Impact of Feeding Activity of Silver Carp on Plankton Removal from a High-Rate Pond Effluent

Nadia Berday,1* Driss Zaoui,1 Abdeljaouad Lamrini2 and Mustapha Abi3

1Department of Biology, Faculty of Sciences, University of Chouaib Doukkali, P.B. 20, El Jadida, Morocco 2Department of Fisheries, Hassan II Agronomic and Veterinary Medicine Institute, P.B. 6202, Rabat Institutes, 10101, Morocco 3National Center of Hydrobiology and Fish-Culture of Azrou, P.B. 11, Azrou, Morocco

The effect of silver carp (Hypophthalmichthys molitrix Val.) feeding activity on the plankton communities in a high-rate pond technology system (HRPTS) effluent was investigated over a period of 100 days. The experiment was conducted at the experimental wastewater treatment plant of the Agronomic and Veterinary Medicine Institute (AVI) of Rabat, Morocco, using a HRPTS in a fish pond receiving the plant effluent. The effluent was highly dominated by phytoplankton (99.95%). Silver carp could survive and grow in the fish pond. Production was 37 kg with a very low mortality rate (12%). The high specific intestine weight (7%) and intake rates of biomass and phytoplankton by silver carp (616 g kg-1 of fish day-1 and 1.6 x 1011 cell kg-1 of fish day-1, respectively) demonstrated the importance of the feeding activity of the fish. Zooplankton intake rates were lower (2 x 107 bodies kg-1 of fish day-1). The high intestine index (3 to 4.3 for fish sizes of 14 to 22 cm) and the dominance of phytoplankton in the gut contents (99.95%) confirmed an omnivorous/ phytoplanctivorous diet. Silver carp were efficient in removing plankton from the HRPTS effluent. The net removal yields of biomass were 285 g m-3 day-1 and 322 g kg-1 of fish day-1, 7 x 1010 algal cells kg-1 of fish day-1 and 8.7 x 107 zooplankton bodies kg-1 of fish day-1, with net removal rates of 47, 64 and 62%, respectively. The total suspended solids concentration decreased from 211 in the inflow to 112 mg L-1 in the fish pond. Key words: silver carp, high-rate pond technology system effluent, plankton removal, food consumption, gut contents

Introduction digestive tracts are adapted to a phytoplanctivorous diet (Cremer and Smitherman 1980; Li 1991; Hampl et al. The wastewater treatment plant of AVI is an experimen- 1983; Bitterlich 1985a; Domaison and Devaux 1999) so tal pilot plant using the high-rate pond technology sys- silver carp could be used to reduce phytoplankton and tem (HRPTS) (El Hafiane et al. 2003). It was built in zooplankton concentration in the HRPTS effluent. 1997 with the goal of obtaining results that could be The aim of this work was to determine the diet of used to design large-scale HRPT plants and that efflu- silver carp in a fish pond receiving a HRPTS effluent and ents could be exploited efficiently for irrigation. The El its impact on plankton removal from the effluent by fol- Attaouia HRPTS project, supported by the USAID and lowing the plankton progress in the fish pond and in the El Attaouia Municipality, treats a mean flow rate of digestive tract of the fish. 700 m3 day-1 of domestic sewage and was carried out in 2002 based on the AVI prototype. Materials and Methods The HRPTS is a very efficient wastewater treatment system (the removal rate of fecal coliforms is 4 logarith- Wastewater Treatment Plant of Agronomic mic units) (El Hafiane 2003). The high phytoplankton and Veterinary Medicine Institute (AVI) production that occurs in this system enhances degradation of organic matter, but the high algal biomass con- The wastewater treatment plant of AVI treats waste- centration in the effluent causes plugging problems when water collected from the AVI campus with a mean flow the effluent is reused in drip irrigation systems. rate of 63 m3 day-1. The system consists of anaerobic Silver carp is the species most used for plankton con- treatment followed by aerobic treatment. The anaero- trol in eutrophic lakes (Leventer and Teltsch 1990; Barry bic system is constituted of two units with two covered and Costa-Pierce 1992). This fish is a versatile omnivo- ponds in series, of a total capacity of 126 m3 and a rous species (Bitterlich and Gnaiger 1984), so it is able to retention time of 1 day. The aerobic system is made up significantly reduce phytoplankton and zooplankton of an algal high-rate pond (AHRP) followed by two (Kajak et al. 1975). The specialized gill apparatus and maturation ponds in series. The AHRP has an area of 960 m2 , a depth of 0.5 m, and a retention time of * Corresponding author; [email protected] 4.6 days. The maturation ponds that receive the AHRP

191

Downloaded from http://iwaponline.com/wqrj/article-pdf/40/2/191/233613/wqrjc0400191.pdf by guest on 28 September 2021 192 Berday et al.

