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Stable isotope analysis confirms substantial differences between subtropical and temperate shallow lake food webs

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Differences in trophic web structure in otherwise similar ecosystems as a consequence of direct or indirect effects of ambient temperature differences can lead to changes in ecosystem functioning. Based on nitrogen and carbon stable isotope analysis, we compared the food-web structure in a series of subtropical (Uruguay, 30–35°S) and temperate (Denmark, 55–57°N) shallow lakes. The food-web length was on average one trophic position shorter in the subtropical shallow lakes compared with their temperate counterparts. This may reflect the fact that the large majority of subtropical fish species are omnivores (i.e., feed on more than one trophic level) and have a strong degree of feeding niche overlap. The shapes of the food webs of the subtropical lakes (truncated and trapezoidal) suggest that they are fuelled by a combination of different energy pathways. In contrast, temperate lake food webs tended to be more triangular, likely as a result of more simple pathways with a top predator integrating different carbon sources. The effects of such differences on ecosystem functioning and stability, and the connection with ambient temperature as a major underlying factor, are, however, still incipiently known.
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PRIMARY RESEARCH PAPER
Stable isotope analysis confirms substantial differences
between subtropical and temperate shallow lake food webs
Carlos Iglesias .Mariana Meerhoff .Liselotte S. Johansson .
Ivan Gonza
´lez-Bergonzoni .Ne
´stor Mazzeo .Juan Pablo Pacheco .
Franco Teixeira-de Mello .Guillermo Goyenola .Torben L. Lauridsen .
Martin Søndergaard .Thomas A. Davidson .Erik Jeppesen
Received: 14 December 2015 / Revised: 4 June 2016 / Accepted: 6 June 2016
ÓSpringer International Publishing Switzerland 2016
Abstract Differences in trophic web structure in
otherwise similar ecosystems as a consequence of
direct or indirect effects of ambient temperature
differences can lead to changes in ecosystem func-
tioning. Based on nitrogen and carbon stable isotope
analysis, we compared the food-web structure in a
series of subtropical (Uruguay, 30–35°S) and temper-
ate (Denmark, 55–57°N) shallow lakes. The food-web
length was on average one trophic position shorter in
the subtropical shallow lakes compared with their
temperate counterparts. This may reflect the fact that
the large majority of subtropical fish species are
omnivores (i.e., feed on more than one trophic level)
and have a strong degree of feeding niche overlap. The
shapes of the food webs of the subtropical lakes
(truncated and trapezoidal) suggest that they are
fuelled by a combination of different energy pathways.
In contrast, temperate lake food webs tended to be
more triangular, likely as a result of more simple
pathways with a top predator integrating different
carbon sources. The effects of such differences on
ecosystem functioning and stability, and the connec-
tion with ambient temperature as a major underlying
factor, are, however, still incipiently known.
Keywords Food-web structure Food-web length
Omnivory Ecosystem functioning
Introduction
The height and shape of trophic webs may potentially
affect the entire ecosystem functioning (Post et al.,
Handling editor: Katya E. Kovalenko
C. Iglesias (&)M. Meerhoff
I. Gonza
´lez-Bergonzoni N. Mazzeo
J. P. Pacheco F. T. Mello G. Goyenola
Grupo de Ecologı
´a y Rehabilitacio
´n de Sistemas
Acua
´ticos, Departamento de Ecologı
´a Teo
´rica y Aplicada,
Centro Universitario de la Regio
´n Este-Facultad de
Ciencias, Universidad de la Repu
´blica, Tacuarembo
´s/n
CP 20000, Maldonado, Uruguay
e-mail: caif@cure.edu.uy
C. Iglesias M. Meerhoff L. S. Johansson
I. Gonza
´lez-Bergonzoni T. L. Lauridsen
M. Søndergaard T. A. Davidson E. Jeppesen
Department of Bioscience, Aarhus University,
Vejlsøvej 25, 8600 Silkeborg, Denmark
I. Gonza
´lez-Bergonzoni
Departamento de Ecologı
´a y Evolucio
´n, Facultad de
Ciencias Universidad de la Repu
´blica, Montevideo,
Uruguay
T. L. Lauridsen T. A. Davidson E. Jeppesen
Arctic Research Centre, Aarhus University, Building
1110, C. F. Møllers Alle 8, 8000 Aarhus, Denmark
T. L. Lauridsen M. Søndergaard E. Jeppesen
Sino-Danish Education and Research Centre, Beijing,
China
123
Hydrobiologia
DOI 10.1007/s10750-016-2861-0
2000; Woodward, 2009; Emmerson, 2012). Particu-
larly, the number of steps involved in the transfer of
energy from primary producers to top predators, i.e.,
the food-web length (hereafter FWL), seems at least
partly determined by ecosystem productivity and size,
ambient temperature, habitat heterogeneity, and
changes in species richness (including arrival and loss
of species). These variations may occur among, but
also within, ecosystems across temporal and spatial
scales [as described in the pioneer works by Elton
(1927) and Lindeman (1942) and reviews by Doi et al.
