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 production system
3.27 1.86 1.18 0.26 0.23 0.11
6.9 4.0 2.5 0.6 0.5 0.2
CM CM CM CM CM CM
1.9 0.6
3.86 1.03
8.2 2.2
P P
3.31 2.89 2.47 1.58 1.04 0.79 0.75 0.69 0.63 0.56 0.45 0.44 0.37 0.26 0.21 0.16
10.7 9.4 8.0 5.1 3.4 2.6 2.4 2.2 2.0 1.8 1.5 1.4 1.2 0.8 0.7 0.5
3.09 2.66 2.83 1.45 0.83 0.89 1.94 2.20 0.55 0.47 0.54 1.36 0.55 0.42 0.82 0.16
6.6 5.6 6.0 3.1 1.8 1.9 4.1 4.7 1.2 1.0 1.1 2.9 1.2 0.9 1.7 0.3
P P P P P P P C P P P P/R P P P P
24.01 16.24 30.86
77.8 52.6 100.0
32.56 22.09 47.08
69.2 46.9 100.0
Volume 106 MT
%
Common name
Scientific name
Molluscs Pacific cupped oyster Japanese carpet shell Yesso scallop Blue mussel Blood cockle Mediterranean mussel
Crassostrea gigas Ruditapes philippinarum Pecten yessoensis Mytilus edulis Anadara granosa Mytilus galloprovincialis
3.44 1.43 0.86 0.50 0.25 0.16
11.1 4.6 2.8 1.6 0.8 0.5
Shrimp Giant tiger prawn Whiteleg shrimp
Penaeus monodon Penaeus vannamei
0.58 0.19
Finfish Silver carp Grass carp Common carp Bighead carp Crucian carp Nile tilapia Rohu Atlantic salmon Catla Mrigal White Amur bream Rainbow trout Milkfish Channel catfish Japanese eel Mud carp
Hypophthalmichthys molitrix Ctenopharyngodon idellus Cyprinus carpio Aristhichthys nobilis Carassius carassius Oreochromis niloticus Labeo rohita Salmo salar Catla catla Cirrhinus mrigala Parabramis pekinensis Oncorhynchus mykiss Chanos chanos Ictalurus punctatus Anguilla japonica Cirrhinus molitorella
Total this list Total ponds (excluding Oncorhynchus mykiss) Total world (finfish, molluscs and shrimp)
of the proportion of the standing stock of phytoplankton that accumulates as sediment in the bottom range from 20 to 50% per day (Jiménez-Montealegre, 2001). Thus, a large part of the phytoplankton production is decomposed on the pond bottom and contributes to the accumulation of nutrients in the sediment. Because many fish species are not able to harvest phytoplankton directly from the water column, an extra trophic level is involved in converting phytoplankton into fish biomass. With an estimated energy transfer efficiency of 10% per trophic level (Pauly and Christensen, 1995), maximum fish yield may be no more than 1% of the energy fixed by the phytoplankton consumed. Fish yields from extensive and
Value 106 US$
semi-intensive ponds could be up to ten times higher if primary production could be harvested directly by herbivorous fish. Whether phytoplankton can be harvested directly by fish depends largely on the fish species stocked. Although species like silver carp and bighead carp are capable of harvesting microalgae directly, many species used in aquaculture cannot. Even for Nile tilapia, generally regarded as a phytoplankton feeder, it seems questionable whether it can derive enough energy from exploiting phytoplankton (Dempster et al., 1993, 1995). Phytoplankton has some other disadvantages. Nighttime respiration by phytoplankton in ponds may lead to oxygen depletion during the
4 early morning hours, causing a risk of fish mortality (Madenjian et al., 1987). Decomposition of sedimented phytoplankon may result in toxic decomposition products (ammonia, nitrite) and increased oxygen demand. Phytoplankton blooms are unstable and may collapse unexpectedly, resulting in a sudden drop in dissolved oxygen concentrations and fish mortality (Delincé, 1992). On the other hand, phytoplankton serves a number of very important functions in pond aquaculture. It is a net producer of dissolved oxygen, which is indispensable for fish growth and production (Smith and Piedrahita, 1988; Teichert-Coddington and Green, 1993). It is also the most important sink of ammonianitrogen, which is excreted by fish and potentially toxic (Hargreaves, 1998; Jiménez-Montealegre, 2001). Most truly herbivorous fish species feed on larger, benthic, epilithic or periphytic algae, rather than on phytoplankton (Horn, 1989). Such algae require substrates for attachment, which are virtually absent in fish ponds. In response to the high nutrient levels that are 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, more fish species may be able to harvest them, resulting in a more efficient utilization of primary production. Communities of attached algae are generally more stable than phytoplankton and the risk of collapse is much lower (Westlake et al., 1980). Some studies suggest that the production of attached algae per unit water surface area is higher than of phytoplankton (Wetzel, 1964). Horne and Goldman (1994) stated that “it is mechanically more efficient to scrape or graze a two-dimensional layer of periphyton than to filter algae from a three-dimensional planktonic environment”. Considering all these aspects, it might be advantageous to develop periphyton-based pond culture. Objectives and scope of the review The main objective of this review is to assess the potential of periphyton-based fish/shrimp production in aquaculture pond systems on the basis of the available literature on periphyton productivity and on periphyton utilization by fish and shrimp. We present an overview of data on natural and culture systems where fish utilize periphyton and describe the