effluent have a total area of 170 m2, a depth of 1 m, and at the inflow and at the downstream part of the fish a total retention time of 1.4 days. The fish pond is situ- pond, at six depths (0, 20, 40, 60, 80 and 100 cm). The ated downstream of the plant and has an area of 26 m2 fish pond bottom samples were collected at the and a depth of 1.2 m. upstream, the downstream and the middle of the fish pond. Sampling of the aforementioned depths and the Fish culture. Fingerlings of silver carp (Hypophthalmich- bottom was done using an aquarium water pump. At the thys molitrix Val.) (582) and grass carp (Ctenopharyn- end of the sampling operation, all samples of the inflow godon idella Val.) (145) of a mean weight of 1 to 3 g were were mixed to obtain an “inflow composite sample” brought from the Carp Culture Plant of Deroua of Beni (inf). All samples collected in the fish pond at different Mellal and introduced in the fish pond in March 2001. depths were mixed to obtain a fish pond composite sam- Grass carp were introduced in the fish pond with the aim ple (p) and all samples of the pond bottom were mixed of reducing development of filamentous Cyanophycae on to obtain a “bottom composite sample.” the pond sides. The fish pond received freshwater during The physical and biological parameters analyses the first 15-day acclimation period, to permit the fish to were completed on the three composite samples. The fol- overcome the stress caused during transport. The pond lowing water parameters were measured: total suspended was treated with green malachite (0.1 g m-3) because the solids (TSS), total biomass, phytoplankton and zooplank- grass carp were infected with Saprolenia during trans- ton. The TSS were determined using a filtration method port. The Saproleniose caused 47% mortality of grass at 105°C using Wathman GF/C filters. The wet weight carp during the first days following fish introduction, (w.w.) of the total biomass (B) was calculated according while the silver carp mortality rate remained very low to the formula B = TSS.100(100-H)-1 where H was the (6%). Then, to adapt the fish to the HRPTS effluent, well relative humidity of algae (H = 93% was determined water was progressively replaced by this effluent during a according to Rodier [1996]). Plankton was identified and second 15-day acclimation period. During the whole counted on an optical microscope (Olympus). The plank- acclimation period, silver carp grew to 13 g while grass ton was determined using the manuals of Bourrely (1966, carp grew to only 2.3 g. 1968, 1970) and Cox (1981). The cells and body counts The experiment was carried out from April to July of phytoplankton and zooplankton were completed using 2001, using 548 and 76 silver and grass carp fingerlings, Thoma and Rosenthal cells, respectively. respectively. The inflow rate of the fish pond (HRPTS Before introducing the fish into the pond, the same effluent) was 4.3 m 3 day-1 from April to June and 9 m 3 parameters were followed fortnightly in the pond without day-1 in July. At night, the fish pond was mechanically fish from January to July 2000 (control pond). The pond aerated to avoid anoxy. The physicochemical character- flow rates were 4.3 m 3 day-1 from January to June and istics of the fish pond are summarized in Table 1. No 9m3 day-1 in July. Sampling and physicobiological analy- supplementary food was applied to the fish pond during ses were completed in the same method as in the fish pond. the study period. Fish sampling. Fish were sampled four times during the Physical and biological parameters analysis of the pond study period one day after water sampling. One hundred water. The fish pond was sampled four times during the silver carp and 40 grass carp were caught in the morning study period from April to July 2000. Water sampling using a fishing net, weighed and measured. Six silver was conducted every two hours between 8:00 and 18:00, carp were retained for digestive tract analysis and the remaining fish were put back in the fish pond.

Silver carp gut content and feces analysis. The fish TABLE 1. Physical, chemical and biological water parameters of the fish pond (mean ± standard error), (number of data = 8) were sacrificed, digestive tracts were removed, weighed and the length of the intestines were measured. The Parameters Influent Fish pond intestines were gutted and their contents were weighed T (°C) 26.2 ± 1.3 26 ± 1 and homogenized in 100 mL of 1% formaldehyde solu- DO (mg/L) 14 ± 3 8.1 ± 1 tion to immobilize the plankton. Feces were collected pH 8.6 ± 0.3 8.3 ± 0.1 using a strainer with a 1-mm mesh and diluted in EC (µS/cm) 999 ± 150 963 ± 100 + 100 mL of 1% formaldehyde solution. The gut contents N-NH4 (mg/L) 14 ± 2 11 ± 2 a and fecal samples were immediately examined using an N-NH3 (mg/L) 10 ± 4.4 3 ± 1 - N-NO2 (mg/L) 1.4 ± 0.4 1.8 ± 0.4 optical microscope. The qualitative and quantitative - N-NO3 (mg/L) 0.1 ± 0.01 0.1 ± 0.01 composition of plankton were determined in the same 3- P-PO4 (mg/L) 1.5 ± 0.4 1.4 ± 0.4 manner as the water samples. TSS (mg/L) 211 ± 40 112 ± 31 Chl-α (mg/L) 0.6 ± 0.2 0.3 ± 0.1 Calculation methods of measurement parameters. The aCalculated according to Emerson et al. (1975). algal species concentration in the samples (cj) is: cj (cell

Downloaded from http://iwaponline.com/wqrj/article-pdf/40/2/191/233613/wqrjc0400191.pdf by guest on 28 September 2021 Plankton Removal by Silver Carp 193

-1 9 L ) = nj 10 /64, where nj is the number of the j species individual weight and length, respectively. The intestine -1 counted on the Thoma cell. index (Iint) is Iint = lint L where lint is the length of the The zooplankton species concentration in the sam- intestine. The specific intestine weight (IWs) is -1 7 -1 ples (cj) is: cj (body L ) = nj 10 /32, where nj is the num- IWs =wint 100 w , where wint is the weight of intestine. ber of the j species counted on the Rosenthal cell. The total abundance of the j species in the gut contents The percentage (relative frequency) of a j species (Fj) (Nintj) is: Nintj = cj vs, where cj is the concentration of the versus total phytoplankton or zooplankton is: Fj = nj j species in the sample and vs (vs = 100 mL) is the sample -1 100N , where nj is the number of cells or bodies of the j volume. The density of the j species versus the body species and N is the number of cells or bodies of total weight of silver carp (Dj) and versus the gut contents -1 -1 phytoplankton or zooplankton. weight (dj) are: Dj (cell or body kg of fish) = Nintj w -1 -1 The biomass (B) or plankton (P) net-removed load and dj (cell or body g of gut contents) = Nintj wint . The in the fish pond per unit of pond volume (NRLv) (daily index of electivity of the j species (Ej) (Ivlev 1961) is: -1 net load of biomass or of plankton removed from the fish Ej =(Fjf - Fjp) 100 (Fjf + Fjp) , where Fjf is the relative fre- 3 -1 pond per m of pond water) is: NRLv = (cinf - cp) fl v , quency of the j species in the digestive tract of silver carp where cinf and cp are the inflow and the fish pond con- and Fjp is the relative frequency of the same species in centrations, respectively, and fl and v are the fish pond the fish pond. inflow rate and volume (v = 31 m3). The B or P net-removal load in the fish pond per unit Results of silver carp load (NRLf) (the daily net load of biomass or plankton removed from the fish pond corresponding to Fish Production -1 a silver carp load of 1 kg) is: NRLf = NRLv vW , where W is the total load of silver carp in the fish pond. The silver carp production results are summarized in The B or P net-removal rate in the fish pond (NRR) Table 2. In 100 days, the production was 37 kg (fish -1 is: RR(%) = (cinf - cp) 100 cinf . taken from the pond are not included), with a daily The mean daily sedimentation rate estimated in the growth rate of 0.6 to 1.8 g weight and 1 to 1.3 mm control pond was approximately 25% of biomass load length. The increase in body weight was 8%. The mean entering the pond (unpublished). The total daily biomass condition factor was equal to 1. The mortality occurred added by plankton multiplication (BPM) in the control on June 3 (12%), as a consequence of a DO decline to pond, mainly due to primary productivity was calculated 1 mg L-1 at night. To avoid this problem, the number of using the equation: silver carp was reduced to 12 fish per m3. The grass carp initial load was highly reduced by B = TBL + TSBL – TBL (1) PM p p inf mortality (47%) due to infection by Saprolenia in the

