Effect of algae density on breathing and feeding of filter-feeding silver carp (Hypophthalmichthys molitrix Val.)

    Effect of algae density on breathing and feeding of filter-feeding silver carp (Hypophthalmichthys molitrix Val.) Zhigang Zhao, Shuanglin Dong, Fang Wang, Xiangli Tian, Qinfeng Gao PII: DOI: Reference:

S0044-8486(14)00274-9 doi: 10.1016/j.aquaculture.2014.05.043 AQUA 631203

To appear in:

Aquaculture

Received date: Accepted date:

19 May 2014 30 May 2014

Please cite this article as: Zhao, Zhigang, Dong, Shuanglin, Wang, Fang, Tian, Xiangli, Gao, Qinfeng, Effect of algae density on breathing and feeding of filterfeeding silver carp (Hypophthalmichthys molitrix Val.), Aquaculture (2014), doi: 10.1016/j.aquaculture.2014.05.043

This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

ACCEPTED MANUSCRIPT Effect of algae density on breathing and feeding of filter-feeding

IP

T

silver carp (Hypophthalmichthys molitrix Val.)

a

SC R

Zhigang Zhaoa,b, Shuanglin Donga,, Fang Wanga, Xiangli Tiana, Qinfeng Gaoa,

The Key Laboratory of Mariculture, Ministry of Education, Ocean University of

Heilongjiang Fisheries Research Institute, Chinese Academy of Fishery Sciences,

MA

b

NU

China, Qingdao 266003, People’s Republic of China

TE

*Corresponding author

D

Harbin 150070, People’s Republic of China

CE P

E-mail: [email protected] Tel: +86 532 6678 2697

AC

Fax: +86 532 6678 2799

1

ACCEPTED MANUSCRIPT Abstract The respiratory process of silver carp, a typical filter-feeding fish, works in conjunction with

IP

T

its feeding mechanism when it filters plankton in water. In the present study breathing and feeding

SC R

of silver carp were measured in response to increases of algae density from 0 to 242 mg/L in order to explore the relationship between breathing and feeding in higher algae biomass environments. The results showed that (1) the oxygen consumption rate (VO2) of the fish increased significantly

NU

with increases in algae density (P<0.05), but there were no significant differences in VO2 among

MA

fish at algae densities of 63.3-242 mg/L (P>0.05). The respiratory frequency (fR), gill ventilation (VG) and VG/VO2 of the fish did not show significant differences among algae densities of 0-23.8

D

mg/L (P>0.05). However, when algae density increased to 63.3 mg/L, the fR, VG and VG/VO2

TE

increased significantly and reached a peak, but then declined significantly with further increases in

CE P

algae density (P<0.05). With increases of algae density, oxygen extraction efficiency (EO2) first declined and then increased, with the lowest value occurring at an algae density of 63.9 mg/L. The

AC

EO2 was negatively correlated to VG in the present study (P<0.05). There were no significant differences in respiratory stroke volume (VS.R) among fish at algae densities of 0-242 mg/L (P>0.05). (2) The filtration rate (FR) of silver carp increased significantly with increases of algae density, but did not show significant differences at levels of 63.3-242 mg/L (P>0.05). The changes of the clearance rate (CR) and filtering efficiency (E) of the fish showed the same trend, in which the highest values occurred at algae densities of 63.3 mg/L and 23.8 mg/L, respectively (P<0.05). In addition, an anti-filtering response occurred at algae densities over 138 mg/L. The present studies indicates that in order to acclimate to environments with higher algae biomass, silver carp can actively reduce clearance rate through a decline of filtering efficiency and/or gill ventilation. 2

ACCEPTED MANUSCRIPT

SC R

IP

T

Keywords: silver carp; Hypophthalmichthys molitrix Val.; breathing; feeding; algae densities

1. Introduction

NU

The silver carp (Hypophthalmichthys molitrix Val.) belongs to Cyprinidae,

MA

Cypriniformes, and occurs naturally from Heilongjiang River to Hong Song River in Asia (Li and Wan, 1993). It has received much attention worldwide because of its

D

importance as a worldwide aquaculture species, as well as its potential for the

TE

bio-manipulation of plankton communities, especially in nutrient rich waters where

CE P

blooms occur (Starling, 1993; Fukushima et al., 1999; Xie and Liu, 2001; Tucker, 2006; Ke et al., 2007; Yan et al., 2009).