species composition of periphyton and the architecture and functionality of the periphyton assemblage. The productivity of periphyton in natural systems in relation to environmental factors, substrate types and grazing are reviewed and the potential productivity in culture sytems is estimated. We also review the quality of periphyton as a fish feed and examine the morphological and physiological adaptations of fish for utilizing periphyton. Data on periphyton grazing by fish and the effects of grazing on periphyton productivity are discussed. Based on this body of information, we estimate potential periphyton-based fish production with a simple simulation model. To conclude, we indicate knowledge gaps for developing periphytonbased aquaculture and make recommendations for further research. Terminology Throughout this paper, we will use the term “periphyton” to indicate the assemblage of attached aquatic plant and animal organisms on submerged substrates, including associated non-attached fauna. Several other terms are used with regard to this assemblage. The most general terms are “aufwuchs” (often also written with a capitalized A, from the original German word Aufwuchs) and “biofilm”. Some authors prefer to talk about “attached algae”, but this disregards the many other forms that live in periphyton assemblages. Aufwuchs includes all the organisms that are attached to, or move upon, a submerged substrate, but which do not penetrate into it, whereas periphyton refers to the total assemblage of sessile or attached organisms on any substrate (Reid and Wood, 1976; Weitzel, 1979). The difference is in the unattached organisms that are often found in association with the periphyton assemblage. Sometimes, the terms “euperiphyton” (immobile organisms attached to the substrate by means of rhizoids, gelatinous stalks, or other mechanisms) and “pseudoperiphyton” or “metaphyton” (freeliving, mobile forms that creep among or within the periphyton) are used (Weitzel, 1979). The term “biofilm” is preferred in other fields of application, 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 for attached bacteria and protozoa but not algae (O’Toole et al., 2000). Other terms used to indicate periphyton indicate the substrate on which it grows: epiphyton (on
5 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 carried out in lakes, and it was shown that periphyton can have an important share (42.4% for the lake studied) in the total annual production, especially in shallow lakes with large littoral zones (Wetzel, 1964). In five oligotrophic lakes, periphyton contributed 43–97% of the total productivity in the shallow (2–3 m) zone (Loeb et al., 1983). In the littoral zone, periphyton can grow on rocks and sediments but also as epiphyton on macrophytes. In natural, unpolluted streams periphyton density is highest in the mid-waters, where currents are moderate and erosion and deposition are balanced. Nutrients, imported from upstream, are absorbed by periphyton attached in locations with sufficient light for photosynthesis, such as rocks or the stream bed. Upstream, the current is stronger, erosional processes and allochthonous inputs are more important, nutrients are scarce and shredders dominate the food chain. In the lower reaches, the currents are slow and deposition processes are dominant. In this nutrient-rich environment phytoplankton thrives (Welcomme, 1985). An example of this trophic gradient was shown in a study of a grassland stream in New Zealand, where nitrate concentrations increased along a downstream gradient which was reflected in the species composition and biomass of the periphyton (Biggs et al., 1998a, b). The key feature of periphyton in running water environments is its ability to utilize scarce nutrients in a fixed position favourable for photosynthesis. Once trapped, nutrients can be recycled within the periphyton assemblage. A model of periphyton biomass with nutrient concentration and water velocity as main driving variables gave good results when compared to field data from a river in Argentina (Saravia et al., 1998). In marine habitats, periphyton is also found in littoral zones (mangrove forests, estuaries) and on coral reefs. On coral reefs, the accumulation of organic material is facilitated by the combination of a high primary productivity of the attached algae with nitrogen fixing by cyanophytes, the capture of N from the surrounding ocean and the recycling of nutrients within the reef. This explains how a relatively
high fish biomass can be sustained in oligotrophic water. An important part of the primary production is transferred to the coral host in the form of organic exudates. The main limiting factor is the surface area available for photosynthesis by attached primary producers (Longhurst and Pauly, 1987). A range of herbivores, including fish, echinoids, and other invertebrates, graze on coral reef algae. Exclusion experiments with cages have shown that intense grazing by fish or sea urchins leads to reefs with a less diverse (in terms of species), lower algal biomass dominated by the smaller turfs and crustose corallines than ungrazed reefs (Ogden and Lobel, 1978; Hatcher, 1983; Steneck, 1988). Primary productivity in coral reefs is very high, but values probably depend a lot on the part of the reef where the measurement was done (depth, exposure to currents). Algal productivity is generally believed to increase when the standing crop is reduced by grazing, because of reduced self-shading, enhanced nutrient exchange with the water and maintenance of the plants in the exponential growth phase (Ogden and Lobel, 1978; Hatcher, 1983). Brush-park fisheries Brush-park fisheries are practiced in a large number of countries and areas: West Africa, Madagascar, Sri Lanka, Mexico, Bangladesh, Cambodia, China, and Ecuador (Kapetsky, 1981). It is a traditional technology that shares features of both capture fisheries and aquaculture. Research on brush-park fisheries in the United States was done as early as the 1930s (Rodeheffer, 1940; in Pardue, 1973). Current examples are the “katha” fishery in Bangladesh (also called “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 trees such as hizol (Barringtonia sp.), jamboline (Eugenia sp.) or acacia (Streblus sp.). Branches are piled up between a number of bamboo poles fixed in the bottom to maintain the structure and delimit the area of the katha. Kathas are usually built in secondary rivers or canals in floodplain lakes. Water hyacinth may be used to cover the katha. The whole structure can be 6–9 m long, 2–6 m wide and approximately 1.25 m deep. Kathas are usually operated for 5–7 months each year, during which period they are fished 3– 4 times, principally between September and March when water levels recede and the water becomes cool.
