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5 FiguresPrey species and size choice of the molluscivorous fish, black carp (Mylopharyngodon piceus)
Abstract
The black carp, Mylopharyngodon piceus, is used for biological control of freshwater mollusks in various parts of the World. Fish-borne zoonotic trematodes (FZTs) are a public health concern in Vietnam and we suggest using black carp in nursery ponds, which are important for FZT transmission, to control snails serving as first intermediate hosts. However, the use of large juvenile (>2 kg) black carp in nursery ponds could be problematic and we decided to determine consumption rates by black carp of various sizes and their choice of different sizes of selected snail species found in aquaculture ponds in northern Vietnam. Furthermore, shell strength of common snails was assessed. Average daily consumption as percentage of fish weight ranged from 8.12% for smaller fish (100–250 g) to 4.68% in the larger fish (610–1250 g). Bithynia fuchsiana, the intermediate host of Clonorchis sinensis, and some intestinal trematodes were readily consumed by even the smallest black carp tested. The proportion of Melanoides tuberculata, an important host for intestinal trematodes, declined with an increase in its shell height. The same was observed for two viviparid snail species, Angulyagra polyzonata and Sinotaia aeruginosa; these species do not serve as first intermediate host for FZTs. Small black carp (100–250 g) consumed 50.4% of the second largest size class (26–30 mm) and 19% of the largest size class (>30 mm), while medium-sized black carp consumed 49.6% of the largest M. tuberculata and almost all snails of other size classes. Large black carp consumed 75% of the largest size class (>30 mm) of M. tuberculata. Crush resistance (loge-transformed) increased linearly with shell size (loge-transformed) in most species tested. Crush resistance was the lowest in B. fuchsiana, while there was an overlap between M. tuberculata and the viviparid snails. We concluded that black carp of smaller size preferentially fed on M. tuberculata.
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Prey species and size choice of
the molluscivorous fish, black carp
(Mylopharyngodon piceus)
N. M. Hung a , J. R. Stauffer b & H. Madsen c
a Department of Parasitology , Institute of Ecology and Biological
Resources, Vietnam Academy of Science and Technology , Hanoi ,
Vietnam
b Ecosystem Science and Management , The Pennsylvania State
University , University Park, PA , USA
c Centre for Health Research and Development, Department
of Veterinary Disease Biology, Faculty of Health and Medical
Sciences , University of Copenhagen , Thorvaldsensvej 57,
Frederiksberg C , 1871 , Denmark
Published online: 13 Jun 2013.
To cite this article: N. M. Hung , J. R. Stauffer & H. Madsen (2013) Prey species and size choice of
the molluscivorous fish, black carp (Mylopharyngodon piceus), Journal of Freshwater Ecology, 28:4,
547-560, DOI: 10.1080/02705060.2013.800826
To link to this article: http://dx.doi.org/10.1080/02705060.2013.800826
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Prey species and size choice of the molluscivorous fish, black carp
(Mylopharyngodon piceus)
N.M. Hung
a
*, J.R. Stauffer,
b
and H. Madsen
c
a
Department of Parasitology, Institute of Ecology and Biological Resources, Vietnam Academy of
Science and Technology, Hanoi, Vietnam;
b
Ecosystem Science and Management, The Pennsylvania
State University, University Park, PA, USA;
c
Centre for Health Research and Development,
Department of Veterinary Disease Biology, Faculty of Health and Medical Sciences, University of
Copenhagen, Thorvaldsensvej 57, 1871 Frederiksberg C, Denmark
(Received 5 December 2012; final version received 31 March 2013)
The black carp, Mylopharyngodon piceus, is used for biological control of freshwater
mollusks in various parts of the World. Fish-borne zoonotic trematodes (FZTs) are a
public health concern in Vietnam and we suggest using black carp in nursery ponds,
which are important for FZT transmission, to control snails serving as first intermedi-
ate hosts. However, the use of large juvenile (>2 kg) black carp in nursery ponds
could be problematic and we decided to determine consumption rates by black carp of
various sizes and their choice of different sizes of selected snail species found in aqua-
culture ponds in northern Vietnam. Furthermore, shell strength of common snails was
assessed. Average daily consumption as percentage of fish weight ranged from 8.12%
for smaller fish (100–250 g) to 4.68% in the larger fish (610–1250 g). Bithynia fuchsi-
ana, the intermediate host of Clonorchis sinensis, and some intestinal trematodes were
readily consumed by even the smallest black carp tested. The proportion of
Melanoides tuberculata, an important host for intestinal trematodes, declined with an
increase in its shell height. The same was observed for two viviparid snail species,
Angulyagra polyzonata and Sinotaia aeruginosa; these species do not serve as first
intermediate host for FZTs. Small black carp (100–250 g) consumed 50.4% of the
second largest size class (26–30 mm) and 19% of the largest size class (>30 mm),
while medium-sized black carp consumed 49.6% of the largest M. tuberculata and
almost all snails of other size classes. Large black carp consumed 75% of the largest
size class (>30 mm) of M. tuberculata. Crush resistance (log
e
-transformed) increased
linearly with shell size (log
e
-transformed) in most species tested. Crush resistance was
the lowest in B. fuchsiana, while there was an overlap between M. tuberculata and the
viviparid snails. We concluded that black carp of smaller size preferentially fed on
