Food web properties of the recently constructed, deep subtropical Fei-Tsui Reservoir in comparison with the ancient Lake Biwa
Food web properties of the recently constructed, deep subtropical Fei-Tsui Reservoir in comparison with the ancient Lake Biwa
Noboru Okuda . Yoichiro Sakai . Kayoko Fukumori . Shao-Min Yang . Chih-hao Hsieh . Fuh-Kwo Shiah 0 1 2 3 4
Handling editor: Michael Power 0 1 2 3 4
0 K. Fukumori Center for Environmental Biology and Ecosystem Studies, National Institute for Environmental Studies , Tsukuba 305-8506 , Japan
1 Y. Sakai Lake Biwa Environmental Research Institute , Otsu 520-0022 , Japan
2 N. Okuda (&) Research Institute for Humanity & Nature , Kyoto 603-8047 , Japan
3 F.-K. Shiah (&) Research Center for Environmental Changes , Academia Sinica, Taipei 115 , Taiwan
4 S.-M. Yang C. Hsieh Institute of Oceanography, National Taiwan University , Taipei 10617 , Taiwan
Using carbon and nitrogen stable isotope analysis, we characterised food web properties of the deep subtropical Fei-Tsui Reservoir (FTR), which was recently altered from a lotic to a lentic system after dam construction. In the littoral zone, zoobenthos showed strong reliance (83.9%) on benthic algal production. Zoobenthos were never found in the profundal zone because of anoxia. Zooplankton depleted 13C more than that of particulate organic matter as their putative food source, suggesting a contribution of methane-derived carbon to pelagic food webs. Excluding juveniles, non-native and fluvial species, adult fish showed strong reliance (on average 80.9%) on benthic production, weakly coupled with pelagic food webs. These results contrast low benthic production reliance (on average 27.4%) for a fish community in Lake Biwa, which is also classified as a subtropical lake. Both lakes are characterised by deep pelagic waters but quite different in their geological ages, suggesting that the aquatic communities in the FTR have fluvial origins, and their lacustrine history was too short for them to adapt to newly emerged deep pelagic habitat. Our isotope data are useful as a reference of newly established lentic food webs to monitor ongoing ecological and evolutionary dynamics as a result of anthropogenic disturbances.
Dam construction; Production reliance; Stable isotope analysis; Trophic flow; Trophic position
Dams and reservoirs have been constructed to meet
accelerated demands for water and energy resources as
populations experience explosive growth and climate
change worldwide (Nilsson et al., 2005). While dams
provide high public utility, they can negatively impact
river ecosystems by drastically changing waterway
from lotic to lentic systems (McAllister et al., 2001).
In dammed rivers, some taxa can modify and adapt
their life histories to sustain their populations;
however, others that cannot adapt may go into local
extinction due to loss of original habitats. At present,
dam construction is considered as one of the major
drivers of biodiversity loss in the freshwater
ecosystems through the alteration and homogenisation of
natural hydrological regimes (Poff et al., 2007), the
creation of physical barriers to migratory species
(Liermann et al., 2012), the dispersal and colonisation
of non-native lentic species (Havel et al., 2005), and
the pollution and eutrophication at dam sites
(Dudgeon, 2000). Therefore, it is important to perform
ecosystem assessments after dam construction for
water quality management and biodiversity
Stable isotope analysis (SIA) is a powerful tool to
assess ecosystems, especially food web properties
characterised by trophic interactions within a
biological community. Food web characterisation is of
ecological and social significance because trophic
interactions can drive nutrient cycling and energy
flows, which in turn affect ecosystem services (e.g.
