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Agriculture, Ecosystems and Environment 188 (2014) 9396

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Agriculture, Ecosystems and Environment


journal homepage: www.elsevier.com/locate/agee

Short communication

Response of the sh assemblage structure in a small farm pond to


management dredging operations
Yoshito Mitsuo a, , Hiroshi Tsunoda b , Genki Kozawa c , Masahide Yuma a
a
Department of Environmental Solution Technology, Faculty of Science and Technology, Ryukoku University, 1-5 Yokotani, Seta-Oe, Otsu,
Shiga 520-2194, Japan
b
Research Center for Wildlife Management, Gifu University, Yanagido, Gifu 501-1193, Japan
c
Department of Environmental Solution Technology, Graduate School of Science and Technology, Ryukoku University, 1-5 Yokotani, Seta-Oe, Otsu, Shiga
520-2194, Japan

a r t i c l e

i n f o

Article history:
Received 5 December 2013
Received in revised form 3 February 2014
Accepted 9 February 2014
Available online 12 March 2014
Keywords:
Farm pond
Management
Fish assemblage
Dissolved oxygen

a b s t r a c t
Articial water bodies, including farm ponds, contribute to regional biodiversity by providing alternative
habitats for many species. Although management operations, such as dredging, are commonly conducted
in farm ponds to maintain their function, little is known about the effects of habitat change associated
with such operations on sh assemblages. The objective of this research was to examine the relationship
between sh assemblage structure and pond management and via a comparative study before and after
a dredging event. It was found that the sh assemblage structure was signicantly different after the
dredging event. Before dredging, extensive growth of aquatic macrophytes and low dissolved oxygen level
were observed. Only two Cobitidae species, which have a tolerance to dissolved oxygen depletion, were
recorded just before dredging. After dredging, the dissolved oxygen level and number of sh species had
increased. The results indicated that management operations could change the sh assemblage structure
via a shift in the dissolved oxygen level associated with changes in macrophyte coverage.
2014 Elsevier B.V. All rights reserved.

1. Introduction
As an alternative to natural wetlands, articial water bodies
located within an agricultural landscape can provide suitable habitats for many species (Crghino et al., 2008; Tourenq et al., 2001).
Because they support a greater number of unique and rare species
relative to that found in other water bodies, farm ponds, in particular, can contribute signicantly to regional biodiversity (Biggs et al.,
1994; Williams et al., 2004). In Japan, small farm ponds, the majority with a surface area <1 ha, have been constructed since the 4th
century to irrigate rice paddy elds and are also important habitats
for many organisms, including sh and dragonies (Mitsuo et al.,
2010; Takamura, 2012).
The management and restoration of lakes and farm ponds, via
operations such as dredging and plant removal, have been widely
conducted to prevent silting and eutrophication (Phillips et al.,
1999). Juan et al. (2012) has reported that dredging operations were
performed on farm ponds in south-east Spain once every 8.6 years,
on average, with the main aim of controlling excessive vegetation

Corresponding author at: Department of Environmental Solution Technology,


Faculty of Science and Technology, Ryukoku University, 1-5 Yokoya, Seta-Oe, Otsu
520-2194, Japan. Tel.: +81 77 544 7178.
E-mail address: mitsuo4@gmail.com (Y. Mitsuo).
http://dx.doi.org/10.1016/j.agee.2014.02.015
0167-8809/ 2014 Elsevier B.V. All rights reserved.

growth and sediment accumulation. Similarly, on traditional farm


land in Japan, dredging is carried out on farm ponds approximately
once every 5 years (Hamashima et al., 2001). Moreover, there is a
strong association between lake inhabitants and aquatic plants and
lake morphology (Teixeira-de-Mello et al., 2009; Tejerina-Garro
et al., 1998); for example, aquatic plants provide habitat heterogeneity for sh assemblages (Tonn and Magnuson, 1982). Thus, it is
predicted that habitat changes, caused by management operations,
will have a major impact on sh assemblages in farm ponds.
However, although many studies have been conducted on the
restoration and management of lakes, little is known about the
effect of management operations on organisms in small lentic systems, such as farm ponds. Therefore, the objective of this research
was to establish the relationship between sh assemblage structure and habitat changes associated with management operations
via a comparative study before and after a dredging event in a farm
pond.

2. Materials and methods


2.1. Study pond
The study site was located on agricultural land in Iwate Prefecture, northern Japan (39 11 N, 141 03 E). In many regions of Japan

94

Y. Mitsuo et al. / Agriculture, Ecosystems and Environment 188 (2014) 9396

Table 1
List of sh species collected in the study pond.
2005
sum
Carassius spp.
Pseudobagrus tokiensis
Rhodeus ocellatus ocellatus
Oryzias latipes
Cobitis biwae
Misgurnus anguillicaudatus
Rhinogobius sp. OR
Micropterus salmoides

Number of species

2006
win

2007

sum

win

sum

2008
win

sum

2009
win

2010

sum

win

2012

sum

win

sum

win

+
+

+
+
3

+
+
+

+
+

+
+

+
+

+
+

+
+
+
+

+
+
+

+
+
+
+
+
+

+
+
+

Fig. 1. Condition of the study pond (a) before dredging and (b) after dredging.