M. tuberculata.
Keywords: fish-borne zoonotic trematodes; biological control; intermediate host
snails; crushing resistance; Red River delta
Introduction
Fish-borne zoonotic trematodes (FZT) are an important human health concern in areas
where eating raw or undercooked fish is common (Rim et al. 1994;WHO1995; Chai
et al. 2005; Taylor et al. 2007). Trematodes, particularly intestinal trematodes of family
Heterophyidae, but also to some extent liver trematodes (Opisthorchis viverrini Stiles &
Hassall, 1896 and Clonorchis sinensis Looss, 1907) of family Opisthorchiidae, may be
*Corresponding author: Email: hung_iebr@yahoo.com or nmhung@iebr.ac.vn
Ó2013 Taylor & Francis
Journal of Freshwater Ecology, 2013
Vol. 28, No. 4, 547–560, http://dx.doi.org/10.1080/02705060.2013.800826
Downloaded by [Copenhagen University Library] at 10:17 12 December 2013
found in aquaculture ponds in Vietnam (Le 2000;De2004; Dung et al. 2007; Phan et al.
2010a) where eating raw fish is a common practice (Chi et al. 2009; Phan et al. 2011).
Dung et al. (2007) found from fecal examination that 64.9% of the adult people in Nam
Dinh were positive for small trematode eggs (Heterophyidae and Opisthorchiidae) and
expulsion of adult trematodes from 33 people with high egg counts (>1000 eggs/g feces)
showed that 51.5% were infected with C. sinensis.
One way to control trematode infections is to reduce intermediate host snail abundance
(Madsen et al. 2011). Chemical control of these freshwater snails is not really feasible in
aquaculture installations since most chemicals that are toxic to snails (molluscicides) also
are toxic to fishes (Hoffman 1970; Calumpang et al. 1995). Pond management, such as
regular mud removal, may reduce density of the intermediate hosts, but this may not be
enough to prevent transmission (Clausen et al. 2012a). Biological control of snails, how-
ever, may be a viable option and in northern Vietnam (Red River delta) many fish farmers
already use the black carp, Mylopharyngodon piceus (Richardson, 1846) for snail control
in grow-out ponds. Generally, one-to-two specimens of black carp are released in ponds of
a size of 300–400 m
2
where various other carp species are primarily cultured. The black
carp feeds almost exclusively on gastropods and bivalves (Nico et al. 2005). Also, at
harvesting the black carp, which is a valued species for human consumption, may be
consumed or they may be transferred to other ponds. Little information, however, is
available on snail species and size selection by different sizes of the black carp; fish ponds
may harbor several species of snails and only some of them serve as intermediate hosts for
FZTs. Controlling these snails may also benefit the production of juvenile fishes as the
metacercariae of FZTs may harm fishes.