AC

Like other filter-feeding fish, the silver carp uses gills equipped with gill rakers to feed and respire (Liu et al., 1992; Li and Dong, 1996). It exhibits passive size-selection for food particles in water, but it cannot actively select for its preferred species of plankton which are evenly distributed in the water. However, the silver carp can select feeding areas where there are different plankton species or densities (Dong et al., 1992; Dong and Li, 1994). In large waters, like lakes and reservoirs, phytoplankton species are distributed in certain patterns (Reynolds, 1984), so silver carp in these waters may swim actively to specific areas to feed. Phytoplankton species are distributed evenly in fish farming ponds, especially in those with aeration 3

ACCEPTED MANUSCRIPT facilities. However, phytoplankton communities bloom and collapse frequently in nutrient rich ponds, and as a result, cultured silver carp experience regular

IP

T

phytoplankton density fluctuations.

SC R

The breathing mechanism of silver carp works in conjunction with its feeding mechanism when it filters water containing plankton. Zhao et al. (2011) reported that silver carp can acclimate to lower dissolved oxygen content by regulation of

NU

respiratory and filter-feeding parameters, such as respiratory frequency, oxygen

MA

consumption rate, and gill ventilation. It is of critical importance to know how silver carp acclimate to conditions of high phytoplankton density, and regulate food intake,

D

especially under conditions of low oxygen and high plankton density. In order to

TE

clarify the relationship between respiration and food intake under conditions of higher

CE P

plankton densities, the interaction of breathing and feeding mechanisms were studied in response to different algae densities. The present results are useful for drafting

AC

stocking strategies of silver carp for integrated aquaculture, as well as the bio-manipulation of plankton communities in nutrient rich waters.

2. Materials and methods

2.1. Experimental materials Silver carp (Hypophthalmichthys molitrix Val.) with a body weight of 61.2 ± 8.2 g and a body length of 16.6 ± 0.5 cm were obtained from a fish farm in Qingdao, Shandong Province, P. R. China. Fish were kept in an outdoor pool (15 m × 20 m) for 4

ACCEPTED MANUSCRIPT at least 1 month prior to experiments. During this period, the fish filtered natural plankton in the pool (the main species were Chlorophyta; densities were 20-60 mg/L).

IP

T

The water temperature in the pool was 23 ± 2 °C; pH value was 7.5 ± 0.2.

SC R

Healthy fish from the pool were transferred into a 200 L indoor cylindrical tank for acclimation. During the acclimation period, aeration was provided continuously, and 90% of the water (dechlorinated tap water) in the tank was replaced daily. A

NU

mixture of phytoplankton at a density of 10-20 mg/L was fed daily at 09:00 and 17:00.

MA

The water in the tank was maintained at a temperature of 23.5 ± 0.6 °C. Dissolved oxygen content was maintained above 7.0 mg/L, and the photoperiod was 12L: 12D.

D

The fish were acclimated for 7 days before experiment.

TE

In this experiment, the food organism was Padorina morum (diameter 20.1 ± 4.6

CE P

μm), which was obtained from the Institute of Hydroblology, Chinese Academy of Sciences, Wuhan, P. R. China. P. morum was cultured in SE medium. Phytoplankton

AC

solution of P. morum was filtered through the funken (mesh diameter 9.8 μm) in order to avoid toxicity of the culture medium to the experimental fish. The filtered phytoplankton particles were re-suspended in dechlorinated tap water for later use. 2.2. Experimental methods After acclimation, silver carp were starved for 48 h, and then each fish was transferred to an individual perspex flow-through respiratory chamber (Dong et al., 1992) for parameter measurement. Each fish was acclimatized in the respiratory chamber for at least 5-6 h before measurement, until the respiratory frequency fell to resting level and stabilized. During the acclimation period, clean water without 5

ACCEPTED MANUSCRIPT phytoplankton flowed through the respiratory chamber continuously at approximately 9 L/h (Zhao et al., 2011). The differences between the DO concentrations of the inlet

IP

T

and outlet water of the respiratory chamber were kept at approximately 10-15%

SC R

(Hughes et al., 1983).