6 For fishing, the katha is encircled with a net and all branches are removed. Fishing the whole katha may take several days and usually involves 4–5 persons using scoop nets. Harvests range from 100 to 1000 kg, depending on the size of the katha. Similar fisheries are the “kua” fishery where branches are placed in natural or excavated depressions at the beginning of 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 West African coastal lagoons. An acadja is an artificial reef made of tree branches (mangrove poles or sometimes palm trunks) and installed in water of about 1–1.5 m deep. It attracts fish and is colonized by periphyton which serves as food for the fish. Most important species in the brush-park fisheries of Benin are the blackchin tilapia (Sarotherodon melanotheron, Cichlidae) and bagrid catfish (Chrysichthys nigrodigitatus, Bagridae), but many other species are reported from other countries. After encircling the acadja with a net and removing the branches, the fish are removed, if necessary using traps or baskets. In some areas, fishing is done by hook and line. Apart from attracting fish from outside, fish also reproduce inside the acadja system. Production figures reported are high, from 4–20 t ha−1 y−1 (Welcomme, 1972; Hem and Avit, 1994). Because of their profitability, acadjas proliferated in 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 be beneficial to capture fisheries because fish disperse to adjacent open waters; Welcomme, 1972). There are also negative environmental impacts, such as increased silting in the lagoons due to accelerated sedimentation around the brush-parks, organic pollution caused by the decaying branches in the water, increased erosion as a result of deforested catchment areas and a net export of nutrients in areas of intense acadja harvesting (Durand and Hem, 1996; Weinzierl and Vennemann, 2001). An experiment with the so-called “acadja-enclos” was reported by Hem and Avit (1994). They compared three 625 m2 enclosures in the Ebrié lagoon in Ivory Coast (salinity 0–9): one empty, one with a 100 m2 acadja of Echinochloa pyramidalis (a floating macrophyte), and one with a 100 m2 traditional acadja made of the usual tree branches. Fish recruited to these systems naturally by swimming through the 14-
mm mesh surrounding nets. After 12 months, total biomasses of 11.7, 18.2, and 80.5 kg, respectively were harvested from the three enclosures. Blackchin tilapia was the dominant fish species in the enclosure with tree branches. Subsequent trials with different sizes of acadja-enclos (200–2500 m2 ) yielded on average 1.8 t ha−1 . Because of the high requirements for wood, additional trials with bamboo sticks (10 sticks m−2 , appoximately 6 cm diameter) were done, leading to average yields of 8.3 t ha−1 . The authors expect even higher yields if a scheme of successive selective harvesting would be employed. Similar experiments in Sri Lanka using different mangrove and non-mangrove tree species to construct brush-parks of 4-m diameter resulted in comparable yields (extrapolated: 2.3–12.9 t ha−1 y−1 , assuming 10 productive months per year and depending on substrate species) of mainly green chromide (Etroplus suratensis, Cyprinidae), streaked spinefoot (Siganus javus, Siganidae), dory snapper (Lutjanus fulviflammus; Lutjanidae), prawns (Penaeus spp., Metapenaeus dobsoni and Macrobrachium spp.) and ornamental fish (Costa and Wijeyaratne, 1994). Traditional aquaculture systems in southeast Asia In the Philippines, Indonesia, and Taiwan, the traditional culture system for milkfish (Chanos chanos, Chanidae) in coastal ponds was based on mats of benthic algae, protozoa, and detritus (in the Philippines called “lablab”) stimulated by organic fertilization. In Indonesia, mangrove leaves (notably Avicennia sp.) and twigs were used, whereas in the Philippines green manures or copra slime were applied. Inorganic fertilization was rare. Supplementary feeding with rice straw, rice bran, oil cake, wheat starch, water hyacinth, or other macrophytes was sometimes applied. In the shallow ponds (0.3–0.7 m water depth), a thick mat of algae developed, consisting of cyanobacteria (e.g., Oscillatoria, Lyngbya, Phormidium, Spirulina, Microcoleus, Chroococcus, Gomphosphaeria) and diatoms (e.g., Navicula, Pleurosigma, Nastogloia, Stauroneis, Amphiora, Nitzschia and Gyrosigma). Other benthic flora and fauna as well as filamentous green algae were also ingested. Apart from the target species, about 20% of the harvest in Java could consist of prawns (Huet, 1986). Benitez (1984) distinguished between floating lablab that contained 15% protein (ash-free dry matter basis), and benthic lablab with only 6% protein, and reports an observation by fish farmers
7 that milkfish consuming filamentous green algae had a slower growth rate than fish eating lablab consisting of unicellular algae and diatoms. Nowadays, many of these traditional systems have been replaced by deeper milkfish ponds with higher stocking density and supplemental feeding. Another traditional culture system is rice-fish culture. Rice fields harbour lots of phytoplankton and filamentous higher algae, but studies on rice field ecology do not reveal much about periphyton (Roger, 1996). Not much is known about the natural feeds consumed by fish in these systems. Periphytic detrital aggregate was the most important item in the food of Nile tilapia and common carp in rice fields in northeast Thailand (Chapman and Fernando, 1994). Fish feeding on periphyton on rice plants could be so vigorous that the rice plants were observed to be shaking (Chapman, 1991). Similar observations are reported from rice-fish studies in Vietnam (Rothuis et al., 1999) and in Bangladesh (Gupta et al., 1998). Aquaculture experiments Pardue (1973) reports two experiments from Alabama with bluegill (Lepomis macrochirus, Centrarchidae) grown in plastic circular tanks (stocking density 2 m−2 , 3 m diameter, water volume 5,400 l) equipped with yellow pine boards with surface areas equivalent to 20, 40, 60, 80 and 100% of the tank surface. Fish production increased linearly with increasing surface area, and the highest mean yield with 100% surface area 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 experiment with 40 and 100% additional surface area and three levels of fertilization, there was no difference between the two levels of added surface but a strong effect 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 during the 180 days culture period). The increase in bluegill production was linked to the increase in macroinvertebrates on the substrates, notably Diptera, Hemiptera, Odonata, and Plecoptera. Cohen et al. (1983) added substrates to 200-m2 ponds for freshwater prawn (Macrobrachium rosenbergii) in Israel in an attempt to mimic the natural conditions for prawn growth by increasing the available surface area. The substrates consisted of two horizontal layers of plastic 2-cm mesh nets with corrugated plastic pipes attached to them (8-cm