Black carp is one of the large Chinese carps and has been introduced and used for the
control of freshwater snails in different parts of the World (Venable et al. 2000; Ben-Ami
and Heller 2001; Ledford and Kelly 2006). Black carp were used to control Pomacea
canaliculata (Lamarck, 1819), which damages rice plants in Taiwan (Mochida 1991). In
the United States, the trematodes, Bolbophorus confusus Dubois, 1935 and Centrocestus
formosanus Nishigori, 1924 cause serious losses in catfish culture, and black carp is
used successfully to control the first intermediate host snails of these trematode species,
for example, Planorbella trivolvis (Say, 1817) (Venable et al. 2000; Ledford and Kelly
2006). Black carp may feed on commercial catfish feed and this may reduce its consump-
tion of snails but its effectiveness as a biological control of ramshorn snails was not
affected (Ledford and Kelly 2006).
Using black carp for snail control was the most cost-effective strategy in hybrid
striped bass farms compared to no snail control, chemical control with hydrated lime or
copper sulfate, and biological control with redear sunfish, Lepomis microlophus (G€
unther,
1859) (Wui and Engle 2007). In Israel, black carp has been used in reservoirs and canals
to control Melanoides tuberculata (M€
uller, 1774) and Physella acuta (Draparnaud,
1805), which can block filters and pipes and thus reducing water flow (Shelton et al.
1995; Ben-Ami and Heller 2001). The major concern about using black carp outside its
natural distribution is its potential spread to large rivers, where it may establish popula-
tions with potential severe effect on native mollusk populations (Nico et al. 2005; Wui
and Engle 2007).
Its natural distribution is the largest rivers in Eastern China and Russia. The Red River
in Vietnam marks its southern distribution, although its presence may be the result of an
early introduction (Nico et al. 2005). These fish are capable of feeding on mollusks from
an early developmental stage. Larva and juvenile fish consume a variety of soft food
items, but as soon as pharyngeal teeth are formed they start to feed on hard food such as
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small snails and bivalves; moreover, mature individuals (from about 6 kg) feed exclu-
sively on mollusks (Nico et al. 2005).
The intermediate hosts of the FZT include species of Thiaridae, Bithyniidae, and
Stenothyridae (Dung et al. 2010). The species of Thiaridae (intermediate hosts of intesti-
nal trematodes), including M. tuberculata,Thiara scabra (M€
uller, 1774), Tarebia grani-
fera (Lamarck, 1822), and Sermyla riquetti (Grateloup, 1840) are commonly found in
aquaculture ponds. The species of Bithyniidae are the main hosts for the liver trematode,
C. sinensis in this area but are not commonly found in aquaculture ponds (Dung et al.
2010). Other snail species commonly found in aquaculture ponds include species of
Viviparidae, primarily Angulyagra polyzonata (Frauenfeld, 1862) and sometimes Sino-
taia aeruginosa (Reeve, 1863), but these seem to play no role in transmission of FZT
(Dung et al. 2010). Since the black carp is also a valued species for human consumption,
farmers who use black carp may also provide snails collected from outside the pond as
feed for the black carp; thus black carp maintenance could potentially also become a risk
factor for FZT transmission if the snails collected as feed for black carp from outside the
ponds would include intermediate host snails. Infection levels with FZT in intermediate
hosts collected from small canals and rice fields were high, that is, 15.4% and 6.2%,
respectively, for thiarid snails (Dung et al. 2010).
The transmission of FZT to fish is intense in nursery ponds (Thien et al. 2009; Phan
et al. 2010b), and this seems to be partly linked to favorable conditions for snails in these
ponds (Dung et al. 2010). Nursery ponds are stocked with fry (mainly carp species) from
commercial hatcheries about 1 week after hatching and they will be kept in the pond for
about 9 weeks (the normal duration of a nursing cycle) when the juvenile fish will be sold
to for growth in a potentially large upland. During this period, the prevalence of infection
with FZT may reach more than 80% (Clausen et al. 2012a).
Using black carp in these ponds could be problematic because the fry that it should
protect from infection are of very small size (15–20 mm when stocked); large juvenile
specimens (>2 kg) might affect pond conditions, for example, by suspension of bottom
sediment as a result of its feeding; furthermore, small-sized black carp (<250 g) might
not be able to feed on the intermediate host snails but would focus on juvenile specimens
of the Viviparidae which have relatively fragile shells. Hung (2013) showed that black
carp are not likely to feed on fry raised in nursery ponds, but the question is whether small
black carp can control populations of the FZT intermediate hosts. Some farmers actually
produce A. polyzonata in their ponds; large specimens can be collected and sold for
human food when ponds are emptied before introducing a new fish stock.