The inlet and outlet water of the respiratory chamber were obtained by siphoning into a glass container, following which the DO concentrations (CinO2 and CoutO2,

NU

mg/L) and algae densities were measured. The DO concentrations of inspired (CiO2,

MA

mg/L) and expired (CeO2, mg/L) water, were continuously measured by siphoning water into a glass container from fixed polyethylene catheters (3 mm in inner diameter)

D

anterior to the mouth of the fish and the outlet of opercular cavity of the fish (Zhao et

TE

al., 2011). The catheters were fixed close to the front of the mouth and the outlet of

CE P

opercular cavity of the fish, respectively, but did not affix to the fish. The average flow rate through the respiratory chamber was 9.0 L/h. The respiratory chamber was

AC

covered with black cloth to avoid any visual disturbance to the fish during the measurement. Each fish in the experiment always underwent the same experimental sequence.

After blank samples (without algae in water) were measured, algae densities were increased to 5.88 mg/L, 10.6 mg/L, 23.8 mg/L, 63.9 mg/L, 138 mg/L, and 242 mg/L, respectively. Each experimental algae density was maintained for 40 min before the measurement. There were 12 replicates in the experiment. During the experiment, the water was maintained at a temperature of 23.6 ± 0.3 °C. Because of natural sedimentation of 6

ACCEPTED MANUSCRIPT algae cells, blank samples (without fish) were set up and measured, in order to eliminate systematic error due to sedimentation.

IP

T

DO concentrations were measured with a YSI BOD probe (Model 5010)

SC R

connected to an YSI oxygen meter (Model 5000-230V, YSI Incorporated, Yellow Springs, OH, USA). Algae densities were measured under a microscope using an algae count box, and algae weights were estimated from approximate geometric

NU

volumes of Padorina morum.

MA

2.3. Parameter measurement

Oxygen consumption rate was measured by means of a flow-through

D

respirometry system, concomitantly with the determination of gill ventilation,

TE

respiratory stroke volume, and dissolved oxygen extraction from water according to

CE P

the modification of Fernandes and Rantin (1989). Oxygen consumption rate (VO2, mg/kg/h) was calculated as:

AC

VO2 = VR (CinO2 - CoutO2) / Wt, where VR was the volume flow rate through the respiratory chamber (L/h), and Wt was body weight of the fish (kg). Gill ventilation (VG, L/kg/min) and oxygen extraction efficiency (EO2, %) were calculated as: VG = VO2 / 60 (CiO2 – CeO2) EO2 = 100 (CiO2 – CeO2) / CiO2 Respiratory stroke volume (VS.R, ml/kg/breath) was calculated as: VS.R = 1000 VG/fR, 7

ACCEPTED MANUSCRIPT where fR was respiratory frequency or filtration frequency (breaths/min), which was measured by counting the number of buccal movements of the fish during 5-8 min at

IP

T

each algae density level.

SC R

Filtration rate (FR, mg/kg/h), clearance rate (CR, L/kg/h), and filtering efficiency (E, %) were calculated as:

FR= VR (C in- C out) / Wt (Turker et al., 2003)

NU

CR= VR (C in- C out) / C in Wt (Savina and Pouvreau, 2004)

MA

E=100 CR/ VG

where Cin (mg/L) and Cout (mg/L) were the algae particle concentrations at the inlet

TE

2.4. Statistical analysis

D

and outlet of the respiratory chamber.

CE P

Statistical analyses were performed using SPSS 17.0 for Windows. To analyze possible differences among algae densities, a one-way ANOVA followed by

AC

Duncan’s multiple comparisons test was employed after previous determination of normality and homoscedasticity of the data. Differences were considered significant at the level P<0.05.

3. Results

The breathing and feeding parameters of silver carp at different algae densities are shown in Fig. 1. The respiratory frequency (fR) and gill ventilation (VG) of silver carp in the blank sample (without algae in water) were 42 breaths/min and 1.11 8

ACCEPTED MANUSCRIPT L/kg/min, respectively (Fig. 1-A; Fig. 1-B). With increases of algae density, fR and VG of the fish increased gradually, and reached a peak at an algae density of 63.3

IP

T

mg/L (P<0.05), and then declined significantly with further increase in algae density

SC R

(P<0.05). Oxygen extraction efficiency (EO2) of the fish showed the opposite variation to VG with increasing algae density (Fig. 1-C).

The oxygen consumption rate (VO2) of silver carp in the sample without algae in

NU

the water was 139 mg/kg/h. With increases of algae density, VO2 of the fish increased

MA

significantly (P<0.05), to a level of 192 mg/kg/h at 63.3 mg/L algae density, and then leveled off (Fig. 1-D). There were no significant differences in VO2 among carp

D

subject to algae densities of 63.3-242 mg/L (P>0.05).