water quality, food supply for humanity). At present,
the stable isotopic approach is the preferred method for
studying aquatic food webs, in which carbon (d13C)
and nitrogen (d15N) isotope ratios, for aquatic species,
are used to distinguish primary trophic pathways, for
example, pelagic versus littoral pathways (France,
1995a, b) or aquatic versus terrestrial pathways
(Peterson & Fry, 1987; Finlay, 2001). Especially for
fish, their isotopic signatures provide useful
information in estimating the relative importance of trophic
energy flows in lake ecosystems. Fish predators
integrate a variety of trophic pathways as they couple
pelagic and littoral food webs due to their high mobility
and omnivory (Vander Zanden & Vadeboncoeur,
2002; Vander Zanden et al., 2011). The stable isotopic
approach can also be applied to assess food web
alterations in aquatic ecosystems under human
disturbances (Vander Zanden et al., 1999; Layman et al.,
2007; Anderson & Cabana, 2009; Hamaoka et al.,
2010). In most cases, however, stable isotopic studies
are conducted after ecosystem alterations were
perceived. As such, limited information is available on
original conditions before the disturbance (but see
Okuda et al., 2012; Vander Zanden et al., 2003).
Newly constructed dams and reservoirs provide a
good possibility to understand ecological processes of
food web alterations if initial conditions of the lentic
system are assessed soon after dam or reservoir
construction. In this study, we conducted d13C and
d15N analysis to characterise food web properties of
the Fei-Tsui Reservoir (hereafter, FTR; Fig. 1;
Table 1), which was established in 1987 to supply
drinking water for more than 5 million people in
metropolitan Taipei. Since its construction, the local
government has been responsible for ecosystem
management of the reservoir, focusing mainly on
water quality. In contrast to physical and chemical
characteristics, biological information was monitored
less with the exception of phytoplankton data that
were monitored as an indicator of water quality (Wu
et al., 2007). Recently, Chang et al. (2014a, b) reported
community dynamics and size-based food webs in the
FTR, focusing on plankton communities in pelagic
waters. A holistic approach that encompasses benthos
and fish as higher consumers in coastal and pelagic
waters is needed to view the overall trophic energy
flows in lentic food webs of the FTR before future
anthropogenic disturbances occur. This study can,
therefore, be regarded as a reference for ongoing
In this study, we also intend to compare food web
properties of FTR with those of Lake Biwa, in which
a holistic approach towards food web analysis was
performed in a similar way to the present study
(Okuda et al., 2012). According to Yoshimura
(1937)’s lake classification, both lakes were
classified as subtropical, monomictic lakes in Monsoon
Asia. During the quaternary glaciation, terrestrial and
aquatic species migrated between southern Japan and
Taiwan through a land bridge, often forming sister
species (Chiang & Schaal, 2006; Ho et al., 2016).
Such a biogeographical history has enabled the same
species and congeners to exist in both lakes. These
lakes are also similar in terms of depth and trophic
state (Table 1). Considering their biogeographical
and limnological backgrounds, they are comparable
in relation to trophic positions of some common
taxa. However, they are quite different temporally as
the lentic waters emerged at different times. We will
discuss how the historical difference in the lentic
community colonisation affects trophic energy flows
in these deep lakes.
Fig. 1 The map of Fei-Tsui Reservoir (b) in Taipei, Taiwan (a). Star and square symbols represent the pelagic and littoral sampling
Table 1 Comparison of
between Fei-Tsui Reservoir
and Lake Biwa
a Paleo-Lake Biwa
appeared ca. 4 mya ago,
while the current lake basin
was characterized by deep
pelagic waters through
faulting ca. 0.4 mya ago
Materials and methods
Study site and environmental issues
FTR, one of the largest reservoirs in Taiwan, is
located downstream of Peishih Creek, residing in a
watershed of 303 km2 in northern Taiwan (121 340E,
24 540N; Fig. 1a). Its limnological and bathymetric
characteristics are shown in Table 1. Although the
FTR was classified as an oligotrophic lake for several
years after dam construction (Chang & Wen, 1997), its
trophic state currently ranges between mesotrophic
and eutrophic according to Carlson’s trophic state
index (Chou et al., 2007). Dominance in
phytoplankton flora has shifted from dinoflagellates to
cyanobacteria and green algae, suggesting a long-term trend
towards eutrophication (Wu & Chou, 1998; Wu et al.,
In the reservoir, seasonal and vertical profiles of
dissolved oxygen are affected by weather- and
climatedriven hydrodynamics (Fan & Kao, 2008). A recent
concern is the frequent release of typhoon-induced
suspension interflows from the main tributary,
increasing phosphorous loading and affecting water quality
(Chen et al., 2006). Moreover, strong summer
stratification and incomplete winter mixing due to warming
have often caused hypoxia in profundal waters (Itoh
et al., 2015), which may have non-linear and lethal
effects on profundal communities. Considering such
emerging environmental issues, long-term ecosystem
monitoring was launched in 2004. The physical and
chemical environmental data we obtained have been
published (Itoh et al., 2015; Chow et al., 2016).