The purpose of this study was to assess species and size preferences among the snail
species commonly found in aquaculture ponds in northern Vietnam by black carp of vari-
ous sizes. These findings are then viewed in relation to the crush resistance of the snails.
Methods
The specimens of black carp were purchased from farmers in Tu Son town. The fish were
grouped into three size classes based on their weight and fork length: large (610–1250 g;
320–455 mm), medium (260–600 g; 210–370 mm), and small (100–250 g; 155–
220 mm). Prior to the trials, 40 individuals of each size class were maintained separately
in enclosures (3 31.4 m). The enclosures were made of nylon net with a mesh size
of 1 1 mm at the bottom and of 2 2 mm around the sides to permit water circulation.
They were fixed in the pond bottom to ensure that the enclosures would always be
extended. Water level was maintained at 0.8 m inside the enclosure. Snails of different
Journal of Freshwater Ecology 549
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species and sizes collected nearby were supplied as food for the black carp at a rate of
10% of their body weight per day; this amount is close to satiation level (Nico et al.
2005).
Tank experiment
Three cement tanks (1.2 31.4 m, W LH) were used for this experiment.
Water level in the tanks was kept at 1.2 m, and water was constantly aerated and recir-
culated through a filter system at a rate of 0.5 m
3
/hour. The filter contained a net (mesh
size 0.5 0.5 mm), and water filtered through foam rubber and sand before returning
to the tank. One specimen (either large, medium, or small) of black carp was released in
each tank 24 hours before the trial started. After this period, 50 specimens of thiarid
snails (mainly M. tuberculata and a few T. scabra) and 30 specimens of viviparid snails
(mainly A. polyzonata and a few S. aeruginosa) of various sizes were introduced every
second day for 2 weeks. The trial was repeated three times. The total weight of snails
introduced in each tank and the total weight of live snails at termination of experiment
were recorded.
Prey size selection experiment
Eight glass tanks (0.6 0.4 0.45 m) were prepared for experiments with well water to
a level of 0.4 m and constant aeration. Twenty-four hours before snails were introduced,
black carp of different sizes were introduced to the aquaria, one specimen in each aquar-
ium, and each size class of black carp was represented by two to three aquaria. A black
carp specimen was used in only one trial. Snails were collected the same day as used
in the experiment from canals in the neighborhood and included Bithynia fuchsiana
(Moellendorff, 1888), M. tuberculata,S. aeruginosa, and A. polyzonata.
Snails were grouped into six size classes (<10 mm, 10–15 mm, 16–20 mm, 21–25 mm,
26–30 mm, and >30 mm) on the basis of shell height. For B. fuchsiana and M. tuberculata,
50 specimens representing as much of the size variation as possible were introduced in
each aquarium. Due to the availability, all size classes could not be equally represented in
each repeat trial. For A. polyzonata and S. aeruginosa, only 30 specimens were used per
aquarium. For M. tuberculata, the trial was repeated eight times, for A. polyzonata five
times, while for B. fuchsiana and S. aeruginosa it was done only once (i.e., eight aquaria).
After 24 hours, the number of live snails of each class was counted. In a separate but other-
wise similar trial, the two viviparid snail species were tested together in the same aquaria.
This experiment was repeated five times.
Crushing study
Crush resistance was measured as described by Brodersen et al. (2003) by placing snails
with the aperture facing down on a glass plate underneath a plexiglass cylinder closed at
the bottom with a glass plate. This procedure ensured that force was applied to snails
against their minimal dimension (Evers et al. 2011). For crushing, we used two cylinders
of different sizes; one for small or fragile snails (diameter 42 mm, height 500 mm, weight
427 g) and one for large and strong shells (diameter 85 mm, height 1200 mm, weight
2723 g). Before the actual experiment started, we estimated the approximate crush resis-
tance of larger shells because the tube for larger shells had to be preloaded with extra
weight to create the necessary crush weight. Sand was slowly poured into the tube until
550 N. Hung et al.
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the snail shell crushed. The weight of the tube, additional weights, and sand were deter-
mined to the nearest 2 g using an electrical balance. The snails selected represented as
much of the size variation as possible for each species.