(2012), Pimm (1991), and Post (2002a)]. However, a
global-scale analysis showed that lake and stream
FWL exhibited no direct or, at most, a weak relation-
ship with ecosystem size, mean annual air tempera-
ture, or latitude; however, there was a tendency for
FWL to be longer at high latitudes than in the tropics
(Vander Zanden & Fetzer, 2007).
Theoretical analyses (Arim et al., 2007a,b; Post &
Takimoto, 2007) and modeling exercises (Takimoto
et al., 2012) suggest that the length and also the
connection strength within a food web may be
explained, at least in part, by the degree of omnivory
of intraguild predators (IGP) (Post & Takimoto, 2007;
Takimoto et al., 2012). Widespread feeding on lower
trophic positions would result in shorter FWL (Lay-
man et al., 2005; Post & Takimoto, 2007), a
phenomenon termed the ‘‘omnivory mechanism’
(Post & Takimoto, 2007). In contrast, addition of
species with potentially different diets, as expected in
subtropical regions where fish richness and specific
and functional diversity are far higher than in similar
temperate shallow lakes (Teixeira-de Mello et al.,
2009), could result in longer FWL [the ‘‘addition
mechanism’’ sensu Post & Takimoto (2007)]. Thus,
contrasting scenarios, indirectly linked to the climate
regime, could emerge depending on the predominance
of each mechanism. However, empirical evidence of
the relationships between omnivory and specific
richness and FWL, and the relative importance of
the underlying mechanisms, is still scarce (Glazier,
2012).
The shape of food webs also responds to the
occurrence of different types of primary producers.
When several resources co-occur, more complex
pathways for the transfer of energy and matter may
exist (Polis & Strong, 1996; Vadeboncoeur et al.,
2005). Such multiple pathways may occur in shallow
lakes where both pelagic primary production (by
phytoplankton) and littoral or benthic primary pro-
duction (by periphyton) can be important sources of
energy (Vadeboncoeur et al., 2003; Vander Zanden
et al., 2011). However, the extent to which the
different basal resources are exploited might be
indirectly linked to differences in ambient temperature
(Meerhoff et al., 2007). Changes in the width of the
carbon resources (carbon range, sensu Layman et al.
(2007)), together with the occurrence of complex
pathways, could thus be found in different lake types
and under different climate regimes.
To elucidate variations in the length and shape of
trophic webs from shallow lakes in two regions with
distinct climates, we analyzed stable isotopes (d
15
N,
d
13
C) of key biological communities of the food web
in five subtropical (Uruguay, 30–35°S) and four
temperate (Denmark, 55–57°N) shallow lakes. Con-
sidering the greater fish species richness of subtropical
systems, we expected that longer FWL and a wider use
of carbon sources would occur, if the ‘‘addition
mechanism’’ prevails. Alternatively, FWL might be
shorter in the subtropics, if the expected higher degree
of omnivory and its consequent effects at the com-
munity level predominate in the set of studied lakes.
Methods
Study sites
We selected five shallow lakes located along the east
coast of Uruguay covering a wide range in trophic
states and water transparency (Table 1). The lakes
represent the typical variability in the trophic state of
Uruguayan shallow lakes (Kruk et al., 2009; Pacheco
et al., 2010). For the comparison, we used data from
four lakes representative of shallow lakes in Denmark,
selected to ensure, to as high an extent as possible,
comparability with the Uruguayan lakes regarding
trophic state and key limnological characteristics, an
exception being size that was somewhat smaller in the
temperate region.