where TBLp is the total biomass load in the control first days of the acclimation period. The low growth rate pond, TSBLp is the total settled biomass load in the pond and the high mortality rate (46%) during the study and TBLinf is the total inflow biomass load period involved a low increase of the load (0.31 to -1 (BPM = 6.541 kg wet weight of biomass day ) (unpub- 1.9 kg) (Table 3), so it remained negligible toward silver lished). The biomass intake rate by silver carp (BINR) carp load, which represented 96% of total fish load. (the daily load of biomass consumed by silver carp of a -1 load of 1 kg) is: BINR = BNRLf + BPM W . The plank- Biomass Removal in the Control Pond ton intake rate by silver carp (PINR) is: PINR = (PNRLf) -1 BINR BNRLf . The condition factor (Beckman 1948) The biomass of the control pond influent was dominated (CF) is CF = w 105 L-3, where w and L are the silver carp by phytoplankton, with a small amount of zooplankton

TABLE 2. Characteristics of silver carp culture

Period 12/4 15/5 25/5 26/6 21/7 Number of fish 548 538 528 389 379 Load (kg) 7 14 21.1 26.8 43 Mean weight (g) 12.8 26 40 69 113 Weight gain (g/day) — 0.64 1.4 0.91 1.8 Mean size (cm) 10.6 14 15 19 22 Size gain (mm/day) — 1.2 1 1.25 1 Condition factor 1.1 0.95 1.2 1.0 1.1 Mortality rate (%) 0 0 0 12 0 Number of sacrificed fish — 10 10 10 + 65a 10

aFish taken off.

Downloaded from http://iwaponline.com/wqrj/article-pdf/40/2/191/233613/wqrjc0400191.pdf by guest on 28 September 2021 194 Berday et al.

TABLE 3. Characteristics of grass carp culture

Number Load Mean weight Weight gain Mean size Size gain Mortality rate Parameter of fish (kg) (g) (g/day) (cm) (mm/day) (%) Initial 80 0.186 2.3 — 3.2 — — Final 42 1.5 36 0.34 14.6 1.14 46

and organic particles. The main species and groups were pusillum was dominant in May and June, and replaced Micractinium pusillum, ciliates and rotifers. This bio- in dominance by Microcystis in July. Euglena was pre- mass was a great enrichment to the fish pond as a conse- sent only in July and at low concentrations. In the fish quence of plankton multiplication (Table 4). The mud pond, Micractinium was dominant during May and June deposited during the 7 months was 6.5 m3 and there was while Microcystis occurred at equal proportions with frequent flocculation. According to Table 4 and equa- Euglena during July. Other species were present in the tion 1, the mean of the plankton biomass added by inflow or in the fish pond, always at negligible concen- plankton multiplication was 211.3 g m-3 day-1. trations (Scenedesmus, Actinastrum, Navicula, Closteri- opsis, Chlorogonium). The higher removal load yields Biomass Removal in the Fish Pond were noted just for Micractinium and Microcystis (6 × 1010 cell m-3 day-1, 4.4 × 1010 to 9.6 × 1010 cell kg-1 The biomass concentration decreased from 3 g L-1 in the of fish day-1 and 68 to 92%). Zooplankton was mainly inflow to 1.6 g L-1 in the fish pond (Table 5), and in dry represented by ciliates sized 50 to 100 µm in May and weight (TSS) from 211 to 112 mg L-1 (Table 1). This bio- by rotifers sized 200 to 400 µm during June and July mass was dominated by phytoplankton. According to (Table 7). The higher removal load yields occurred in Table 6, it represented 99.95% of total plankton, with May for ciliates and during June and July for rotifers. very low proportions of zooplankton and organic parti- Sediment was absent from the fish pond. Biomass cles. Biomass and plankton concentrations were not cor- and plankton concentrations in the bottom samples were related (p > 0.05). The net load of total biomass removed 1.8 g L-1, 3 × 108 cells L-1 and 105 bodies L-1, respectively. from the fish pond was 285 g m-3 day-1 and 322 g kg-1 of fish day-1, with a removal rate of 47% (Table 5). Silver Carp Intake Rates and Digestive Tract The phytoplankton and zooplankton concentrations and Feces Contents decreased from 6 × 108 cells L-1 and 7.5 × 105 bodies L-1, respectively, in the inflow to 2.6 × 108 cells L-1 and 3 × 105 The biomass intake rate by silver carp usually varied from bodies L-1, respectively, in the fish pond (Table 6). The 388 to 634 g kg-1 of fish day-1 with a mean rate of phytoplankton net load removed from the fish pond was 616gkg-1 of fish day-1 (Table 5). The phytoplankton and 5.6 × 1010 cells m-3 day-1 and 7 × 1010 cells kg-1 of fish day- zooplankton intake rates by silver carp were 1.6 × 1011 cells 1, with a removal rate of 64% but the zooplankton net kg-1 of fish day-1 and 2 × 108 bodies kg-1 of fish day-1, load removed from the fish pond was lower (Table 6). respectively (Table 6). The wet weight and length of the sil- Results of plankton species and removal yields in ver carp digestive tract increased from May to July, with an the fish pond are summarized in Table 7. Phytoplank- increase of intestine index from 3 to 4.3, while the specific ton, which varied in size from 45 to 100 µm, was domi- intestine weight and gut contents biomass decreased from nated by colonial species. In the inflow, Micractinium 9 to 5 and from 85 to 48 g kg-1 of fish weight, respectively