diameter, 15–20 cm long). Each pond was stocked with 2,000 juvenile prawns (2 g) and 15 common carp (100 g). The ponds were fertilized with chicken manure and a 25% pellet feed was given during the night. Selective harvesting of large prawns was done to prevent suppression of growth caused by territorial behaviour. The total marketable yield from ponds with substrates was 2,850 kg ha−1 in six months, against 2,500 in ponds without substrates. The average final weight of the prawns was also higher with substrates (40.3 g versus 35.8 g). There was no difference in survival. Another set of experiments with Macrobrachium rosenbergii was done at Kentucky State University. In a first experiment, substrates consisting of 3 horizontal levels of plastic mesh sheet, suspended 30 cm apart in a PVC pipe frame were placed in 400 m2 ponds. The substrates increased available surface area by about 20%. The substrates increased the yield of prawns stocked at 0.33 g individual weight and 59,280 individuals ha−1 from 1,060 kg ha−1 (without substrates) to 1,268 kg ha−1 in 106 days. Mean size at harvest was also bigger (37 g against 30 g without substrates) and the number of mature females increased with substrates (Tidwell et al., 1998). In a similar experiment with two stocking densities and substrates that added 80% of available surface area to the ponds, the substrates produced an increase in yield from 1,243 to 1,469 kg ha−1 in 95 days (averages for stocking densities 60,000 and 120,000 ha−1 , size at stocking = 0.24 g) and a decrease in food conversion ratio from 2.9 to 2.4 (Tidwell et al., 1999). In a third experiment, the density of the substrates was varied at a fixed prawn density of 74,000 ha−1 with a stocking weight of 0.24 g. Substrates consisted of 120 cm wide, 7.0×3.5 cm mesh polyethylene panels suspended horizontally across the ponds, 30 cm above the bottom with 30 cm between the layers when multiple layers were installed. Three treatments were created, corresponding to surface area increases of 0, 40 and 80%. There was a positive linear response of yield on substrate density: Y (kg/ha) = 1466.3 + 4.4604 X (% increase in surface). Feed conversion ratio was inversely related to increase in surface area: Y (FCR) = 2.784 − 0.0052 X (% increase in surface). There was no significant difference in individual weight at harvest (Tidwell, 2000). Bender et al. (1989) produced a microbial mat by applying 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 from the microbial layer growing on the grass substrate, a detrital gelatinous deposit developed on the pond sediment. Weight gain of 0.5–3.5 g Nile tilapia in a 2-week growth trial was higher with the silage-microbial mat than with a commercial catfish feed applied at 3% BW day−1 . For the microbial mat to induce fish growth, it had to be offered in the same pond where it was grown. Microbial mats or detrital material grown in one pond and offered to fish in another pond (either with or without sediment) did not induce growth in the fish. It was concluded that the integration of the detrital materials with the biomass is crucial for the productivity of such a system. Phillips et al. (1994) obtained significant differences in final individual weight of Nile tilapia between ponds with and without similar microbial mats, but no data on mortality and total yield were given. At the Asian Institute of Technology in Bangkok, Shrestha and Knud-Hansen (1994) carried out two experiments in concrete tanks (2.5×2×1.1 m) using vertically suspended corrugated plastic sheets (7.7 m2 extra surface area per tank) as substrates with inorganic fertilization (2.1 g N m−2 week−1 ). Sexreversed all-male Nile tilapia were stocked (20 g fish−1 , 3 fish m−2 ) for 56 days. Microscopic examination of gut contents and periphyton, as well as observation of feeding behaviour showed that the fish were feeding on the periphyton. In the first experiment, net fish yields were not significantly different between tanks with and without substrates (1.05 and 0.88 g m−2 d−1 , respectively). Although there was a difference in mean periphyton density between tanks with and without fish (0.78 and 0.93 mg dm cm−2 , respectively), the difference was not statistically significant. The second experiment compared the plastic substrate with a similar surface area of bamboo poles. Fish yield was higher with bamboo poles than with plastic (3.43 and 2.51 g m−2 d−1 , respectively) and on this occasion, there was significantly less periphyton in tanks with fish (0.80 against 1.71 mg dm cm−2 on plastic sheets; 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 the suspended solids (consisting mainly of phytoplankton; ash appr. 20%), with the exception of periphyton on bamboo (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 production. In two preliminary experiments, production of common carp, Mozambique tilapia (Oreochromis mossambicus, Cichlidae) and rohu (Labeo rohita, Cyprinidae) in concrete tanks was 45–50% higher with sugarcane bagasse as a substrate, compared to control tanks without substrates. A subsequent bigger trial compared dried sugarcane bagasse, paddy straw, and dried water hyacinth (Eichhornia sp.) leaves, suspended as 60–90 cm bundles in 25 m2 concrete tanks with soil bottoms. Substrate density was 12.5 kg tank−1 (as the authors stressed the biodegradability of the substrates, substrate density was expressed as mass per surface area) and the tanks were fertilized with cow manure and urea. A mixture of common carp (2.1 g) and rohu (1.5 g) were stocked at 13 and 12 per tank, respectively. The experiment lasted 133 days and on day 70, 7.5 kg of fresh substrates were suspended. Both rohu and common carp grew best in the treatment 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, respectively. In all substrate treatments, fish survival on average was higher than in the control (85.7–93.7%, versus 81.3%). The increased fish production could, in the absence of major differences in dissolved oxygen and ammonia concentrations, be attributed to the periphyton on the substrates, as shown by total plate counts of bacteria in the water and on the substrates, and by phytoplankton and zooplankton enumeration. The superior fish production with bagasse was attributed to its higher fibre content and surface area, favouring better bacterial growth and subsequent fish production than the other two substrates. Zooplankton density in the water of the bagasse treatment was higher than in the other treatments. The authors concluded that biodegradable substrates led to better results than less degradable substrates like bamboo or non-biodegradable substrates like PVC and plastic. Bratvold and Browdy (2001) studied changes in water quality and microbial community activity due to AquaMatsTM substrates (3.4 m2 per m3 tank) added to polyethylene tanks stocked with Litopenaeus vannamei postlarvae. Shrimps were fed with a commercial feed. Compared to tanks with only sand sediment or tanks without sediment, tanks with substrates and sand sediment had a higher pH and higher total photosynthesis, lower abundance of pelagic bacteria and phytoplankton, lower turbidity, lower ammonia and orthophosphate and higher nitrification. Shrimp production was significantly higher