Field sampling
The samples were collected at the end of the growing
season (late summer) in both countries (March in
Uruguay, August in Denmark). A similar sampling
protocol was used in both countries and included an
Hydrobiologia
123
intensive sampling of the pelagic and littoral habitats
to obtain taxa representing all trophic levels and
carbon sources. For stable isotope analyses (SIA), we
collected samples of the principal consumers in both
pelagic and littoral areas. To ensure a sufficient
amount of organisms for the analysis, lake water was
pumped through conical plankton nets (20 and 65 lm
for phytoplankton and zooplankton, respectively),
macrophyte-associated macroinvertebrates and ben-
thic macroinvertebrates were sampled by intensively
swiping a hand net and by integrating several dredges
covering the entire bottom of each lake, respectively.
Fish were captured with multimesh-size gillnets and
electrofishing; the sampling effort used included the
deployment of several gillnets which were set over-
night. Electrofishing was conducted in the littoral
areas at sunset to capture small specimens and littoral
sit-and-wait predators. This combined sampling
method can appropriately capture the structure of the
target community in both studied regions (Teixeira-de
Mello et al., 2009), fact confirmed as we found species
a priori unknown to be in the studied systems. All
samples were rapidly frozen and transported to the
laboratory.
Following recommendations by Post (2002b),
principal carbon source signals from the pelagic and
littoral areas were indirectly estimated from the two
well-known primary consumers (as substitution for
primary producers), namely filter-feeding bivalves
and grazing snails (Post, 2002b). The selection of the
right baseline individuals is essential for the estima-
tion of an ‘‘average’’ food-web length in the commu-
nity, and the selection of gastropods and bivalves
seems the best strategy as they are long-living and low
dispersion organisms representing two contrasting
energy uptake pathways (Post, 2002b; Jardine et al.,
2014). Macrophyte leaves and periphyton washed
from the predominant macrophytes were also
sampled.
Sample processing for isotopic analysis and data
analysis
In the laboratory, samples of plants, periphyton,
phytoplankton, zooplankton, macroinvertebrates, fish
flank muscle, and snail and bivalve soft tissue were
freeze dried and ground to a fine powder for
stable isotope analysis (SIA). Each sample (1–3 mg,
weighed to 0.01 mg precision) was transferred to tin
capsules and analyzed at the UC Davis Stable Isotope
Facility (University of California, USA) for carbon
and nitrogen stable isotopes. The food-web structure
of each lake was visualized by plotting the trophic
position (based on d
15
N isotopic signature values)
against d
13
C values for all available organisms (Fry,
1991).
We estimated the trophic position of each individ-
ual according to Post (2002b):
Table 1 Main limnological features of the subtropical and temperate study lakes measured simultaneously with the stable isotope
sampling or according to the already published results (Pacheco et al., 2010)
Vaeng Tranevig Gammelmose Denderup Cisne Diario Garcia Clotilde Blanca
Area 15 2.7 1.3 4.6 127 101 13.5 29 60
Z
max
1.7 0.9 1.6 1.9 3.2 1.7 2 3.1 2.5
SD 0.9 0.75 1.3 1.8 0.4 1.05 1.7 1.8 0.64
Temp 17 16.6 16.4 16.3 13.1 19.2 16.3 17.6 19.6
pH 7.9 7.6 8.1 8.1 7.1 7.3 6.32 7 7.4
Cond 268 71 595 171 210 348 142 360 320
Chl-a 65.8 37.6 78.5 7.2 6 10 2 2.3 38.6
PVI 0 44 3 27 0 40 5 28 13
TP 113 60.5 157 54 413 75.8 29.8 27.7 51.9
TN 1018 1040 2212 664 1048 825 332 451 1017
Lake area (ha), maximum depth, Zmax (m), Secchi depth, SD (m), summer values of temperature, Temp (°C), conductivity, Cond
(lScm
-1
), percentage of lake volume inhabited by submerged plants, PVI (%), phytoplankton biomass as chlorophyll-a
concentration, Chl-a (lgl
-1
), and water concentrations of total phosphorus, TP (lgl
-1
), and total nitrogen, TN (lgl
-1
). Lakes are
ordered by decreasing fish richness in both regions (Table 2)
Hydrobiologia
123
Trophic position TrPoðÞ¼½ðd15Nconsumer
d15Nbase Þ=2:98þ2;
where d
15
N
consumer
is the isotopic signature of each
individual analyzed and d
15
N
base
is the averaged
baseline organisms (bivalves and snails), 2.98 is the
expected d
15
N fractionation per trophic level (Van-
derklift & Ponsard, 2003), and 2 is the theoretical
trophic level of baseline organisms (Post, 2002b). We
estimated the FWL as the maximum trophic position
for each lake.