TE

The respiratory stroke volume (VS.R) of the fish did not show significant

CE P

differences among algae densities of 0-242 mg/L (P>0.05) (Fig. 1-E). With increasing algae density, the filtration rate (FR) of the fish increased

AC

sharply among 5.88-63.3 mg/L (P<0.05), and then leveled off (Fig. 1-G). The clearance rate (CR) (Fig. 1-H) and filtration efficiency (E) (Fig. 1-I) of the fish increased significantly with increases of algae density (P<0.05), and reached a peak at algae densities of 63.3 mg/L and 23.8 mg/L, respectively, and then declined significantly with further increases in algae density(P<0.05). In addition, silver carp developed an anti-filtering response when algae density approached 138 mg/L. The frequencies of the anti-filtering occurrence were 0.08 times/min at algae density of 138 mg/L, and 0.32 times/min at 242 mg/L, respectively.

9

ACCEPTED MANUSCRIPT 4. Discussion

IP

T

4.1. The effects of algae densities on the feeding of silver carp

SC R

Respiratory frequency (filtration frequency) (fR) and respiratory stroke volume (VS.R) are very important ventilatory parameters of filter-feeding fish. Gill ventilation (VG) as the product of fR and VS.R is used to express the respiratory and filtration

NU

ability of silver carp (Zhao et al., 2011). In the present study, the fR (Fig. 1-A), VS.R

MA

(Fig. 1-E) and VG (Fig. 1-B) of silver carp did not show significant variation with increases of algae density from 0 to 23.8 mg/L, indicating that the filtration ability of

D

the fish was not significantly affected by algae density in lower density environments.

TE

Beyond 23.8 mg/L the fish began to filter actively and filtration reached a peak at 63.3

CE P

mg/L algae density. However, with the further increase of algae density the fish began to filter passively.

AC

With increases of algae density, the filtration rate (FR) of silver carp increased significantly, and leveled off beyond an algae density of 63.3 mg/L (Fig. 1-G). There was a power function relationship between FR of silver carp and algae densities. Experiments conducted by Herodek et al. (1989) and Turker et al. (2003a; b) found similar results with silver carp and tilapia. A description of the physiological process of silver carp filtration is usually as follows: water with food particles is pumped into the oropharyngeal cavity by the rhythmic expansion and contraction of the opercles and buccal chamber; and the suitable food particles are filtered by gill rakers and remain in gill raker ditches while 10

ACCEPTED MANUSCRIPT water flows through the gill rakers; then the food particles reach the pharynx and are swallowed by coordinated movements of filtration organs (Liu et al., 1992; Sun and

IP

T

Meng, 1992; Li and Dong, 1996). With accumulation of algae particles, the gill raker

SC R

meshes of the fish are gradually blocked, eventually hindering water flow through the opercular cavities. In response to this, the algae cells assembling on the gill raker meshes of the fish were frequently expelled from oropharyngeal cavity by means of a

NU

strong cough mechanism, namely, an anti-filtering response (Chen et al., 1990). In the

MA

present study, the filtration response of silver carp became weak after the algae density was over 63.3 mg/L, indicating that silver carp could reduce actively gill

D

ventilation in order to acclimate to higher algae density. However, with further

TE

increases in algae density, the fish could not further regulate algae filtration rate

CE P

through gill ventilation due to respiratory demand. In the present study, the anti-filtering response of the fish developed at algae densities over 138 mg/L, and

AC

resulted in a decline of filtration efficiency (E) (Fig. 1-I) and FR. In fact, the anti-filtering response of the fish is a process that clears the gill raker meshes enabling recovery of their normal filtration function. Therefore, anti-filtering response appears to be an additional acclimation strategy used in response to high plankton density. However, operation of the anti-filtering response likely incurs a higher physiological expense, and leaves less energy available for growth. Clearance rate (CR) is the amount of water in which food particles are cleared completely per minute by silver carp. The changes of CR (Fig. 1-H) of the fish in the present study resulted from the changes of VG and E of the fish, which suggests that 11

ACCEPTED MANUSCRIPT silver carp can moderate CR by reducing VG and E in environments with higher plankton densities.