Between 2005 and 2012, the sh assemblage and various environmental factors were monitored twice a year (mid-summer and
early winter). The sh population was sampled using a dip net
(1-mm mesh), cast net (9.5-mm mesh) and minnow trap (60-mm
entrance diameter) for 30 min at each monitoring time. After 2008,
dissolved oxygen levels of surface water (DO; Lutron DO-5509),
maximum depth (cm), vegetation coverage (nearest 5%) and turbidity (cm) were recorded during sh sampling. DO and turbidity
of surface water were monitored in an area of open water 10:00
and 14:00 h.
2.3. Analysis
Differences in species composition between samples before and
after dredging were analyzed by a multi-response permutation
procedure (MRPP) using presenceabsence data by the mrpp
function in the vegan package in R, which is a nonparametric
method for testing the hypothesis of no differences between samples by a Monte Carlo procedure (1000 permutations). Then, a
multivariate generalized linear model (GLM) was used to quantify
the contribution of all the measured environmental factors to sh

3. Results
Coverage of aquatic plants in the pond increased since the survey started in
2005 and the surface of the pond was almost totally covered by aquatic vegetation
in the year before dredging (Fig. 1). Dissolved oxygen (DO) displayed relatively low
values during 20072009 (i.e. before dredging) (Fig. 2), with the measured lowest
value in 2009 of 4 mg/l. DO levels increased after dredging (Fig. 2), with a signicant
difference between before and after dredging operation (U-test, P < 0.05).
A total of eight sh species were recorded during the monitoring program
(Table 1). Only two species of Cobitidae (Misgurnus anguillicaudatus and Cobitis
biwae) were recorded immediately before dredging. Species of Cyprinidae and

100

12

75

50

25

Vegetation
DO

0
sum win sum
2008

win sum

2009

Dissolved oxygen (mg/l)

2.2. Sampling

species richness. In the GLM analyses, a Poisson distribution was


assumed for the number of species (response variable) with the
default log link function in R. DO, turbidity, maximum depth, coverage of aquatic plant and sampling year were included in the analysis
as explanatory variables. Finally, a stepwise procedure was used to
identify the most parsimonious and most accurate combination of
explanatory variables using the AIC criterion.
All statistical analyses were performed using R 2.12 (R Development Core Team 2011).

Vegetation coverage (%) ko

with low precipitation or topographical features that prevent water


exchange with other systems, small farm ponds were constructed
for irrigating rice elds. It is currently estimated that there are over
200,000 of these ponds in Japan (Uchida, 2003), and many of them
are found within the study site (Mitsuo et al., 2011). One of these
ponds, with a surface area of 2100 m2 and maximum depth of
1 m, was continuously surveyed over a period of 7 years. The banks
and bottom of the pond were mainly composed of natural materials and the pond served no purpose other than irrigation. An inlet
channel owed into the study pond throughout the year, and the
pond never dried up. To prevent silting, dredging and removal of
plant material was carried out by the local authorities in late winter 2009. In addition, no sh species were introduced into the pond
during study period.

win sum win

2010

2012

Fig. 2. Changes in vegetation coverage and dissolved oxygen levels. Dissolved oxygen levels were signicantly different before and after the dredging operation
(U-test, P < 0.05).

Y. Mitsuo et al. / Agriculture, Ecosystems and Environment 188 (2014) 9396


Table 2
Results of model selection for GLM. Models with AICc < 2 of the best model are
shown.
Model rank

AIC

Variable

Coefcients

31.54

Intercept
DO

1.037
2.862

1.173
1.401

32.77

Intercept
DO
Year

245.7
2.377
0.122

276.3
1.554
0.138

S.D.

Walds 2
0.884
2.042*
0.889
1.53
0.886

p < 0.05

Gobiidae were observed after dredging (Table 1) and MRPP analysis showed
signicant differences in the assemblage structures (Monte Carlo permutation test,
P < 0.05). Species richness was also signicantly different between before and after
dredging (U-test, P < 0.001), with the number of species captured increasing after
dredging (Table 1). Result of GLM analysis revealed that only DO was signicantly
positively associated with the number of species (Table 2).