In addition to FWL, we also calculated community-
wide metrics (Layman et al., 2007; Jackson et al.,
2011) to identify key features of the specific food
webs: (i) carbon range (CR), which is the difference
between the most d
13
C-enriched and the most d
13
C-
depleted values, for both the total consumer food web
(excluding basal resources) and per trophic level
(CR2, CR3); (ii) total area of the web (TA), measured
as the convex hull area given by all species in the d
13
C-
TrPo biplot and by the adjustment of the standard
ellipse areas (SEA) in the biplot; and (iii) the mean
nearest neighbor distance (NND), as the mean of the
Euclidean distances to the nearest neighbor of each
species in the biplot. CR indicates the amplitude of the
carbon resources being used; TA and SEA represent a
measure of the total amount of niche space occupied
by the trophic web, whereas smaller NND values
indicate redundancy of species with similar trophic
ecology. Although both TA and SEA represent the
trophic niche space occupied by communities, ellipse-
based SEA are developed in a Bayesian framework,
rendering this method unbiased with respect to sample
size and thus more robust than the convex hull area-
based TA metrics (Jackson et al., 2011). Despite that
the estimation of these metrics is usually made using
raw d
15
N (Layman et al., 2007), they have also been
estimated by standardizing d
15
N to trophic web length.
We used the latter method in our study as it shows
reduced variability in d
15
N due to factors other than
trophic fractionation (e.g., Gonza
´lez-Bergonzoni
et al., 2014).
We calculated these parameters using SIAR and
SIBER packages in R software and PAST software
(Hammer et al., 2001) and tested for differences
between climate zones in the measured trophic web
attributes (i.e., FWL, CR, TA, SEAb, and NND) using
the Mann–Whitney nonparametric test. Spearman
correlations among FWL, fish richness, CR,
ecosystem size (i.e., lake surface area), and lake
pelagic productivity (using phytoplankton Chl-a con-
centration as a proxy) were also calculated.
Results
FWL was, on average, one trophic position shorter in
the subtropical lakes than in the temperate lakes
(Table 2; Fig. 1). There was no significant correlation
between FWL and ecosystem size and pelagic pro-
ductivity (inferred using Chl-a concentration as
proxy). Mean fish richness was greater in the subtrop-
ical than in the temperate lakes (9.5 ±1.5 and
5.3 ±1.1 SE species per lake, respectively) and was
significantly correlated with both ecosystem size
(r
2
=0.82) and pelagic productivity (r
2
=0.67).
The subtropical fish assemblages included several
relatively small-sized omnivorous species of which
Jenynsia multidentata Jenyns, 1842 and Cnesterodon
decemmaculatus Jenyns, 1842 were the most abundant
(Table 3). Several potentially piscivorous species
(Teixeira-de Mello et al., 2009) like Australoheros
facetus Jenyns, 1842, Hoplias malabaricus Bloch,
1794, Oligosarcus jenynsii Gu
¨nther, 1864, Rhamdia
quelen Quoy & Gaymard, 1824, and Synbranchus
marmoratus Bloch, 1795 were also frequently
observed (Table 3). Among the piscivores, H. mal-
abaricus did not reach the top of the food web but held
the same trophic position as small-sized omnivores
(Table 3). In contrast, O. jenynsii always occurred at
the highest trophic level. Remarkably, the small-sized
J. multidentata, usually classified as omni-planktivore
(Goyenola et al., 2011), exhibited high mean d
15
N
values in all systems (Table 3). Shrimps, in particular
Palaemonetes argentinus Nobili, 1901, occurred in all
the subtropical lakes and, was abundant in four of the
lakes where they occupied the 3
rd
trophic position
along with predatory macroinvertebrates and several
omnivorous fish species.
Notwithstanding their relative paucity of species,
temperate fish assemblages (Table 4) consisted
roughly of the same trophic groups that characterized
the subtropical communities caught during this study.
Potential piscivores were abundant, including Esox
lucius L., Perca fluviatilis L., and Anguilla anguilla L.
(Table 4). Several fish species held higher trophic
positions (around 4th trophic position) than observed
in the subtropical lakes. Esox lucius was the apical
Hydrobiologia
123
species in the food web in two out of the four lakes,
with values close to the 6th trophic position (corre-
sponding to one individual; Table 4), and was not
lower than the 4th position in any of the lakes. In one
lake, both P. fluviatilis and Tinca tinca L. occupied
higher trophic positions than E. lucius, likely reflect-
ing the overall small body size of the latter (Table 4).