IP

T

4.2. The effects of algae densities on the respiration of silver carp

SC R

The gas exchange efficiency of fish can be analyzed by the ratio VG/VO2, namely water convection requirement (Dejours, 1981). In the present study, variations of VG/VO2 observed in silver carp were similar to the patterns of VG, with lower values

NU

occurring in environment with higher algae densities (Fig. 1-F). In contrast, the

MA

oxygen extraction efficiency (EO2) of fish showed an opposite trend (Fig. 1-C), and was negatively correlated to VG in the present study (Fig. 2). This suggests that silver

D

carp can improve oxygen extraction efficiency by reducing VG in order to meet

TE

increased oxygen demand in environments of high algae density.

CE P

Results of this study demonstrate that the oxygen consumption rate (VO2) of silver carp increases significantly with increases of algae density (Fig. 1-D). In

AC

addition, respiratory stroke volume (VS.R) of the fish changed little throughout the experiment (Fig. 1-E), suggesting that changes in VG were due to changes of fR.

Acknowledgements This work was financially supported by the National Program on Key Basic Research Project (2009CB118706) and 111 Project of China (B08049).

References 12

ACCEPTED MANUSCRIPT Chen, S.L., Liu, X.F., Hu, C.L., Tian, L., 1990. On the digestion and utilization of microcystis by fingerlings of silver carp and bighead carp. Acta Hydrobiol. Sin. 14 (1), 49-59 (in Chinese

IP

T

with English abstract).

-Holland Biomedical Press, Amsterdam, pp. 265.

SC R

Dejours, P., 1981. Principles of Comparative Respiratory Physiology, 2nd Edition. Elsevier/North

Dong, S.L., Li, D.S, 1994. Comparative studies on the feeding selectivity of silver carp

NU

Hypophthalmichthys molitrix and bighead carp Aristichthys nobilis. J. Fish Biol. 44, 621-626.

MA

Dong, S.L., Li, D.S., Bing, X.W., Shi, Q.F., Wang, F., 1992. Suction volume and filtering efficiency of silver carp (Hypophthalmichthys molitrix Val.) and bighead carp (Aristichthys

D

nobilis Rich.). J. Fish Biol. 41, 833-840.

TE

Fernandes, M.N., Rantin, F.T., 1989. Respiratory responses of Oreochromis niloticus (Pisces,

509-519.

CE P

Cichlidae) to environmental hypoxia under different thermal conditions. J. Fish. Biol. 35,

AC

Fukushima, M., Takamura, N., Sun, L., Nakagawa, M., Matsushige, K. and Xies, P., 1999. Changes in the plankton community following introduction of filter-feeding planktivorous fish. Freshw. Biol. 42, 719-735. Herodek, S., Tatrai, I., Olah, J., Vo¨ro¨s, L., 1989. Feeding experiments with silver carp, Hypophthalmichthys molitrix, fry. Aquaculture 83, 331-344. Hughes, G.M., Albers, C., Muster, D. and Gotz, K.H., 1983. Respiration of the carp, Cyprinus carpio L., at 10 and 20°C and the effects of the hypoxia. J. Fish BioI. 22, 613-628. Ke, Z.X., Xie, P., Guo, L.G., Liu, Y.Q., Yang, H., 2007. In situ study on the control of toxic Microcystis blooms using phytoplanktivorous fish in the subtropical Lake Taihu of China: A 13

ACCEPTED MANUSCRIPT large fish pen experiment. Aquaculture 265, 127-138. Li, D.S., Dong, S.L., 1996. The study of structure and function of the filter organs in silver carp

IP

T

and bighead. Acta Zoological Sinica, 42(1), 10-15 (in Chinese with English abstract).

SC R

Li, S.Z., Fang, F., 1993. On the geographical distribution of the four kinds of pond-cultured carps in china. Acta Zoological Sinica. 36(3), 244-248 (in Chinese with English abstract). Liu, H.L., Li, M.H., Li, L.P., Zhu, W.H., 1992. A study on the biology of post-larval development

NU

of the filtering apparatus in bighead carp (Aristichthys nobilis). Journal of Dalian Fisheries

MA

University. 8(3), 1-19 (in Chinese with English abstract). Reynolds, C.S., 1984. The Ecology of Freshwater Phytoplankton. Cambridge: Cambridge

D

University Press.

TE

Savina, M., Pouvreau, S., 2004. A comparative ecophysiological study of two infaunal

289-306.