The snail species used in the crushing resistance study were the most common species
in fish ponds and rice fields (Figure 1) and included M. tuberculata,T. scabra,T. grani-
fera,S. riquetti,A. polyzonata,S. aeruginosa, and B. fuchsiana. Snails were collected
from different rice fields, small canals, or ponds in Nam Dinh, Hanoi, and Bac Ninh prov-
inces and were preserved in 70% ethanol. Shell height and shell diameter were measured
for each shell to the nearest 0.01 mm using an electronic caliper.
Statistical analysis
Survival of snails was compared between treatments using logistic regression with data
arranged in binomial form using a generalized linear model with a logit link function. All
standard errors were adjusted for clustering within an aquarium. Consumption of snails in
the tank experiment was related to fish size using linear regression, and similarly, crush
resistance (log
e
-transformed) was related to either shell height or shell diameter (both
log
e
-transformed) using linear regression. Comparisons of regression lines among species
or families were done using analysis of covariance. All analyses were done in STATA 12
and the differences with probability values below 0.05 were considered significant.
Results
Tank experiment
The proportion of snails consumed by black carp was positively related to fish size
(Figure 2a). Small black carp consumed more than 50% of the snails released, while large
black carp consumed almost 100%. The average daily consumption as percentage of initial
fish weight throughout the experiment ranged from 8.12% for smaller fish to 4.68% in the
larger fish. Consumption decreased as fish size increased but this trend was not significant.
Figure 1. The snail species mentioned in this study. Bithynia fuchsiana and Parafossarulus man-
chouricus are important hosts for Clonorchis sinensis. Melanoides tuberculata,Sermyla riquetti,
Thiara scabra, and Tarebia granifera are hosts for some intestinal trematode species. Angulyagra
polyzonata and Sinotaia aeruginosa are not hosts of these trematodes but are common in aquacul-
ture ponds.
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Figure 2. (a) Consumption as proportion of weight of snails added (y¼0.00052 weight þ
0.4080; r
2
¼0.572; p<0.05); and (b) daily consumption as percent of fish weight (y¼0.00419
weight þ9.0022; r
2
¼0.2247; pnot significant) by individual black carp (n¼9) in cement tanks
over 14 days.
552 N. Hung et al.
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This is probably because larger fish were food limited in these trials (Figure 2b). The pro-
portion of viviparid snails consumed was linearly related to fish weight (Figure 3), while
this was not the case for thiarid snails; thus the smaller fish fed relatively more on thiarid
snails than did the larger fish.
Prey selection
The characteristics of the black carp used in this trial are summarized in Table 1and the
overall consumption of snails of the various species and size classes is summarized in
Table 2. All B. fuchsiana specimens were consumed while the proportion consumed of
the other three species, M. tuberculata,A. polyzonata, and S. aeruginosa declined with
increase in size (Table 2). Some of the size classes for these three snail species were
poorly represented, and therefore, were pooled with the adjoining size class for the subse-
quent analysis. The snail consumption by the three sizes of black carp is shown by snail
size class in Figure 4.
Small black carp consumed 91.6% of the smallest M. tuberculata specimens (11–
15 mm); they consumed 50.4% of M. tuberculata in the second largest size class (26–
30 mm) and 19% of the largest size class. For medium-sized black carp, 49.6% of the
largest M. tuberculata size class was consumed, while most of the snails in the other size
classes were consumed. The ‘large’ black carp used with M. tuberculata were smaller
than those used for viviparid snails, yet they consumed 75% of the largest size class
(>30 mm). Logistic regression showed that the odds of M. tuberculata being consumed
compared to this group declined with an increase in snail class (p<0.001), while
Figure 3. Consumption as proportion of weight of thiarid (y¼0.00019 weight þ0.6751; r
2
¼
0.0572; pnot significant) and viviparid (y¼0.00065 weight þ0.29486; r
2
¼0.6694; p<0.01)
snails added by individual black carp (n¼9) in cement tanks over 14 days.