Prior to food web analysis, we conducted field
sampling of fish, zooplankton, zoobenthos, and their
basal food sources. We collected zooplankton and
their putative food sources from pelagic waters at the
monitoring station near the dam (113.5 m at depth;
Fig. 1b). On 17 November 2009, meso- and
macrozooplankton were collected with a 100-lm-mesh
plankton net towed vertically in the epilimnion
(0–18 m at depth). For sampling of particulate organic
matter (POM) as basal food for pelagic consumers,
lake waters were collected at the depth of 2 m with a
5-L Go-Flo bottle (General Oceanics, Miami, FL) on
13 and 27 October and 10 November 2009. Water
samples were screened with a 10-lm-mesh and then
filtrated with glass fibre filter (GF/F, 0.7 lm,
Whatman) pre-combusted at 450 C for 2 h. Particle sizes of
0.7–10 lm cover the size range of meso- and
macrozooplankton prey in the FTR (Chang et al., 2014b).
These time-series POM samples were mixed in equal
quantities to integrate temporal variations in their
isotopic signatures, reflecting a high turnover rate for
small-sized plankton. This procedure is reasonable
because large-sized zooplankton biomass integrates
temporal variation in their dietary isotopic signatures
for a few months (Ho et al., 2016). In FTR, seasonal
pattern of surface POM isotopic signatures is
predictable (See Fig S1 in Ho et al., 2016), so that our
mixing model with pooled POM data is robust to
temporal variation in its isotopic signatures.
While monitoring the station near the dam, we
collected surface sediment from the deep lake bottom
as the putative food source for profundal consumers,
using an Ekman-Berge grab sampler. The sediment
samples were sorted for zoobenthos, but no
individuals were found in profundal habitats.
We also collected zoobenthos and fish juveniles at a
littoral site (Fig. 1b) using a Sarvar net. As a basal
food source for littoral consumers, we collected
epilithic organic matter (EOM) from the littoral
habitat, scraping it off from each of four boulders
with a brush. After removing zoobenthos from these
suspended samples with a 150-lm-mesh net, they
were mixed and filtered through pre-combusted GF/F
filters. Leaf litter was also collected as allochthonous
terrigenous organic matter (TOM).
Adult fish specimens were obtained from an
aboriginal tribe, with government-authorised licenses
to catch the fish in the FTR, during our sampling
period. Except for the aboriginal fishing, fish sampling
using fishing gears and boat in the FTR is strictly
prohibited by Taipei Feitsui Reservoir Administration
even if it is the academic purpose. Such an
administrative constraint restricted our sampling design to
small sample size and narrow sampling area.
These samples were chilled and transferred to the
laboratory. Dominant zooplankton species were sorted
and identified under a microscope. Due to their little
mass, small-sized animal samples were prepared in
bulk for SIA. For adult fish specimens, we measured
their total length or standard length in millimetres and
then excised their muscle tissues from the dorsal part
of the lateral body. For zoobenthos and juvenile fish
samples, their entire mass was prepared for SIA. All
samples were dried at 60 C for 24 h.
Stable isotope analysis
Dry samples were ground into fine powder. For
animals, the ground samples were immersed in
chloroform:methanol (2:1) solution for 24 h to remove
lipids according to Kling et al. (1992). Each sample
was weighed and wrapped in a tin capsule for
combustion. We determined carbon and nitrogen
stable isotope ratios for each sample using a mass
spectrometer (CF/IRMS; Conflo II and Delta S,
Finnigan MAT, Germany), and carbon and nitrogen
contents were measured using elemental analyzers
(EA1108, Fisons, Italy). Ratios (R) of the heavy
isotope to the light isotope (13C/12C, 15N/14N) were
expressed in parts per thousand, relative to the
standards in delta notation following the formula:
Vienna Pee Dee belemnite and atmospheric
nitrogen were used as standards for carbon (d13C) and
nitrogen (d15N) isotope ratios, respectively. The
analytical precision based on working standard was
±0.1% for d13C and d15N.