9 (1.69 vs. 0.98–1.07 kg m−2 in 100 days) and food conversion ratio (feed given/shrimp produced) was significantly lower (1.5 vs. 1.9–2.1) in the tanks with substrates compared to the tanks without substrates. Keshavanath et al. (2001b) reported an experiment with different types of substrates for enhancing the production of mahseer (Tor khudree, Cyprinidae). Bamboo poles, PVC pipes and sugarcane bagasse substrates were placed in 25 m2 concrete tanks with mud bottoms and fingerlings of about 3 g were stocked at densities of 1, 1.5, and 2 fish per m2 . After 90 days, the highest net production with bamboo substrate was 447 kg ha−1 at the highest fish density, against 399 kg ha−1 with the PVC pipes. In the bagasse treatment, all fish died due to low oxygen concentrations. In subsequent experiments (Keshavanath et al., 2002) using the same tank systems, the effects of periphyton, supplemental feeding and their combination were investigated using mahseer (3.5 g) or the 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 per 25 m2 ) were compared with tanks without substrates. Periphyton alone and feeding alone led to comparable fish yields that were significantly higher (by 30–75%) than the yields obtained without periphyton or feed. There was a significant effect of substrate density on fish survival in both species. The combination of periphyton and feeding resulted in even higher yield increases (54–87%). The higher substrate density improved yield only slightly without feeding and not at all with feeding, suggesting that at the fish stocking density used the carrying capacity of the periphyton was never exceeded. A similar experiment with red tilapia (Oreochromis mossambicus × O. niloticus hybrid) gave similar results, with even more pronounced differences between tanks with and without substrates. Highest tilapia yields were 1,834 g per 25 m2 without, and 2,142 g per 25 m2 with feeding in 75 days (Keshavanath, unpublished results). Sugarcane bagasse was again used as a substrate in a 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 was 13,104 and 14,842 g per 100 m2 in 180 days without and with feed, respectively, compared to 8,076 g in the control without feed or periphyton (Keshavanath et al., 2001a). At the Bangladesh Agricultural University in Mymensingh, Bangladesh, research on periphyton
started with a series of monoculture experiments in which the performance of several fish species with periphyton was assessed. An experiment in six 75 m2 ponds compared the production of 2.1 g orangefin labeo (Morulius calbasu, Cyprinidae) stocked at 1 m−2 with and without substrates made of “kanchi” (bamboo trimmings). While no differences in water quality were observed, survival (87–90% versus 72– 77%) and fish growth were higher with substrates than without, resulting in a net yield of 713 kg ha−1 versus 399 kg ha−1 in 120 days. These relatively low yields could be explained by the sub-optimal water temperatures that prevailed during the experiment (23.6–32.7 ◦ C) (Wahab et al., 1999). Rohu (10 g at 1 m−2 ) and kuria labeo (Labeo gonius, Cyprinidae; 4 g at 1 m−2 ) were then grown with bamboo substrates at 9 poles m−2 (but leaving the pond perimeter free; total substrate area was about 75 m2 ). Net rohu yield with 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 not significantly different (794 and 788 kg ha−1 , respectively, in 120 days). The kuria labeo were never observed to feed actively on the periphyton whereas rohu could be clearly seen eating the periphyton (Azim et al., 2001a). It was concluded that rohu and orangefin labeo are more suitable candidates for periphytonbased aquaculture than kuria labeo. To utilize the other food sources in the pond (plankton, detritus) as well, polyculture of rohu and catla was investigated. With different stocking ratios and bamboo substrate, the growth and total yields from any 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. The combination of 60% rohu and 40% catla was optimal, resulting in a net yield of 586 kg ha−1 70 d−1 (Azim et al., 2002a). Using this stocking ratio, another trial with and without bamboo substrates was carried out to verify the effect of substrates with this species combination. Survival, growth rate, individual weight at harvest as well as net yield of both rohu and catla, were significantly higher in the ponds with bamboo substrates. In ponds with substrate, not only the net yield of periphyton-feeding rohu was higher (by 160%), but also that of surface-feeding catla (220%). The combined net production of the two species in ponds with substrates was 180% higher (1,652 kg ha−1 90 d−1 on average) than that of control ponds (577 kg ha−1 90 d−1 ). In the same experiment, it was found that the addition of 15% orange-fin labeo to the
10 optimum mix of catla and rohu further increased total production by 40% (2,306 kg ha−1 90 d−1 ) (Azim et al., 2001b). Water treatment with periphyton Some investigators have attempted to use fish and periphyton for removing nutrients from wastewater. The nutrients acccumulated in the periphyton are removed by harvesting the periphyton. This can be done manually or mechanically, but fish can also be used. Drenner et al. (1997) used Mozambique tilapia and central stoneroller (Campostoma anomalum, Cyprinidae) for harvesting periphyton grown in circular tanks fed with mock wastewater treatment plant effluent. Maximum removal rates were 48.4 mg total phosphorous (removed in sediments and fish biomass) per m−2 water surface per day.
Periphyton productivity Development of the periphyton assemblage and species composition Development of a periphyton layer on a clean surface generally starts with the deposition by electrostatic forces of a coating of dissolved organic substances (mainly mucopolysaccharides), to which bacteria are attracted by hydrophobic reactions (Hoagland et al., 1982; Cowling et al., 2000). The presence of freefloating organic micro-particles in eutrophic waters stimulates this process. Bacteria actively attach using mucilaginous strands. This can take a week, but in some studies this was observed within days and even within a matter of hours. It is not clear whether bacterial colonization is a prerequisite for subsequent attachment of other organisms, or what the exact role of the bacteria is in this process (Hoagland et al., 1982). In the days that follow, algae start to grow. Low-profile diatoms appear first, followed by small pennate diatoms, short-stalked and longer stalked species and then by diatoms with rosettes and mucilage pads. In the final stages of development, species of green algae with upright filaments or long strands can grow (Hoagland et al., 1982; Horne and Goldman, 1994). On plants, the periphyton community is attached on gelatinous stalks of algal and bacterial mucus interspersed with deposits of calcium carbonate (Wetzel, 1975).