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consumption of small snails by the two larger fish size classes did differ significantly
(Table 3). There was, however, a significant interaction (p<0.001) between fish size
class and snail size class. Thus, the larger fish (just over 600 g, see Table 1) consumed
more of the larger size classes (i.e., in the range of 21–30 mm), while smaller and the
largest size classes appeared to be less consumed (Figure 4). Gape size of medium and
large fish used in the trial with M. tuberculata was substantially greater than the largest
shell diameter of M. tuberculata (about 11 mm), while the smaller black carp had esti-
mated gape widths of 12–16 mm. Thus, the largest M. tuberculata could be too large for
small black carp to manipulate and also they might be too hard to crush.
Small black carp consumed 84.5% of the small (<16 mm) A. polyzonata and the odds
of this snail species being consumed relative to the smallest size category declined signif-
icantly (p<0.001) with snail size and increased (p<0.001) with the size of the black
carp. The interaction between size class of A. polyzonata and black carp size was not
Table 1. Characteristics of the black carp specimens used in the four-prey selection trials.
Size class M. tuberculata B. fuchsiana A. polyzonata
S. aeruginosa
Number of black carp used
Small 23 2 25 9
Medium 33 6 22 10
Large 8 23 19
Weight range (g)
Small 100–250 120 100–250 100–250
Medium 260–590 260–600 270–600 260–600
Large 610–620 610–1250 610–1250
Length range (mm)
Small 155–210 165–170 150–220 150–220
Medium 210–350 210–360 210–370 215–355
Large 360–365 320–455 320–455
Gape width (mm); estimated
Small 12–16 13–13 12–17 12–17
Medium 16–26 16–26 16–27 16–26
Large 26–27 24–33 24–33
Includes trials where the two viviparid species were tested together in the same aquarium.
Table 2. Number of snails of various species and sizes used in experiments and the overall
proportion consumed by black carp.
M. tuberculata B. fuchsiana A. polyzonata S. aeruginosa
Size class
(mm)
No.
tested
Proportion
consumed
No.
tested
Proportion
consumed
No.
tested
Proportion
consumed
No.
tested
Proportion
consumed
<10 400 1.00 12 0.75 6 0.67
10–15 773 0.93 417 0.92 202 0.72
16–20 918 0.84 480 0.81 437 0.55
21–25 700 0.85 496 0.65 136 0.29
26–30 327 0.77 281 0.49 57 0.14
>30 482 0.42 114 0.18 2 0.50
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significant. The estimated gape width of small black carp (12–17 mm) showed that large-
sized A. polyzonata (up to about 21 mm in diameter) would be too large for this size class
of black carp to handle. The largest three size classes from shell diameter 15–21 mm
could be problematic, although the fishes managed to consume some of them.
Small black carp consumed 39.6% of the smallest size class of S. aeruginosa and the
odds of a snail being consumed declined with increasing size class (p<0.001) and
Table 3. Odds of snails of different species and sizes being consumed by black carp of different
sizes; the reference group is small black carp feeding on small sized snails.
Size class (shell height in mm) Shell diameter (mm) Small fish Medium fish Large fish
Melanoides tuberculata
10–15 3.8–5.5 1.00 1.67 0.58
16–20 5.5–7.1 0.22 1.01 0.76
21–25 7.1–8.8 0.21 1.20 2.47
26–30 8.8–10.5 0.09 0.89 3.57
>30 >10.5 0.02 0.09 0.27
Angulyagra polyzonata
10–15 9.7–12.4 1.00 4.88 7.40
16–20 12.4–15.1 0.31 1.50 2.28
21–25 15.1–17.9 0.12 0.57 0.86
26–30 17.9–20.6 0.07 0.32 0.48
>30 >20.6 0.01 0.06 0.10
Sinotaia aeruginosa
10–15 8.7–12.0 1.00 3.86 12.35
16–20 12.0–15.3 0.61 0.94 4.28
21–25 15.3–18.6 0.22 0.11 3.15
>26 18.6–21.9 <0.01 0.25 1.09
Figure 4. Percentage of snails of various species and size classes consumed (gray columns) by dif-
ferent size classes of the black carp. The size class <11 mm is excluded as this class could not be
tested for all species (not available).