Estimation of trophic position
We estimated trophic position of consumers in the
lentic food web of the FTR based on the following
stable isotope mixing model (see also Okuda et al.,
8< f1 þ f2 ¼ 1
f1d13C1 þ f2d13C2 þ Dd13Cef ðTP 1Þ ¼ d13Ccons
: f1d15N1 þ f2d15N2 þ Dd15Nef ðTP 1Þ ¼ d15Ncons;
where f1 and f2 represent the proportion of reliance of
the two major primary producers in the lentic food
web, that is, phytoplankton (POM) and benthic
microalgae (EOM), respectively. dR1, dR2, and dRcons
(R = 13C or 15N) are stable isotope ratios of
phytoplankton, benthic microalgae, and each focal
consumer, respectively. TP is trophic position. Dd13Cef
and Dd15Nef are trophic enrichment factors, assuming
that consumer’s d15N is enriched by 3.4% relative to
its diets (Minagawa & Wada, 1984) and its d13C by
0.8% (DeNiro & Epstein, 1978). The above mixing
model enables us to estimate TP and production
reliance (i.e. fn) for each consumer. If consumer’s
production reliance on either of the two basal foods
slightly exceeds one, we regarded it as exclusive
reliance (i.e. 100%). In the case in which fluvial fish
migrate between coastal and stream habitats (see
Results), we also used the EOM and TOM as basal
food sources in the isotope mixing model.
We measured a total of 45 samples, including 10 fish, 2
macrozoobenthos and 4 zooplankton taxa, together
with their basal food resources from littoral and
pelagic waters in the FTR (Table 2). One littoral
zoobenthos taxon (Chironomidae) was excluded from
our isotopic data because its carbon and nitrogen
contents were less than the lower detection limit. Its
lentic food web was delineated on d13C-d15N bi-plot
space (Fig. 2).
In pelagic habitats, trophic position cannot be
estimated for meso- and macro-zooplankton because
they depleted 13C substantially more than POM, which
is their putative food source (Fig. 2; Table 2).
Amongst the zooplankton samples, two copepods
and the bulk zooplankton community, which was also
dominated by copepods, enriched 15N by 3.5%, on
average, more than two cladocerans. This suggests
that the former TLs were higher than the latter by
around one although their absolute values could not be
calculated because of large deviations from the
isotopic range of their putative food sources, POM
and EOM. In littoral habitats, by contrast, shrimp
enriched their 13C, showing strong reliance on EOM
(83.9%; Table 2).
Fish occupied broad trophic niche spaces in the
lentic food web of the FTR (Fig. 2; Table 1). A catfish
Silurus asotus Linnaeus, 1758, a top predator, had the
highest TP (3.84 TP), showing its strong reliance on
benthic algal production (87.7%). Three fish species
(i.e. juvenile Rhinogobius sp., Carassius cuvieri
Temminck & Schlegel, 1846 and Oxyeleotris
marmorata (Bleeker, 1852)) had relatively low d13C. SIA
of a landlocked goby, Rhinogobius sp., in Lake Biwa
revealed that adult fish are benthic feeders in littoral
habitats, while 0? aged fish have a planktonic life
stage before their settlement (Maruyama et al., 2001).