TABLE 4. Biological water parameters in the control pond

Influent concentration Pond concentration Added load Enrichment rate (%) Biomass (ww)a 1.3b 1.9 b 135.5 e 49 Phytoplankton 22 × 107c 33 × 107c 2.5 × 1010f 47 Zooplankton 36 × 104d 86 × 104d 1.13 × 108g 139

aww; Wet weight. bg L-1. ccells L-1. dbodies L-1. eg.m-3 day-1. fcells.m-3 day-1. gbodies.m-3 day-1.

Downloaded from http://iwaponline.com/wqrj/article-pdf/40/2/191/233613/wqrjc0400191.pdf by guest on 28 September 2021 Plankton Removal by Silver Carp 195

TABLE 5. Biomass net removal yields in the fish pond and estimated biomass intake rate by silver carpa

Biomass intake Biomass Biomass net removal yields in the fish pond (ww) b by silver carp Biomass intake Sample Influent conc. Fish pond conc. Removal rate Removed load Removed load rate (ww) (g L-1) (g L-1) (%) (g m-3 d-1) (g kg-1- of fish d-1) (g kg-1 of fish d-1) 15/5 3.3 1.8 45 208 460 927 25/5 2 1 50 139 204 514 26/6 2.1 1.2 45 125 144 388 21/7 4.5 2.2 52 668 482 634 Mean 3 1.6 47 285 322 616

aEstimated biomass produced by plankton multiplication is 211 ww g of biomass m-3 day-1. bww; Wet weight.

(Table 8). The gut contents biomass was dominated by this species of fish can thrive in difficult conditions (such phytoplankton (99.95%), with very low proportions of as this effluent). The concentrations of unionized ammo- zooplankton. A significant amount of organic particles was nia and nitrites, which were higher than the recom- -1 present, but they were difficult to count. Gut contents bio- mended values for safe cultures (0.41 mg L N-NH3 -1 - mass and plankton densities were not correlated (p > 0.05). [Bartone et al. 1988] and 0.03 mg L N-NO2 [Meade Phytoplankton densities were variable and higher than 1989]), were not the primary problem in this system. zooplankton, with a mean of 9 × 107 algal cells g-1 of gut Rather, a possible DO depletion in the early morning due contents and 5.5 × 109 algal cells kg-1 of fish (Table 8). The to heavy biological demand by fish, bacteria and algae, phytoplankton composition change in the gut contents was could compromise this practice. Such is the case of silver the same as in the influent (Table 7). Micractinium was carp mortality on June 3 due to a decrease to 1 mg L-1of dominant during May and June and Microcystis during DO concentration at night, as a result of a high increase July. Ciliates were dominant in May and rotifers during in fish biomass. This system should therefore be care- June and July (Table 7). Daphnia (Cl. Crustaceae) eggs fully monitored and it necessitates rigorous control of were present only in May with a density of 2 × 103 eggs g-1 the fish loading and the mechanical oxygenation at of gut contents. The index of electivity remained very low night. Grass carp production was compromised by the for total phytoplankton (10-3), low or negative for Micrac- initial load being highly reduced by mortalities caused by tinium and Euglena, high for Scenedesmus and Actinas- Saprolenia infection during the acclimation period. The trum, and very low or negative for zooplankton (Table 7). low growth rate of the fish, with a low survival rate dur- The percentage of algal lysed cells in the gut con- ing the study period, showed that it was more sensitive tents was less than 1% for Micractinium and 25% for to the physical and chemical factors of the HRPTS efflu- Scenedesmus and no Euglena lysed cells were observed. ent. Insufficient variety in diet could also be a cause, The percentage of Microcystis partially lysed colonies because the filamentous Cyanophycea were the only was 20%. The percentage of ciliate lysed cells was high plant matter available in the fish pond. (70%), and all rotifers (eggs and bodies) were in a ground state but Daphnia eggs were intact. Biomass Removal Phytoplankton density of silver carp feces was higher than the gut contents (3 × 108 to 7.7 × 109 cells g-1 w.w. Silver carp digestive tracts were largely dominated by feces, dominated by Micractinium in May and June and phytoplankton with very small amounts of ciliates and by Microcystis) in July (Table 9). A small amount of rotifers. This showed that silver carp consumed the bio- Euglena was found in the feces and Scenedesmus was mass available in the fish pond and maintained an absent. Few zooplankton were present in feces, exclu- omnivorous/phytoplanktivorous diet. The similarity in sively represented by ground rotifers and intact Daphnia the plankton composition of the fish pond and silver carp eggs (Table 9). gut contents proved that the fish filtrated and ingested all plankton species available in this effluent (Vyboronov Discussion 1989; Domaison and Devaux 1999). This good retention was facilitated by the large size of the plankton, which Fish Production was sufficient to be retained by the gill (>10 µm) (Cremer and Smitherman 1980; Vörös et al. 1997). This was par- The silver carp in the fish pond receiving HRPTS efflu- ticularly true of Micractinium pusillum which has very ent had a significant survival rate, demonstrating that long silks and rotifers. The most amorphous particles in