CE P

filter-feeding bivalves: Paphia rhomboïdes and Glycymeris glycymeris. Aquaculture 239,

AC

Starling, F.L.R.M., 1993. Control of eutrophication by silver carp, Hypophthalmichthys molitrix, in the tropical Paranoa Reservoir (Brasilia, Brazil): a mesocosm experiment. Hydrobiologia 257, 143-152.

Sun, X.M., Meng, Q.W.,1992. Development and structure of the filter and digestive organs and their relations with the food habits in silver carp and bighead. Journal of Fisheries of China. 16(3), 202-212 (in Chinese with English abstract). Tucker, C.S., 2006. Low- density silver carp Hypophthalmichthys molitrix (valenciennes) polyculture does not prevent cyanobacterial off-flavours in channel catfish lctalurus punctatus (Rafinesque). Aquat. Res. 37, 209-214. 14

ACCEPTED MANUSCRIPT Turker, H., Eversole, A.G., Brune, D.E., 2003a. Filtration of green algae and cyanobacteria by Nile tilapia, Oreochromis niloticus, in the Partitioned Aquaculture System. Aquaculture 213,

IP

T

93-101.

SC R

Turker, H., Eversole, A.G., Brune, D.E., 2003b. Comparative Nile tilapia and silver carp filtration rates of Partitioned Aquaculture System phytoplankton. Aquaculture 220, 449-457. Xie, P., Liu, J.C., 2001. Practical success of biomanipulation using filter-feeding fish to control

NU

cyanobacteria blooms. Sci. World 1, 337-356.

MA

Yan, L.L., Zhang, G.F., Liu, Q.G., Li, J.L., 2009. Optimization of culturing the freshwater pearl mussels, Hyriopsis cumingii with filter feeding Chinese carps (bighead carp and silver carp)

D

by orthogonal array design. Aquaculture 292, 60-66.

TE

Zhao, Z.G., Dong, S.L., Wang, F., Tian, X.L., Gao, Q.F., 2011. The measurements of filtering

CE P

parameters under breathing and feeding of filter-feeding silver carp (Hypophthalmichthys

AC

molitrix Val.). Aquaculture 319, 178-183.

15

ACCEPTED MANUSCRIPT Figure captions Fig. 1 Breathing and feeding parameters of silver carp at different algae densities. Data with

IP

T

different letters means significant difference from others (P<0.05). Values are mean ± S.E. These

SC R

parameters include respiratory frequency (fR, A), gill ventilation (VG, B), oxygen extraction efficiency (EO2, C), oxygen consumption rate (VO2, D), respiratory stroke volume (VS.R, E), water convection requirement (VG/VO2, F), filtration rate (FR, G), clearance rate (CR, H) and filtration

NU

efficiency (E, I).

MA

Fig. 2 The relationship between gill ventilation (VG) and oxygen extraction efficiency

AC

CE P

TE

D

(EO2) of silver carp at different algae densities.

16

NU

SC R

IP

T

ACCEPTED MANUSCRIPT

MA

Fig. 1 Breathing and feeding parameters of silver carp at different algae densities. Data with

D

different letters means significant difference from others (P<0.05). Values are mean ± S.E. These

TE

parameters include respiratory frequency (fR, A), gill ventilation (VG, B), oxygen extraction efficiency (EO2, C), oxygen consumption rate (VO2, D), respiratory stroke volume (VS.R, E), water

CE P

convection requirement (VG/VO2, F), filtration rate (FR, G), clearance rate (CR, H) and filtration

AC

efficiency (E, I).

17

SC R

IP

T

4 3.5 3 2.5 2 1.5 1 0.5 0

y = -0.0114x + 3.4615 (r² = 0.5148, n=84, P<0.05)

0

10

20

NU

VG (L/kg/min)

ACCEPTED MANUSCRIPT

30

40

50

60

MA

EO2 (%)

Fig. 2 The relationship between gill ventilation (VG) and oxygen extraction efficiency

AC

CE P

TE

D

(EO2) of silver carp at different algae densities.

18

ACCEPTED MANUSCRIPT Highlights

SC R

IP

T

The fish can reduce its clearance rate by reducing its gill ventilation etc.

Anti-filtering response of the fish is another adaptation to high plankton

NU

biomass.

MA

It can improve its oxygen extraction efficiency in high algae biomass

AC

CE P

TE

D

environment.

19