Amongst juveniles of Rhinogobius sp. in the FTR, the
highest reliance on phytoplankton production was
74.0% although adult fish showed strong reliance on
benthic algal production (79.9%). C. cuvieri, a pelagic
species endemic to Lake Biwa, was possibly
introduced into the FTR after dam construction since it
cannot sustain populations in lotic environment. O.
marmorata is a fluvial benthic predator whose basal
food may be derived from allochthonous terrigenous
organic matter (TOM) in river habitats but not from
pelagic POM since it migrates between littoral and
river habitats. Assuming that this fish relies on
allochthonous TOM (i.e. leaf litter) and autochthonous
EOM, we estimated its production reliance on the
TOM as 88.7% and its TP as 3.97. Excluding
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juveniles, non-native and fluvial species, adult native
lacustrine fish showed on average 80.9% benthic
Pelagic and profundal food webs
In pelagic food webs of the FTR, TPs of zooplankton
taxa could not be estimated appropriately because
their isotopic signatures deviated from the isotopic
range of putative food sources. Based on their low
d15N values relative to POM, one may infer that
pelagic food webs are subsidised by allochthonous
TOM with a low d15N value as is often the case for
small lakes (Pace et al., 2004; Cole et al., 2006, 2011).
Cole et al. (2006) demonstrated that TOM is primarily
passed to pelagic food webs as a part of POM. In the
FTR, however, TOM contributes little to zooplankton
production, rejecting the possibility of terrestrial
subsidies (Ho et al., 2016).
Apart from their food sources, when focusing on the
locations of copepods and cladocerans on the
d13Cd15N bi-plot space, their relative trophic positions
were markedly different between the two dominant
taxa. Assuming that cladocerans are grazers and also
that the trophic enrichment factor is 3.4% for d15N,
copepods are considered carnivores. Such trophic
niche segregation has hitherto been reported for these
two taxa in many lakes (Yamada et al., 1998; Grey
et al., 2001; Matthews & Mazumder, 2003; Karlsson
et al., 2004). Since copepods are raptorial feeders, it is
likely that they feed on small-sized grazers, such as
protozoa, rotifers, nauplii, and cladoceran larvae. For
plankton communities, intra-guild predation (i.e.
predation on small-sized zooplankton by large-sized
zooplankton) is often prevalent in lakes dominated
by microbial loops (Grey et al., 2001; Karlsson et al.,
In the FTR, it is also interesting that the
zooplankton community had a much lower carbon isotope ratio
than POM as its putative food source. As pointed out
by Jones & Grey (2011), such an isotopic mismatch
between POM and zooplankton could be ascribed to
zooplankton consumption of 13C-depleted
phytoplankton, which assimilate 13C-depleted CO2 derived
from bacterial respiration of terrigenous DOC in
humic lakes. In the FTR, in contrast, bacterial
Fig. 2 Trophic positions of
each taxon in the lentic food
web of Fei-Tsui Reservoir.
Thick arrows represent the
pathways starting from
phytoplankton and benthic
assumptions from our
mixing model. Each plot and
bar are averaged and
presented with the standard
deviation of isotopic
signatures for each taxon.
Plot numbers correspond to
taxon codes in Table 2
decomposition of DOC is facilitated only when
phosphorous is loaded from the catchment after strong
typhoons (Tseng et al., 2010) and heterotrophically
respired 13C-depleted CO2 is not so much reflected in
the carbon isotope ratio of dissolved CO2 in surface
waters (-12 to -17%; Itoh et al. unpublished data),
suggesting another carbon source for zooplankton. In
eutrophic and/or humic lakes, dissolved methane
generated from the anoxic lake bottom and
characterised by an extremely low carbon isotope ratio is one
of the major carbon sources for zooplankton
(Bastviken et al., 2003; Taipale et al., 2008; Kankaala et al.,
2010). This trophic pathway from dissolved methane
to zooplankton is mediated by methane-oxidising
bacteria (MOBs), defined as methanotrophic food
webs. Long-term monitoring of methanotrophic food
webs is of ecological importance in understanding
how carbon cycling is altered in lakes affected by
In the FTR, it has been reported that MOBs
dominate profundal bacterial communities, showing
remarkable vertical and seasonal variations in
community compositions (Kojima et al., 2014; Kobayashi
et al., 2016). Itoh et al. (2015) experimentally
demonstrated that the methane oxidation activity is
highest in deep sub-oxic layers, in which both
dissolved methane and oxygen are available to MOBs.