Downloaded from http://iwaponline.com/wqrj/article-pdf/40/2/191/233613/wqrjc0400191.pdf by guest on 28 September 2021 196 Berday et al. ) -1 7 7 7 7 7 10 10 10 10 10 × × × × × of fish d -1 40 21 3.6 14.7 24.7 ) (bd kg -1 10 10 10 10 10 10 10 10 10 10 × × × × × of fish d -1 16 9.6 5.8 17.9 30.4 ) (c kg -1 7 7 7 7 7 10 10 10 10 10 × × × × × of fish d -1 15 7.3 9.8 2.7 8.7 ) (bd kg 7 7 7 7 7 -1 d 10 10 10 10 10 -3 × × × × × ) (%) (bd m -1 a bd L 5 (10 e ) -1 3.49 12.17.5 4.2 69 0.78 54 3.1 3.3 63 6.7 62 3.8 6.7 bd L 15.6 6.3 60 13 5 ) (10 -1 10 10 10 10 10 10 10 10 10 10 × × × × × of fish d -1 8.9 3.8 4.4 7.1 11.3 (c kg d 10 10 10 10 10 ) -1 d 10 10 10 10 10 × × × × × -3 57.160.2 4 2.6 5284.6 9.8 6.1 64 5.6 ) (%) (c m 8 8 8 8 8 -1 10 10 10 10 10 c L × × × × × 8 2.2 1.3 6.6 0.4 2.6 (10 8 8 8 8 8 b,c 10 10 10 10 10 ) -1 × × × × × conc. conc. rate load conc. conc. rate load load rate rate Influent Fish pond Removal Removed Removed Influent Fish pond Removal Removed Removed Intake Intake Plankton net removal yields in the fish pond and plankton intake rate by silver carp Conc.; Concentration. d: Day. Phytoplankton relative frequency is 99.95%. c; Cell. bd; Body. TABLE 6. PlanktonGroupSample15/5 (c L 25/526/6 5.1 21/7 3.2 Phytoplankton 13.7 Mean 2.5 a 6.1 b c Plankton net removal yields in the fish pondd e Zooplankton Plankton intake rate by silver carp Phyto- Zoo-

Downloaded from http://iwaponline.com/wqrj/article-pdf/40/2/191/233613/wqrjc0400191.pdf by guest on 28 September 2021 Plankton Removal by Silver Carp 197 (5) (5) (5) (5) 5 7 4 7 10 10 10 10 × × × × (2); 8.9 (2); 7.5 (2); 1.8 (2); 8.4 7 7 4 2 10 11 (2); 100 (5) 10 10 10 × × × × 1.6 0.9 8.1 5 7 7 4 5 Zooplankton community 10 10 10 10 10 × × × × × 2 1.4 silver carp plankton electivity index . 7 6 10 10 × × 2.7 2.9 rog.: Chlorogonium 7 6 10 10 0 0 5.5 × × —— — 4.1 6.2 1.6 2.3 8 7 7 10 10 10 10 10 10 10 × × × × × a,f 2.3 1.9 3.6 6.1 4.4 10 7 7 6 10 10 10 10 10 10 × × × × × 1.2 1.8 -1.9 -1.62 7 9 9 6 10 10 10 10 × × × × 2.2 3.1 4.6 4.2 7 9 9 7 10 10 10 10 0 0 9.1 × × × × 3.5 4.9 7.3 1.3 8 8 7 10 10 10 10 10 10 10 × × × × × 89 13 13 — 99 — — 82 18 (2); 100 (5) Mic. Scen. Actin. Eugl.Actin. Mic. Scen. Clost. Microcy. Chlorog. Ciliates 6.4 9.6 -1 b,c, d -1 of fish d d -1 Plankton species concentrations (C) and net removal yields in the fish pond, plankton densities silver carp gut contents -3 e of gut contents -1 c; Cell. d: Day. Mic.: Micractinium; Scen.: Scenedesmus; Actin.: Actinastrum; Eugl.: Euglena; Microcy.: Microcystis; Clost.: Closteriopsis; Chlo bd; Body. RF; Relative frequency. (1): May-June, (2): May, (3): June, (4): July, (5): June-July. RF (%) 73 12 4 3.1 98.3 12.8 2.7 83 100 (5) TABLE 7. PlanktonSpecies/classInflow C (c/L) RF (%)RF (%) 6.8 (1)Mean removed load (c or bd) kg RF (%) 93 (1) 65 4.8 (1)Index of electivity Phytoplankton community a b c (2; 4) 0.06 3d e f (4)c 1 4.5 (3) 44.7 91 1 (1) 46.5 -0.94 2.4 (2) 0.36 0.68 8 Rotifers 89 -0.49 75 6.8 0.07 100 (5) -0.21 Mean removal rate (%)Mean density (c or bd) 68 7.7 100 83 — 92.3 — — 57 61 (2); 81 (5) Fish pond C (c/L) 2.2 g (c or bd) m

Downloaded from http://iwaponline.com/wqrj/article-pdf/40/2/191/233613/wqrjc0400191.pdf by guest on 28 September 2021 198 Berday et al.