In their study with grass silage, Bender et al. (1989), using colony counts of nitrogen-fixing bacteria, microscopic identification of species and characterization of chemotactic response on agar plates, showed that a chemotactic response to the lactic and acetic acid in the silage from bacteria in the sediments was the first step in the colonization of the grass substrates. The bacteria bloomed in the water and produced slimy exudates that annealed the mirobes to the silage after which cyanobacteria invaded the substrates and caused a further increase in biomass. Using microprobes, it was shown that within the mat, different heterogeneous micro-environments existed with oxic and anoxic zones. Periphyton organisms have various ways of attaching to the substrate: stalks with sticky ends (e.g. ciliates), sticky capsules (bacteria and bluegreen algae), cushions of filaments (seaweeds, algae and aquatic mosses), muscular suction pads (snails), glue (barnacles) or simply clinging to the substrate (e.g., insect larvae). Attachment to sediment can be achieved by rooting (especially higher plants), rhizoids (seaweeds on corals), and with a muscular foot (clams) (Reid and Wood, 1976). During the development of the periphyton layer, conditions for growth of the various algal species change drastically. As the density of organisms increases, there is more competition for substrate surface area and this affects the composition of the periphyton community. The organisms also compete for carbon dioxide, nutrients and light. This explains the development of the periphyton layer away from the substrate, resulting in something that can be compared to the canopy of a terrestrial forest (Hoagland et al., 1982; Figure 1). Another strategy for ensuring optimal nutrient and light conditions is shown by pennate diatom and cyanobacterial cells that can move around the substrate. They “glide” by excreting a polysaccharide mucilage that sticks to the substrate (diatoms) or by using contractile fibrils in their cell walls (cyanobacteria). In this way, they can move away from areas where light or nutrients have become limiting (Horne and Goldman, 1994). It is probably also a way to escape being covered by sediment deposits (Hutchinson, 1975). Some diatoms remain at the base of the periphyton assemblage throughout its development, withstanding extremely low light conditions, while other species move around the periphyton layer looking for the best conditions available (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 with permission, Botanical Society of America.
Coral reef algae can be classified as “algal turf” (1–10 mm), macroalgae or “fleshy algal pavement” (larger than 10 mm) and “crustose algae” (encrusting noncalcified algae or calcareous, crustose corallines) (Steneck, 1988). The epilithic algal community (EAC) of coral reefs generally consists of a mixture of turf and crustose algae (Klumpp and McKinnon, 1992). Species diversity within the periphyton assemblage can be high. Planas et al. (1989) found on average 41 different species in periphyton on ceramic tiles. Wahab et al. (1999) encountered 12 genera of Bacillariophyceae, 25 of Chlorophycaea, 10 of Cyanophyceae, 4 of Eugleno-
phyceae, 1 of Rhodophyceae and 5 of zooplankton in periphyton, as well as a variety of macrobenthic organisms, notably chironomid larvae on scrap bamboo substrates in fishponds in Bangladesh. Lam and Lei (1999) found 81 algal species in periphyton on glass slides in the Lam Tsuen River, Hong Kong. KonanBrou and Guiral (1994) found 24 species of algae in the periphyton community on bamboo substrates in acadjas in Cote d’Ivoire. Often, one or a few species of algae dominate the assemblage. The EAC of coral reefs is often dominated by filamentous Chlorophytes and Rhodophytes (Klumpp and McKinnon, 1992). On plastic substrates
12 in tilapia cages in Bangladesh, filamentous Chlorophyceae and Myxophyceae dominated the periphyton before fish stocking, whereas after stocking of the fish diatoms became more important. Diatoms could be attached directly to the substrate but were also found as epiphytes on larger filamentous algae. In addition, freshwater oligochaetes, Protozoa, Rotifera, and coelenterate Hydrozoa were observed (Huchette et al., 2000). Dominant species in the periphyton of the acadjas were the filamentous algae Rhizoclonium riparium (Chlorophyceae) and Lyngbia (Cyanobacteria) in the surface layers, and Audouinella daviesii (Rhodophyceae) in the deeper layers. Diatoms of the genera Nitzschia and Melosira grew on the filamentous algae (Guiral et al., 1993; Konan-Brou and Guiral, 1994). In eutrophic Lake Valencia, Venezuela, the basis of the “periphytic detrital aggregate” (PDA) growing on macrophytes (Potamogeton sp.) consisted of filamentous cyanophytes, which were also the dominant phytoplankton in the lake. Diatoms, bacteria, and amorphous detritus were the main components of the periphyton attached to the cyanophyte matrix (Bowen, 1979). The composition, biomass, and productivity of the periphyton community vary with season, year, location, and grazing pressure. On coral reefs, the structure of the community is often different depending on whether it is located on the reef flats, the inner or outer shelf, windward or leeward side, and shallow or deep parts and slopes (Klumpp and McKinnon, 1992). Within a single water body, there can be a considerable overlap in species between phytoplankton and peripyton (Havens et al., 1996). In fishponds in Bangladesh, 23 of the 39 genera found in the periphyton were common to the phytoplankton (Azim et al., 2001a). The algal contribution to the dry matter can be estimated from the ratio of ash free dry matter to pigment, called the autotrophic index (AI, mg ash free dry matter/mg chlorophyll a on a given surface area; APHA, 1998). Huchette et al. (2000) reported that AIs were between 150 and 300 in ungrazed conditions and remained stable around 300 when grazed. Azim et al. (2002b) reported AI values ranging from 189 to 346 in freshwater fertilized ponds without fish, depending on substrate. The values decreased with time, indicating that ash-free dry matter of non-algal origin dominated in young periphyton. In general, 1 mg chlorophyll a is equivalent to 65–85 mg algae (Dempster et al., 1993; APHA, 1998), so more than 50% of the periphyton ash-free dry matter is not of algal origin.