4. Discussion
In the study pond, the surface area was almost totally covered
by aquatic macrophytes, such as Trapa japonica and Phragmites
australis, in 2009 (i.e. just before dredging). Previous studies have
reported that aquatic macrophytes support sh species diversity
by providing feeding and/or spawning sites (Beckett et al., 1992;
Persson and Eklov, 1995). However, it has also been reported that
extensive macrophyte stands can have a negative effect on sh
assemblages (Dibble et al., 1997; Fuentes-Rodrguez et al., 2013).
Dibble et al. (1997) have demonstrated that sh species richness is
highest at an intermediate coverage of macrophyte (1040%) and
decreases at greater levels of coverage. In our study, the number
of sh species decreased until nally only two species of Cobitidae were recorded before dredging. Although the mechanism for
the effect of extensive macrophyte stands on sh assemblages is
less well documented, it has been reported that excessive plant
growth reduced the growth and condition of largemouth bass
(Micropterus salmoides), bluegill (Lepomis macrochirus) and redear
sunsh (L. microlophus) (Colle and Shireman, 1980; Wiley et al.,
1984). Wiley et al. (1984) attributed the facts to reduced foraging efciency. Moreover, decreases in dissolved oxygen levels
due to the development of aquatic macrophytes have often been
observed (Gee et al., 1997; Killgore and Hoover, 2001). In a previous study conducted in 49 farm ponds in the same region, we
also found a negative relationship between macrophyte coverage
and the dissolved oxygen levels of open surface water. In addition, Gee et al. (1997) found that the maximum percentage oxygen
saturation recorded at 0.5-m depth intervals was negatively correlated with the coverage of oating plants in small ponds in an
agricultural area of the UK. In this study, the study pond had a low
dissolved oxygen level before dredging; the lowest value measured
was <5 mg/l which is recognized as a threshold level inuencing sh behavior (Kramer, 1987). Moreover, the two species of
Cobitidae, which were observed immediately before dredging, can
tolerate hypoxic conditions by air breathing (Robotham, 1982;
McMahon and Burggrcn, 1987). Therefore, decreasing dissolved
oxygen levels caused by extensive growth of macrophytes may
restrict the number of sh species that could inhabit ponds, resulting in a decrease in species richness. Similarly, Killgore and Hoover
(2001) showed that, in an impoundment in southwest Arkansas,
dissolved oxygen measured at the surface and bottom was negatively correlated with the coverage of aquatic plants and, under
hypoxic conditions, sh assemblages were dominated by species
that exhibited specic behavioral and morphological adaptations to
hypoxia.
After dredging, dissolved oxygen levels increased and a signicant change in the sh assemblage structure was observed because

95

of colonization from surrounding water systems via the inlet channel, with the pond being dominated by cyprinid species, including
bitterling. Bitterling (Rhodeus ocellatus ocellatus) are widely distributed in this area (Mitsuo et al., 2010) and there are no reports of
species being adapted to hypoxic conditions. In addition, our results
of GLM showed that dissolved oxygen is a signicant predictor of
species richness. These observations also indicate that changes in
dissolved oxygen levels relative to aquatic macrophyte abundance
can inuence the sh assemblage in a small farm pond.
Thus, the removal of aquatic macrophytes can change dissolved
oxygen conditions and, consequently, have a major impact on sh
assemblage structure in a farm pond. In lentic systems, top-down
control of higher-order consumers is considered to have a stronger
effect than in other systems (Halpern et al., 2005); disequilibrated
sh assemblages can cause a dramatic shift in lake and pond ecosystems mainly through predation, i.e. trophic cascade (Carpenter and
Kitchell, 1996). For example, it has been demonstrated that a reduction in cyprinid numbers resulted in increasing transparency due
to the considerably reduced phytoplankton biomass (Annadotter
et al., 1999). It has also been reported that not only interspecic but
also even intraspecic variations in foraging behavior inuenced
lower community structure (Post et al., 2008). Although it is common management practice to remove aquatic macrophytes from
lakes and farm ponds to prevent silting and eutrophication (Phillips
et al., 1999), our results suggest that such management operations
affect these aquatic ecosystems by changing the sh assemblage
structure.
Small ponds naturally tend to be covered by dense aquatic
macrophytes (Crghino et al., 2008). In this study, more than half
the surface area of the pond was covered by macrophytes nearly one
year after dredging. Thus, although small ponds make an important contribution to regional biodiversity owing to their high
diversity (Oertli et al., 2002), the suspension or cessation of management operations due to neglect or agriculture modernization
would lead to homogenization of sh assemblages in small farm
ponds, resulting from the development of hypoxic conditions.

5. Conclusions
This study demonstrated, via a 7-year monitoring program, the
inuence of dredging operations on the sh assemblage structure
in a farm pond. Before dredging, extensive aquatic macrophyte
stands covered the pond, dissolved oxygen levels were low and
only two Cobitidae species, which have a tolerance to hypoxic conditions, were recorded. Conversely, after dredging, the number
of sh species increased with increasing dissolved oxygen levels, and a signicant change to the cyprinid assemblage was also
observed. Although aquatic macrophytes are thought to contribute
to sh species richness, our results suggest that excessive vegetation growth can have a negative impact on sh assemblages. While
sh are considered to have a major effect in lentic ecosystems,
dredging operations, which are widely used to maintain the function of lakes and ponds, can signicantly change the structure of
pond-dwelling sh by altering the dissolved oxygen level.

Acknowledgements
We are grateful to the staff of the city government of Oshu
for their constant support that made this study possible. We also
thank M. Ohira, R. Yokomizo, Y. Shono, Y. Yamamoto, M. Doi, and
A. Takiguchi for eld assistance, and two anonymous reviewers for
their helpful comments on former draft of this article. This work
was partly supported by KAKENHI (19658088), (20-3522) and (238703).

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Y. Mitsuo et al. / Agriculture, Ecosystems and Environment 188 (2014) 9396

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