TABLE 8. Silver carp intestine index, specific intestine weight, biomass and densities of plankton digestive tract

Period 15/5 25/5 26/6 21/7 m ± sda

Intestine length (cm) 40 50 73 95 64.5 ± 24.6 Intestine index 3 3.3 3.8 4.3 3.5 ± 0.6 Intestine wet weight (g fish-1) 2.3 2.9 4 5.7 3.75 ±1.7 Specific intestine weight (%) 9 7.3 5.8 5 6.8 ± 1.7 Gut contents biomass (g kg-1 of fish) 85 70.4 55.1 48 64.5 ± 16.5 Phytoplankton density 107 cell g-1 of gut contents 5 9.1 17.6 3.7 9 ± 6.4 Phytoplankton density 109 cell kg-1 of fish 4.2 6.4 9.7 1.7 5.5 ± 3.4 Zooplankton density 104 body g-1 of gut contents 1.3 1.94 1.95 1.54 1.8 ± 0.5 Zooplankton density 105 body kg-1 of fish 11 13.6 10.6 7.4 10.8 ± 2.9

am ± sd; Mean ± standard deviation.

the silver carp digestive tract resulted from digestion biomass, phytoplankton and zooplankton of 1.6 g L-1, because they were less concentrated in the inflow and the 2.6 × 108 cells L-1 and 3 × 105 bodies L-1, respectively. fish pond. Grass carp are not filter-feeding fish, so they The TSS in the fish pond were reduced from 211 to had no effect on plankton intake. Plankton intake by sil- 112 mg of dry weight L-1, but remained largely higher ver carp was the primary factor acting on plankton than the water quality guidelines value of 30 mg L-1 removal in the fish pond. According to the results (Public Law, 95-217 in Mc Donald 1987). The fish pond obtained in the control pond, the biomass added to the should, therefore, be monitored more closely for the pond by plankton multiplication, mainly due to primary increase in fish load, or in the length of retention time productivity, was high (approximately 211 g m-3 day-1) and for the use of adequate techniques to remove fish and was accompanied by an important sedimentation feces from the pond (Opuszynski et al. 1994). The loads and flocculation process. The introduction of silver carp of biomass and plankton removed from the fish pond in the pond prevented mud development and allowed for and silver carp intake rate increased with the increase in the reduction of plankton. Several authors confirmed the the inflow load. The effect of temperature on the change consumption of the deposit by silver carp (Barthelmes of these parameters was not important because its varia- and Jalnichen 1978; Opuszunski 1979; Bitterlich 1985b). tion during the study period was low (26 ± 3ºC). The The settled particles were stirred by fish agitation, so pond flow rate acted indirectly on the removal by influ- could be reused as food by silver carp (Malecha et al. encing the inflow load. The weight of plankton biomass 1981; Bardach 1997). was not correlated to plankton concentration because The significant removal of biomass from the fish the qualitative composition of plankton in the inflow pond (285 g m-3 day-1, 322 g kg-1 of fish day-1 and 47%) and the fish pond (species and size) changed during the was mainly due to the high removal of phytoplankton study period. (5.6 × 1010 cells m-3 day-1, 7 × 1010 cells kg-1 of fish day-1 and 64%). The removal load of zooplankton remained Silver Carp Diet low because of its low amount in the inflow. The very large biomass intake rates by silver carp (616 g kg-1 of The progressive increase in the intestine length and index fish day-1 and 1.6 × 1011 algal cells kg-1 of fish day-1 and were related to fish growth. The intestine index that 2 to 3 times higher than the removed load in the fish reached 4.3 for 22-cm long fish (6 months) tended pond) proved the high grazing capacity of silver carp. towards the value of 6, characterizing two-year-old phy- The difference between removal in the fish pond and the toplanktivorous fish (Bitterlich 1985a). The index silver carp intake rate is due to the process of consump- increase allowed for the increase in intestinal transit time tion being thwarted by plankton multiplication and by a and therefore enhanced the fish digestibility (Bitterlich supply of intact algal cells in silver carp feces. The effect 1985a). The increase in the weight of gut contents during of grass carp defecation processes was negligible because the study period was attributed to the increase of food its load was lower than silver carp. Silver carp biomass intake by silver carp, as a consequence of an improve- intake rate in the fish pond was higher than the values of ment in filtration activity of the fish further to the growth 100 to 200 g kg-1 of fish day-1 reported by Li (1991). of the gill apparatus (Hampl et al. 1983). This related to This difference could be attributed to the high amount of the body growth of the fish, which was particularly biomass available in the fish pond. The plankton important in the fish when at a juvenile stage. The impor- removal by fish resulted in a fish pond concentration of tant specific intestine weight (or gut contents biomass)

Downloaded from http://iwaponline.com/wqrj/article-pdf/40/2/191/233613/wqrjc0400191.pdf by guest on 28 September 2021 Plankton Removal by Silver Carp 199

TABLE 9. Mean density and composition of silver carp fecal planktona

Period From May to June July

Phytoplankton Zooplankton Phytoplankton Zooplankton Plankton (cell g-1 of feces) (body g-1 of feces) (cell g-1 of feces) (body g-1 of feces) Mean density 2.2 × 108 Mic. 2.3 × 103 Rotif 7.68 × 109 Microcys. 5.6 × 104 Rotifers 8 × 107 Actin. 9.2 × 103 Daphnia 2 × 107 Eug. Total 3 × 108 1.15 × 104 7.7 × 109 5.6 × 104 Composition 73% Mic. 80% Daphnia eggs 99.7% Microcys. 100% Rotifers

aMic.; Micractinium, Actin.; Actinastrum, Microcys.; Microcystis.