Biomass and productivity Table 2 gives an overview of the standing crop of periphyton found on different substrates in various kinds of natural and culture systems. Because of the wide variation in methods used, environments, and species composition it is difficult to compare the biomass figures directly. The biomasses found in natural systems (streams, lakes, and coral reefs) can be greater than those found in brush-parks and culture systems (tanks and ponds). In a comparison of periphyton biomass in a wide range of natural systems, biomasses of up to 2350 mg m−2 chlorophyll a were reported (Westlake et al., 1980). The main reasons for this are probably the higher fish densities and associated grazing intensity in culture systems, although biomasses in culture systems without fish were still lower than those in, for example, coral reefs. Likely, there is a strong effect of the algal species composition, with especially high biomasses attained by the fleshy macroalgae that make up the algal assemblage on lightly grazed coral reefs. Furthermore, substrate type has a strong effect on the density of periphyton, as shown by the differences between different substrate types in experiments in India and Bangladesh (Azim et al., 2002b; Keshavanath et al., 2001b). Table 3 shows data on periphyton productivity. Again, comparisons are difficult, but the productivity of the acadja systems was the highest (7.9 g C m−2 d−1 ). In this study, not only area-specific but also chlorophyll-specific productivity was higher in periphyton than in phytoplankton (highest contrast measured on one day was 22.5 and 5.9 mg C (mg chla)−1 h−1 for periphyton and phytoplankton, respectively) (Guiral et al., 1993). Coral reefs are also very productive, with net productivity of up to 3 g m−2 d−1 (see Table 3). Productivity measurements were much lower in temperate lakes. An intermediate estimate (±1.7 g C m−2 d−1 ) was made in a pond in Bangladesh (Azim et al., 2002b), based on the periphyton biomass after the first two weeks of colonization on clean bamboo substrates. The other measurements were made using UV-transparent respiration chambers. Effects of environmental factors Nutrients Inorganic nutrients can have a strong effect on periphyton biomass, as shown by numerous enrichment studies in both natural and artificial systems
76.8–397 0.4–33.1 2–100
Sediment X-ray plates
Natural stones Dead reed stems
Glass, sand disk, Active carbon
Water treatment system
70–100
3.3–9.5 19–113 7–18 125–228 60–300a
4.1–167a
2.5–154
132–683 600–1200
Biofilm on biological reactors with layer of substrate, value depending on substrate
Apil´anez et al., 1998
Arfi et al., 1997 Shrestha and Knud-Hansen, 1994 Azim et al., 2002b Keshavanath et al., 2001b, 2002
5 m2 concrete tanks, Asian Institute of Technology, Bangkok 75 m2 fishponds Mymensingh, Bangladesh 25 m2 concrete tanks, Mangalore, India. Higher values without fish
Konan-Brou and Guiral, 1994
Bruggeman, 1995 Hatcher and Larkum, 1983 Klumpp and McKinnon, 1992
Cattaneo, 1987 Meulemans and Heinis, 1983
Lohman et al., 1992 Baffico and Pedrozo, 1996
Izaguirre and Pizarro, 1998 Putz, 1997 Scholz and Boon, 1993
Reference
Depending on depth and location Ebri´e Lagoon, Cote d’Ivoire Depending on depth and salinity/season, Ebri´e Lagoon, Cote d’Ivoire
Depending on algal type, Bonaire (Netherlands Antilles) Macroalgae, Great Barrier Reef Mainly crustose and turf algae, Great Barrier Reef.
Nutrient-poor vs. enriched sites, Northern Ozarks, Missouri (USA) Oligotrophic lake with trout farm, Patagonia, Argentina. Higher values near fish farm 10 lakes of varying trophy, Quebec, Canada Oligo-mesotrophic lake, Netherlands. Low biomass in summer, high in winter
Glacial stream, Antarctica Amazon river, depending on zone Billabong (lentic system), on Eucalyptus camaldulensis
Remarks
a Total pigment (chlorophyll a + pheophyton). b Converted from g carbon by assuming 48% C in afdm.
Plastic sheets Bamboo, kanchi, hizol Bagasse, bamboo, PVC
7.2–25
Bamboo
Culture system
0.2–38
Bamboo
Brush-park
400–700 160–240b
Coral rock Coral rock Coral rock
Coral reef
3–50 5–50
0–48.4 7.1–46 13–42
Lake/reservoir
0.8–20 7–33
Natural stones Cellulose-acetate Wood
Chl-a (mg m−2 )
Stream/river
AFDM (g m−2 )
Substrate type
System type
Table 2. Periphyton biomass (standing crop) in various natural and artificial systems. Biomass is expressed as g ash-free dry matter (AFDM), or as mg chlorophyll a (Chl-a) per m2 of substrate area
13
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 converted to these units assuming 50% C in dm and 12 hours active feeding per day System type Substrate type
River
Net productivity Remarks (g C m−2 d−1 )
Cellulose-acetate 0.082–1.04
Lake
0.02–0.20
Reference
Amazon river, depending on zone
Putz, 1997
Reed stems 0.14–0.72 Debris and plants 0.73
Littoral zone, 5 oligotrophic lakes, California/Nevada Loeb et al., 1983 USA Littoral zone, oligo-mesotrophic lake, Netherlands Meulemans and Heinis, 1983 Whole-lake estimate, large shallow lake Wetzel, 1964
Coral reef
Coral rock Coral rock Coral rock Coral rock Coral rock Coral rock
0.6–1.1 1.79–2.15 1.98–2.00 1.8–3.1 2.16–4.80 0.64–2.00
Great Barrier Reef. Lower on slopes, higher on flats Great Barrier Reef. Damselfish territories Papua New Guinea, turf algae Virgin Islands Several Pacific benthic reef communities Fringing coral reef, Bonaire
Brush-park
Bamboo
7.9
Fishpond
Bamboo
1.7
Fishpond
Grass silage
7.5
Klumpp and McKinnon, 1992 Klumpp and Polunin, 1989 Polunin, 1988 Carpenter, 1986 Marsh, 1976 Van Rooij et al., 1998 Guiral et al., 1993
Estimated from increase in total biomass on clean substrates
(e.g., Aizaki and Sakamoto, 1988; Lohman et al., 1992; Ghosh and Gaur, 1994). Periphyton biomass and productivity can thus be used as indicators of eutrophication in natural waters (e.g., Mattila and Raeisaenen, 1998). In a fertilization experiment in ponds, a quadratic relationship between periphyton biomass and fertilization level was established, with a maximum periphyton biomass (mean biomass over 6 weeks) of 3.3 mg cm−2 dry matter realized with fertilization rates of 4,500, 150, and 150 kg ha−1 of cow manure, urea, and TSP, respectively (equivalent to 1.5 times the standard rate for fishponds in Bangladesh). Phytoplankton biomass increased linearly with increasing fertilization rate up to 2 times the standard rate (Azim et al., 2001c). Investigative studies of nutrient limitation show mixed results. In most freshwater studies, phosphorous was identified as the limiting nutrient (e.g., Ghosh and Gaur, 1994; Vymazal et al., 1994), but nitrogen (Barnese and Schelske, 1994), carbon (Sherman and Fairchild, 1989) and silica can also be limiting, depending on the algal species and on other environmental factors such as hardness and acidity. High Si:P and N:P ratios favoured diatoms, and low N:P and Si:P ratios favoured cyanophytes in a reservoir in Patagonia (Baffico and Pedroso, 1996). Similarly, high Si:N or Si:P ratios favoured diatoms, low