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increasing fish size (p<0.05). There was, however, a significant interaction between
snail size class and fish size class (p<0.001). The trial with the two viviparid species
tested together showed that the odds of S. aeruginosa being consumed was 0.63 of that of
A. polyzonata (p<0.05) when adjusting for snail size class, fish size class, and the inter-
action between these two factors (p<0.001).
Crushing resistance
The characteristics of snails used in this experiment and linear regression between crush
resistance and either shell height or shell diameter are summarized in Table 4. Except in
S. riquetti and A. polyzonata, crush resistance (log
e
-transformed) was linearly related to
shell size (log
e
-transformed). Crush resistance was very variable for most species proba-
bly because more populations were represented in each sample. For the thiarid snails,
slopes of the regression lines did not differ significantly, but T. granifera had higher crush
weight than M. tuberculata (p<0.001), S. riquetti (p<0.001), and T. scabra (p<0.01).
M. tuberculata and S. riquetti did not differ in crush resistance and T. scabra had lower
crush resistance than both M. tuberculata (p<0.001) and S. riquetti (p<0.01). The
crush resistance of S. aeruginosa increased with size while this was not observed for A.
polyzonata but within the size range covered by both species, differences were not
pronounced.
The relationship between crush resistance and shell size of the species used in the
prey selection trial showed that B. fuchsiana had the lowest crush weight, while there
was considerable overlap between M. tuberculata and the viviparid snails when using
shell height as measure for size. Using shell diameter the size range covered by both
groups was small and M. tuberculata was smaller than the viviparid snails, but crush
resistance in M. tuberculata overlapping the viviparid was similar to that of the
viviparid (Figure 5).
Table 4. Shell size range (height or diameter), crush weight range and slope, and intercept from
linear regression analysis on log
e
(crush weight) and log
e
(shell size).
No.
Shell size
(mm)
Crush weight
(kg) Slope Intercept R
2
pvalues
Shell height
Bithynia fuchsiana 61 6.2–10.6 0.8–6.7 2.57 2.19 0.47 <0.001
Tarebia granifera 11 14.3–41.1 14.2–59.0 0.93 7.18 0.63 <0.01
Sermyla riquetti 15 11.9–23.7 4.5–17.4 1.06 6.04 0.23 n.s.
Thiara scabra 65 9.0–24.3 4.8–22.0 0.66 7.44 0.29 <0.001
Melanoides tuberculata 152 6.5–39.6 2.3–31.6 1.10 5.97 0.48 <0.001
Angulyagra polyzonata 121 13.8–32.5 6.5–60.5 0.18 10.32 0.00 n.s.
Sinotaia aeruginosa 63 10.1–32.1 12.3–68.3 0.64 8.36 0.18 <0.001
Shell diameter
B. fuchsiana 61 4.9–6.2 0.8–6.7 5.85 2.35 0.47 <0.001
T. granifera 11 5.3–15.7 14.2–59.0 0.91 8.11 0.63 <0.01
S. riquetti 15 5.1–8.1 4.5–17.4 1.57 6.12 0.23 n.s.
T. scabra 65 4.5–10.8 4.8–22.0 0.74 7.78 0.29 <0.001
M. tuberculata 152 2.3–13.4 2.3–31.6 1.13 7.09 0.48 <0.001
A. polyzonata 121 11.2–21.4 6.5–60.5 0.24 10.44 0.00 n.s.
S. aeruginosa 63 8.1–22.6 12.3–68.3 0.71 8.36 0.18 <0.001
Note: n.s.- not significant.
556 N. Hung et al.
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Discussion
Small black carp mostly fed on M. tuberculata, with even small (100–250 g) fish consum-
ing fairly large specimens (>30 mm). M. tuberculata is the primary host for intestinal
trematodes in aquaculture ponds i.e., mainly Haplorchis spp., Stellantchasmus falcatus,
and C. formosanus (Phan et al. 2010a). The black carp is primarily molluscivorous and
most fish ponds have a dense population of viviparid snails, in particular, A. polyzonata.
Since this species is also consumed by black carp, it could switch to feeding on these snail
species if M. tuberculata becomes scarce. The intermediate hosts of C. sinensis, B. fuchsi-
ana, and Parafossarulus manchouricus are readily consumed by even the smallest (about
120 g) black carp. The bithynid snails are not commonly found in the majority of fish
ponds, but occasionally occur at relatively high density.