and growth rate of silver carp (0.64 to 1.8 g day-1) should be confirmed by in vitro digestion testing. The resulted in high feeding activity and good food conver- presence of 25% of Microcystis lysed colonies in the gut sion by the fish. The decrease in specific intestine weight contents proved that this algae was digested by silver during the study period was due to the improvement of carp. Microcystis digestion by silver carp was confirmed food conversion during the fish growth. The gut contents by Vörös et al. (1997), with a digestive efficiency of biomass and plankton density were not correlated for the 33% (Hamada et al. 1983). Vörös et al. (1997) con- same cause as for the fish pond plankton biomass. firmed also a decrease of Euglena biomass of 40% when The low or negative electivity index of phytoplank- incubated with silver carp gut juice, but no lysed cells ton and zooplankton by silver carp indicated that there were found in the gut contents. The percentage of was no selectivity for these two groups and that they Scenedesmus lysed cells in silver carp gut contents was were retained passively by the fish. The most eliminated 25%. However, the lack of this genus in the feces indi- species in the fish pond and the most dominant in the cated that it was well digested by silver carp. The same fish gut contents were the most concentrated in the influ- observation was made by Kajak et al. (1977), with a ent (Micractinium and Microcystis). The fish retained digestive efficiency of 45.7% (Hamada et al. 1983). the higher concentrated species (Sparatu and Gophen The important ciliate lysis that occurred in the gut 1985). Also, there was no selectivity for Micractinium, and their absence in feces indicated that they were well Microcystis or Euglena. The high value of Scenedesmus digested by silver carp. The quasi-totality of rotifers and Actinastrum electivity indices was linked to their were hardly ground and digested by silver carp. Bitter- large size, which permitted good retention by the gill lich and Gnaiger (1984) demonstrated that contact of apparatus. Their low concentration allowed them to dis- rotifers with the intestinal juice caused a fast lyse of appear rapidly from the pond. rotifers. Daphnia eggs were not digested by silver carp, The digestibility of algae by silver carp is a very so the quantity in the feces was high. The increase of important parameter acting on phytoplankton removal plankton density in feces was a consequence of a com- from the HRPTS effluent. It determines the amount and pression of gut contents during intestinal transit. The the quality of feces produced by the fish. Feces constitute feces contribution to the plankton supply in the fish a supply of biomass in the fish pond and contribute to a pond was significant (3 × 108 to 8 × 109 algal cells g-1 of decrease in plankton removal yields. According to Bitter- feces), but Opuszyunski (1994) noted that fecal algae are lich and Gnaiger (1984), the digestibility of algae by sil- in a degradation stage that easily permitted their decom- ver carp is low, because of the lack of a sufficient position by bacteria. amount of cellulase in the fish gut. But the significant algal removal that occurred in the fish pond and the high Conclusion growth rate of silver carp when feeding on the HRPTS effluent biomass (which was highly dominated by phyto- The use of silver carp to reduce plankton in a HRPTS plankton), allowed the authors to conclude that phyto- effluent is an efficient practice, but could be limited by plankton was well used as food by silver carp. This fish unsuitable physical and chemical conditions of the efflu- has specialized pharyngeal teeth (Robison and Buchanan ent, particularly nighttime DO depletion. Therefore, the 1988) that can grind phytoplankton, and a longer fish pond should be monitored carefully. intestinal transit time (8 to 10 h) (Domaison and Devaux The silver carp intake rate reached 616 g of biomass 1999) that leads to an increase in algal digestibility. The kg-1 of fish day-1, 1.6 × 1011 algal cells kg-1 of fish day-1 and low proportions of Micractinium lysed cells in the fish 2.1 × 108 zooplankton bodies kg-1 of fish day-1 and permit- gut could be explained by its high density in the gut ted biomass removal from the HRPTS effluent of 285 g of which diluted lysed cells. Micractinium digestibility biomass m-3 day-1, 322 g of biomass kg-1 of fish day-1 and

Downloaded from http://iwaponline.com/wqrj/article-pdf/40/2/191/233613/wqrjc0400191.pdf by guest on 28 September 2021 200 Berday et al.