Azim et al., 2002b Bender et al., 1989
N:P ratios favoured cyanophytes and high N:P ratios favoured chlorophytes in periphyton of the Baltic Sea (Sommer, 1996). Whether or not nutrient enrichment stimulates periphyton productivity also depends on the type of substrate. Benthic periphyton has an advantage over phytoplankton because it is closer to the nutrient-rich sediment and the interstitial pore water, or in the case of epiphytes to macrophyte nutrients. In a series of whole-lake experiments, it was shown that periphyton on sediments utilized the nutrients in the sediment pore water and therefore, responded much less to enrichment than periphyton growing on wood in the same lake (Blumenshine et al., 1997). Epilithic algae are more likely to become nutrient-limited because they have to absorb nutrients from the water (SandJensen and Borum, 1991). Lower nutrient concentrations do not necessarily mean lower biomass and productivity. In an experiment with an artificially created upstream-downstream gradient, there were large differences in nutrient concentrations between upstream and downstream parts of the stream, but differences in periphyton biomass were poorly related to gradient. More nutrient recycling took place downstream (Mulholland et al., 1995). Similarly, in a modelling study of nutrient enrichment in seven New Zealand streams, biomass
15 levels in the area studied were lower than predicted using the calibrated model. This was ascribed to differences in other factors such as increased grazing, shading, or differences in substrate characteristics (Welch et al., 1992). Apart from the impact of enrichment on periphyton, periphyton has an effect on the nutrient concentration in the overlying water. Periphyton lowered the phosphorous of the overlying water (Hansson, 1989; Bratvold and Browdy, 2001) and sediment (Hansson, 1989). By lowering the nutrient concentration of the water, periphyton can affect the growth of the phytoplankton, as was shown in a study in Swedish lakes (Hansson, 1990). In aquaculture experiments with periphyton, ammonia concentrations in tanks with periphyton were lower than in control tanks, indicating a stimulating effect of the periphyton on nitrification (Langis et al., 1988; Ramesh et al., 1999; Bratvold and Browdy, 2001). Organic nutrients are also important for the heterotrophic components of the periphyton. The activity of ectoenzymes in a Mediterranean river was higher during periods of high dissolved organic matter concentrations (Romaní and Sabater, 2000). Such enzymes are retained in the periphyton layer by the extracellular polysaccharide matrix (Thompson and Sinsabaugh, 2000). Similarly, the organic load caused by decomposing salmon carcasses led to increased stream periphyton growth (Fisher-Wold and Hershey, 1999). Pulses of highly available carbon created a change in the composition of the biofilm from chemoautotrophic to heterotrophic organisms, and biofilms adapted their metabolism to the prevailing environmental conditions (Battin et al., 1999; Butturini et al., 2000). The algae from the periphyton are important suppliers of organic matter to the heterotrophs. In river biofilms, maximum enzyme activity was seen with an algal biomas that was two to three times as high as the bacterial biomass. Bacteria are likely to utilize the algal exudates and lysis products, as well as photosynthetically produced oxygen, whereas algae utilize the inorganic carbon produced by the heterotrophs (Kuehl et al., 1996; Romaní and Sabater, 2000). Organic matter quality affects the rate at which it is processed, as shown by differences in turnover times between two rivers with different sources of organic matter (Romaní, 2000). Dissolved organic matter may play a role in determining the structure of the periphyton. Periphyton communities treated experimentally with dissolved
organic carbon contained less mucilage than untreated controls (Wetzel et al., 1997). Grazing Grazing is the most important determinant of periphyton biomass. On coral reefs, algal communities can be grazed down completely by fish or echinoids (e.g. Hixon and Brostoff, 1981; Hay, 1981). Exclusion and removal experiments on coral reefs showed that algal standing crop could increase 1.5 to 15-fold when grazers were excluded (Hatcher and Larkum, 1983). Not all components of the periphyton assemblage are equally susceptible to grazing. Diatoms belonging to the overstory of the periphyton layer were removed by 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 algal diversity is lower when grazed (Jacoby, 1987; Horn, 1989; Swamikannu and Hoagland, 1989). Most studies of grazing have been done with invertebrate grazers such as snails and insect larvae while studies with fish are much less common. Huchette et al. (2000) compared the species composition of grazed (four weeks) and ungrazed periphyton communities on plastic substrates in tilapia cages in a Bangladesh river. Four weeks after stocking with fish, the filamentous algae were reduced to short colony lengths and other species such as Ankistrodesmus became more important in the periphyton. Grazing also resulted in a size reduction of epiphytic diatoms. Grazing tilapia preferred the larger-sized diatoms (Melosira spp., Cycotella spp.) as shown by a larger proportion of these species in the stomachs. The fish were not grazing on the periphyton only, as shown by a higher diversity of diatom species in the fish stomachs than in the periphyton and the presence of nanoplankton in the fish stomachs. Grazing resulted in a much lower standing biomass of periphyton than in the ungrazed treatment. Similarly, periphyton biomass was 60% lower on nets in cages stocked with Kariba tilapia (Oreochromis mortimeri, Cichlidae), redbreast tilapia (Tilapia rendalli, Cichlidae) and Nile tilapia than in unstocked cages (Norberg, 1999). However, in a study with redear sunfish (Lepomis microlophus, Centrarchidae) and snails, it was shown that the fish had a positive effect on periphyton biomass by reducing the grazing on the periphyton by snails. Nutrient concentrations in the water were also higher with fish, but this did not affect the periphyton much (McCollum et al., 1998). In streams in the Ozark
16 Mountains (Missouri, USA), stones were covered by cyanobacteria (Calothrix sp.) when exposed to grazing by fish and invertebrates. Once protected from grazing, diatoms would overgrow the cyanobacteria within four to ten days. Grazing minnows could strip the diatom layer in a matter of minutes, after which regeneration of the cyanobacteria happened in 11 days (Power et al., 1988). Predators of grazing fish can also affect the density of periphyton layers, as shown by a study in streams in Panama where bands of high periphyton biomass occurred in the top water layer (