The tall and slender shell shape of M. tuberculata makes it more vulnerable to preda-
tion by black carp, which has a comparatively small mouth opening (gape width) while
the larger specimens of A. polyzonata have refuge from predation. When the black carp
reach a size where they can manipulate them in their buccal cavity, however, they can
also exert sufficient pressure to crush the shell. Occasionally, we found shells where the
black carp had only been able to cause partial damage.
Small black carp fed primarily on thiarid snails, whereas larger ones tended to con-
sume more viviparid snails. This could be partly related to the shell strength relative to
the energy gain. Thus, Brodersen et al. (2003) showed that Sargochromis codringtoni
consumed Bellamya capillata specimens with relatively low energetic cost/benefit (C/B)
ratio. Also for the redear sunfish, L. microlophus, low energetic C/B ratio was found to be
the best determinant for snail selectivity (Stein et al. 1984). Other experiments have indi-
cated that handling time is also important for snail size selectivity by fish (Slootweg
1987). Relative abundance of the different snail species would be another determinant of
food selection (Evers et al. 2006).
The thiarid species, which all seem to serve as intermediate hosts for intestinal tremat-
odes differ in their shell strength. T. granifera has the strongest shell and this probably is
due to its thicker shell. A shell’s strength is typically correlated with its size (Miller and
Figure 5. Crush resistance of Bithynia fuchsiana,Melanoides tuberculata, and the pooled data for
Angulyagra polyzonata and Sinotaia aeruginosa in relation to shell height (a) and shell diameter (b).
Journal of Freshwater Ecology 557
Downloaded by [Copenhagen University Library] at 10:17 12 December 2013
LaBarbera 1995; Cote et al. 2001), but the correlation with its thickness is stronger
(Zuschin and Stanton 2001).
Shell shapes also profoundly affect strength and resistance against lethal breakage.
This factor is not well understood because comparing shells of distinctly different shapes
is very difficult (Currey 1988). In gastropods, globular compact shapes are more resistant
against crushing than loosely coiled ones (Vermeij 1983; Palmer 1990a,1990b; Savazi
1991). The presence of an umbilicus decreases the strength of shell (Palmer 1983).
The implication of our findings is that black carp of relatively small size (100–200 g)
should be used for the control of the intermediate host snails of FZT because this size
class would feed primarily on snails with small shell diameter. This size class of black
carp can handle most of the size ranges available in M. tuberculata populations. Although
it may be possible to control snails in aquaculture ponds by pond management, this may
not be sufficient for controlling infections in fishes because ponds may interact with the
surrounding habitats such as small canals and rice fields (Clausen et al. 2012b). Thus, we
also recommend that the possibility of stocking surrounding habitats, especially small
canals, with black carp should be further explored. This, however, would require very
strong community collaboration as the small canals are commonly targeted for fishing.
The chances of success would be increased if this could be seen as part of the production
system as the black carp is a valued fish for human consumption.
Acknowledgements
We would like to thank the Research Institute for Aquaculture No. 1 and the FIBOZOPA project for
all assistance and hospitality. This study was funded by DBL-Centre for Health Research and
Development, Department of Veterinary Disease Biology, Faculty of Life Sciences, University of
Copenhagen.
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- ... Water level was kept at 1.2 m, and constantly aerated and re-circulated through a filter system at a rate of 0.5 m 3 /h. The filter contained a net (mesh size 0.5 Â 0.5 mm), and water passed through a layer of foam rubber and a layer of sand before being returned to the tank (Hung et al., 2013). Food pellets, supplied by MINH TAM Company (http://minhtamgroup.com.vn) were round with diameter ranging between 2.5 and 3.0 mm. ...
- ... In the nursery ponds, the most pronounced reduction in density was observed for the thiarid snails. Hung et al. [43] showed that even small black carp can handle fairly large specimens of M. tuberculata, while larger black carp specimens consumed relatively more viviparid snails and this is probably due to the difference in shell shape, i.e. M. tuberculata has a much smaller shell diameter than the viviparid snails. ...
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