In the deep FTR, methanotrophic food webs can be
mediated through zooplankton vertical migration to
feed on profundal MOBs, leading to the coupling of
pelagic and profundal food webs. Using isotopic and
theoretical models, Ho et al. (2016) revealed that the
relative contribution of MOBs to zooplankton
production seasonally varied from 0.6 to 14.6% in the
FTR, depending on hydrodynamic changes in
dissolved methane and oxygen concentrations. In the
FTR, methanotrophic contributions are not as great as
the contributions in boreal lakes (up to 50%; Kankaala
et al., 2010), which generate allochthonous carbon
subsidies for pelagic food webs during less productive
seasons. Using meta-analysis for lakes worldwide,
Bastviken et al. (2004) predicted that methane
production would increase with increasing total
phosphorous and dissolved organic carbon concentrations.
Considering the trend towards eutrophication after
dam construction, it is reasonable to expect long-term
changes in methanotrophic contributions to pelagic
food webs in the FTR. As reported by Ho et al. (2016),
the results from this study allow for long-term
monitoring of plankton isotope signatures to assess
alterations in trophic carbon flows in pelagic food
webs due to climate and land use changes.
In deep lakes, the oxic–anoxic conditions of the
lake bottom habitat also affect infaunal zoobenthos
communities and their trophic carbon flows in
profundal food webs. In Lake Biwa, many benthic species
have adapted to profundal habitats since deepening of
the lake basin ca. 0.4 million BC (Kawanabe et al.,
2012). Some hypoxia-tolerant burrowing chironomids
are characterised by extreme isotopic depletion of 13C,
suggesting the existence of methanotrophic food webs
in the sub-surface of lake sediments where an
oxidation–reduction boundary layer has developed
(Kiyashko et al., 2001). In the FTR, by contrast, there
exist no zoobenthos in the profundal habitat that is
anoxic. Since original zoobenthos faunas were living
in shallow and lotic environments before the
construction of this reservoir, they may not be tolerant to
deep anoxic conditions. The long-term monitoring
revealed that the profundal habitat interannually
alternates between anoxic and hypoxic conditions,
depending on the intensity of winter vertical mixing
under changing climates (Itoh et al., 2015). If there are
some scopes for hypoxia-tolerant species to colonise
populations from adjacent lakes, trophic carbon flows
in profundal food webs may be modified over time.
Trophic energy flows to higher consumers
In the FTR, a lacustrine fish community, except for
juvenile, fluvial and non-native fish, showed 80.9% of
benthic production reliance. It contrasts with Lake
Biwa in which the benthic production reliance is
27.4% for the whole fish community (Okuda et al.,
2012). The food chain length, defined as the TP of top
predators, was not so different between the FTR (3.84
TP for a catfish Silurus asotus) and Lake Biwa (3.75
TP for a giant catfish Silurus biwaensis Tomoda, 1961;
Okuda et al., 2012), whereas their benthic production
reliance was much higher for the former (87.7%) than
for the latter (25.6%). Vander Zanden et al. (2011)
estimated benthic production reliance as on average
57% for fish communities in 75 lakes worldwide, in
which carbon isotope data are available for food web
analysis. The relative contributions of benthic algae to
whole-lake primary production can be affected by
bathymetry (Vadeboncoeur et al., 2008). Amongst
temperate lakes of North America, for instance, a lake
trout, a top predator, shifts its production reliance from
benthic to pelagic drastically when the lake’s surface
area is more than 10 km2 (Vander Zanden &
Vadeboncoeur, 2002). Large lakes tend to have a
lower perimeter-to-area ratio, and they also tend to be
deeper than small lakes, thus reducing the relative
contribution of benthic algae to the whole-lake
production and subsequently to trophic carbon flows
in zoobenthos and fish (Vadeboncoeur et al., 2002).
Considering the limited area of shallow coastal
habitats in dams and reservoirs with steep slopes, it
is likely that benthic algae contribute little to the
whole-lake primary production in the FTR.
In this study, because the sample size and sampling
area were limited under the administrative constraints,
our results may be less conclusive in relation to
intraspecific and spatial variations in the fish trophic
position and production reliance within the reservoir.