47%, with removal yields of phytoplankton of 5.6 × 1010 systématiques. Tome II . Les algues jaunes et brunes cells m-3 day-1, 7 × 1010 cells kg-1 of fish day-1 and 64% and Chrysophycées, Phéophycées, Xanthophycées et removal yields of zooplankton of 6.7 × 107 bodies m-3 Diatomées, Editions N. Boubée et Cie. Paris VI. day-1, 8.7 × 107 bodies kg-1 of fish day-1 and 62%. Bourrely P. 1970. Les algues d’eau douce : Initiation à la systématiques. Tome III. Les algues bleues et rouges, Acknowledgements Les Eugléniens, Péridiniens et Cryptomonadines, Edi- tions N. Boubée et Cie. Paris VI. We present our acknowledgements to the team of Cox FEG. 1981. Protozoa, p. 3–42. In Practical inverte- researchers in the Unit of Treatment and Reuse of Waste- brate zoology, a laboratory manual for the study of the water in Agriculture headed by Professor B. El Hamouri major groups of invertebrates, excluding Protochor- and to Professor M. Shafee of the AVI Institute of Rabat. dates. Blackwell Scientific Publications. We thank the members of the Belgian Technique Cooper- Cremer MC, Smitherman RO. 1980. Food habits and ation, the Hydrobiology and Fish Culture National Cen- growth of silver carp and bighead carp in cages and ter of Azrou and the Water and Forest Direction (Min- ponds. Aquaculture 20:57–64. istry of Agriculture and Rural Development). Domaison I, Devaux J. 1999. Experimental study of the impact of silver carp on plankton communities of References eutrophic Villerst reservoir (France). Aquat. Ecol. 33(2):193–204. Bardach JE. 1997. Sustainable aquaculture: 1. Fish as food El Hafiane RA, El Hamouri B. 2003. Mécanismes d’élimi- and the case for aquaculture. John Wiley and Sons, Inc. nation de l’azote et du phosphore dans un chenal algal p. 1–14. à haut rendement. Revue des Sciences de l’Eau Barry A, Costa P. 1992. Review of the spawning requirements 16:157–172. and feeding ecology of silver carp (Hypophthalmichtithys El Hafiane F. 2003. Une nouvelle approche combinant deux molitrix Val.) and reevaluation of its use in fisheries and systèmes à haut rendement (anaérobie/aérobie) pour aquaculture. Rev. Aquat. Sci. 6(3.4):257–273. l’épuration des eaux usées domestiques. Doctorat es- Barthelmes D, Jahnichen H. 1978. Zur nahrungswahl und Sciences Agronomiques. 127 p. rationsgrosse 3-4 sommriger silberkarpfen. Z. Binnen- Emerson K, Russo RC, Lund RE, Thurston RB. 1975. Aque- fisch. 25. In Bitterlich G. 1985b. The nutrition of stom- ous ammonia equilibrium calculations: effects of pH and achless phytoplanktivorous fish in comparison with temperature. J. Fish. Res. Bd. Canada 32:2379–2383. Tilapia. Hydrobiologia 121:173–179. Hampl A, Jirasek J, Sirotek D. 1983. Growth morphology Bartone CR, Khouri N. 1988. Reuse of treated pond efflu- of the filtering apparatus of silver-carp (Hypoph- ents for fish culture in Lima, Peru, p. 122–130. In Proc. thalmichthys molitrix Val). II. Microscopic anatomy. Internat. Sem. Waste Reclam. Reuse for Aquaculture, Aquaculture 31:153–158. Calcutta, India. Hamada A, Maeda W, Iwazaki J, Kumamaru A. 1983. Con- Beckman W. 1948. The length-weight relationship factors version efficiency of phytoplankton in the growth of sil- for conversion between standard and total lengths and ver carp, Hypophthalmichthys molitrix. Jap. J. Limnol. coefficients of condition for seven Michigan fishes. 44(4):321–328. Trans. Am. Fish. Soc. In Sparatu P, Gophen M. 1985. Ivlev VS. 1961. Experimental ecology of feeding of fish. Yale Feeding behaviour of silver carp (Hypophthalmichthys University Press, New Haven. In Sparatu P, Gophen M. molitrix Val.) and its impact on the food web in Lake 1985. Feeding behaviour of silver carp (Hypoph- Kinneret, Israel. Hydrobiologia 120:53–61. thalmichthys molitrix Val.) and its impact on the food Bitterlich G, Gnaiger E. 1984. Phytoplanktivorous or web in Lake Kinneret, Israel. Hydrobiologia 120:53–61. omnivorous fish, digestibity of zooplankton by silver Kajak Z, Rybak JI, Spodniewska I, Waclawa A, Lipowa G. carp, Hypophthalmichtithys molitrix Val. Aquaculture 1975. Influence of the planktivorous fish (Hypoph- 40:261–263. thalmichthys molitrix Val.) on the plankton and ben- Bitterlich G. 1985a. Digestive enzyme pattern of two stom- thos of the eutrophic lake. Pol. Arch. Hydrobiol. achless filter-feeders, silver carp (Hypophthalmichthys 22(2):301–310. molitrix Val.) and bighead carp (Aristichthys nobilis Kajak Z, Spodniewska I, Wisniewski J. 1977. Studies on Rich). Fish Biol. 27:103–112. food selectivity of silver carp (Hypophthalmichthys Bitterlich G. 1985b. The nutrition of stomachless phyto- molitrix Val.). Ekol. Pol. 25:227–239. planktivorous fish in comparison with Tilapia. Hydro- Leventer H, Teltsch B. 1990. The contribution of silver carp biologia 121:173–179. (Hypophthalmichthys molitrix) to the biological control Bourrely P. 1966. Les algues d’eau douce : Initiation à la of Netofa reservoirs. Hydrobiologia 191:47–55. systématique. Tome I. Les Algues Vertes, Editions N. Li S. 1991. Aquaculture and its role in ecological waste- Boubée et Cie Paris VI. water treatment, p. 228.28. In Etnier C, Guterstam B. Bourrely P. 1968. Les algues d’eau douce : Initiation à la (ed.), Ecological engineering for wastewater treatment.

Downloaded from http://iwaponline.com/wqrj/article-pdf/40/2/191/233613/wqrjc0400191.pdf by guest on 28 September 2021 Plankton Removal by Silver Carp 201

Proceeding of the International Conference at Stensund (ed.), Aquatic plants for water treatment and resource Folk College, Sweden. recovery. Magnolia Publishers, Inc., Orlando, Fla. Malecha SR, Buck DH, Baur RJ, Onizuka DR. 1981. Poly- Robison HW, Buchanan TM. 1988. Fishes of Arkansas. culture of the freshwater prawn, Macrobrachium rosen- The University of Arkansas Press. Fayette Ville. 535 p. bergii, chinese and common carp in ponds enriched with Rodier J. 1996. L’analyse de l’eau : eaux naturelles, eaux swine manure. I. Initial trials. Aquaculture 25:101–116. résiduaires, eaux de mer. 8ème Edition, Dunod, Paris. Meade JW. 1989. Aquaculture management, Vol. 2, p. Sparatu P, Gophen M. 1985. Feeding behaviour of silver 211–229. In Animal production and aquacultural engi- carp (Hypophthalmichthys molitrix Val.) and its neering. CIGR Handbook of Agricultural Engineering. impact on the food web in Lake Kinneret, Israel. CIGR-The International Commission of Agricultural Hydrobiologia 120:53–61. Engineering. Van Nostrand Reinhold, New York. Vörös L, Oldal I, Présing M, Balogh KV. 1997. Size selec- Opuszyunski K. 1979. Silver carp (Hypophthalmichthys tive filtration and taxon-specific digestion of plankton molitrix Val.), in carp ponds. III. Influence on ecosys- algae by silver carp Hypopphthalmichthys molitrix. tem. Ekol. Pol. 27:117–133. Hydrobiologia 342/343:223–228. Opuszynski K, Shireman JV, Opuszynski W. 1994. Feces col- Vyboronov AA. 1989. Effects of silver carp (Hypoph- lection of filter-feeding fish as a method for wastewater thalmichthys molitrix Val.) on production indices of treatment and enhancement of aquaculture/agriculture phyto- and zooplankton under experimental condi- production. Pol. Arch. Hydrobiol. 41(1):103–108. tions. Voprosy Ikhtiologii 5:874–887. Public Law 95–217 in Donald ME. 1987. Biological removal of nutrients from wastewater. An algal-fish system mode, p. 959–968. In Reddy KR, Smith WH Received: January 19, 2004; accepted: February 1, 2005.

Downloaded from http://iwaponline.com/wqrj/article-pdf/40/2/191/233613/wqrjc0400191.pdf by guest on 28 September 2021