Considering a general rule that large body-sized fish
have high mobility and low turnover rate (McCann
et al., 2005), however, our adult fish specimens should
have time- and space-integrated isotopic information
on food webs, ensuring that our estimation of their
trophic position and production reliance is reliable.
Since commercial and recreational fishing, except for
small-scale aboriginal fishing, is prohibited by the
Administration of Taipei FTR, the possibility of
overexploitation of pelagic fish, which would bias
fish community compositions to littoral species
relying on benthic production, can be ruled out. Rather,
strong benthic production reliance can be ascribed to
the fact that the native fish have fluvial origins,
associated with habits for feeding on benthos in river
habitats before the reservoir was constructed.
In the FTR, interestingly, a non-native fish
introduced from Lake Biwa showed the highest reliance
(81.9%) on pelagic production. In Lake Biwa, many
endemic fish species evolved from their fluvial
ancestors to adapt to the pelagic environment after
the lake deepened through faulting ca. 0.4 million
years ago (Okuda et al., 2013). In the FTR, by contrast,
its lentic history may be too short for the native fish to
adapt well to the pelagic habitat. However,
evolutionary biologists have recently reported numerous cases
studying rapid evolution, which occurs on an
ecological time scale much shorter than expected from
conventional evolutionary process (Stockwell et al.,
2003; Hairston Jr. et al., 2005). For instance, the
bluegill sunfish Lepomis macrochirus Rafinesque,
1810 was introduced into Lake Biwa from the United
States in the 1960s. Its colonised populations showed
benthic morphs feeding on littoral zoobenthos during
the early phases of colonisation in the 1970s
(Terashima, 1980). More than half a century after
the introduction, however, some of the bluegill sunfish
shifted to pelagic morphs with specialised feeding
habits for plankton preys (Yonekura et al., 2002). Such
trophic polymorphism was also detected by SIA
(Uchii et al., 2007). For native fish species in the
FTR, on one hand, it is interesting to correlate
longterm changes in their isotopic signatures with the shift
from benthic to pelagic habitats over time from now
on. As in the case of the FTR, on the other hand, we
have to warn against human introduction of non-native
pelagic fish in term of biodiversity conservation
because they easily occupy vacant niches after
reservoir construction (Liew et al., 2016), decreasing
opportunities for ecological adaptations of the native
fish to the pelagic habitat.
At present, the trophic state of FTR has become
mesotrophic and sometimes even eutrophic, a gross
difference from its original state as oligotrophy
immediately after reservoir construction. The dams
and reservoirs are destined to become eutrophic,
sooner or later, given nutrient loading from the
catchment. The relative importance of whole-lake
primary production will shift from benthic algal to
phytoplankton production through eutrophication
(Vadeboncoeur et al., 2001). Such a change in primary
production can also alter trophic carbon flows to
aquatic consumers, which can be detected by carbon
isotope analysis (Vadeboncoeur et al., 2003). Our
study is currently descriptive, but it can be a milestone
for future ecosystem assessments and evolutionary
research for the FTR. As reported for Lake Biwa
(Okuda et al., 2012), long-term isotopic monitoring in
the FTR will provide more insights into the dynamic
nature of lentic food webs due to ongoing
Acknowledgements This research was financially supported
by the Japan-Taiwan Joint Research Program of Interchange
Association, Japan, the JSPS Grant-in aid (No. 24405007 and
16H05774) and RIHN Project (D-06-14200119). FS was funded
by RCEC-Academia Sinica. We thank the staff of the Research
Center for Environmental Changes, Academia Sinica and
Institute of Oceanography, National Taiwan University for
their field assistance. We also thank Hiromi Uno and Shohei
Fujinaga for their laboratory assistance. Masayuki Itoh
generously provided his unpublished data on d13C of CO2.
The stable isotope analysis was conducted with Joint-Use
Facilities of the Center for Ecological Research, Kyoto
Open Access This article is distributed under the terms of the
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creativecommons.org/licenses/by/4.0/), which permits
unrestricted use, distribution, and reproduction in any medium,
provided you give appropriate credit to the original
author(s) and the source, provide a link to the Creative
Commons license, and indicate if changes were made.
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