Taking the food webs as a whole, the overall mean
d
13
C carbon range (CR) was slightly (though not
statistically significant) wider in the warmer lakes,
being 8.7 in the subtropical and 7.5 in the temperate
lakes (Table 2). The carbon range per distinct trophic
level showed some variation between regions: no
significant differences appeared at trophic position 2
(primary consumers), but CR was twice as wide at
position 3 (secondary consumers) in the subtropical
lakes (Z=1.96, P=0.05; Table 2).
Temperate trophic webs typically had a triangular
convex hull area, whereas the subtropical webs were
typically trapezoid shaped (Figs. 1,2), being shorter
and wider at the 3rd trophic position (Table 3; Fig. 2).
Also SEAb captured the differences in trophic niche
space between the regional food webs, the minor and
major axes being more similar in the temperate lakes,
whereas a larger area towards the major axis was
occupied in the subtropical systems (Fig. 3). Surpris-
ingly, TA did not show statistically significant differ-
ences between climate zones, in contrast to SEAb
(Z=2.32, P=0.02; Table 2; Fig. 2). The nearest
neighbor distance (NND) was significantly shorter in
the subtropical lakes (Z=1.98, P=0.05; Table 2).
Discussion
Results based on SIA showed large differences in
trophic web structure between comparable shallow
lakes from regions with contrasting climates. In
particular, food-web length was shorter in the sub-
tropical than in temperate shallow lakes, supporting
the second of the contrasting hypotheses. This finding
cannot be ascribed to differently sized top predators in
each climate region as large fish specimens, usually
classified as piscivores or omni-benthi-piscivores
(Teixeira-de Mello et al., 2009; Gelo
´s et al., 2010),
occurred in both the regions. However, in the
subtropical lakes, the trophic position of larger fish
was similar to that of smaller-sized species and in
Table 2 Fish species richness (FR) and community-wide metrics from subtropical (above) and temperate (bottom) lakes, calculated
based on the distribution of species in the d
13
C-d
15
N biplots (Fig. 1)
Lake FR* FWL* CR CR 2 CR 3* SEAb* TA NND*
Cisne 13 4.0 7.7 4.5 3.5 5.2 35.2 0.4
Diario 11 3.4 9.7 9.7 5.9 4.2 27.6 0.4
Garcia 11 3.9 9.9 9.4 7.6 5.8 29.7 0.6
Clotilde 9 4.1 8.5 7.7 5.1 5.4 30.1 0.6
Blanca 4 4.4 7 7 3.4 5.2 17.2 0.7
UY Median 11 4.0 8.5 7.7 5.1 5.2 29.7 0.6
Range 4–13 3.4–4.4 7.0–9.9 4.5–9.7 3.4–7.6 4.2–5.8 17.2–35-2 0.4–0.7
Vaeng 8 5.1 4.9 4.3 2.6 6.8 58.7 0.6
Tranevig 6 5.8 10.5 7.3 0.6 6.8 45.7 0.9
Gammelmose 4 4.6 4.6 4.4 3.0 6.7 18.3 1.2
Denderup 3 4.4 9.9 9.9 4.1 6.6 36.7 0.6
DK Median 5 4.8 7.4 5.9 2.8 6.75 41.2 0.8
Range 3–8 4.4–5.8 4.6–10.5 4.3–9.9 0.6–4.1 6.6–6.8 18.3–58.7 0.6–1.2
Z
value
1.85 2.2 0.1 0.7 1.96 2.32 1.35 1.98
P0.06 0.02 0.9 0.5 0.05 0.02 0.18 0.05
Food web length (FWL), maximum trophic position for each lake, carbon range (CR), standard ellipse areas (SEAb), total area (TA),
convex hull area encompassed by all species, and mean nearest neighbor distance (NND) values are shown. Median and range for
each climate area are provided together with the results of statistical analyses, indicating significant (P\0.05) or marginally
significant (0.05 \P\0.10) differences (*) between locations (Mann–Whitney non parametric tests). Lakes are ordered by
decreasing FR in both the regions
Hydrobiologia
123
Hydrobiologia
123
some cases similar to that of predatory macroinverte-
brates. Such an apparent mismatch between measured
and expected trophic positions for large predatory fish
has previously been reported for some tropical rivers
(Layman et al., 2005), where the wide variation in
trophic position of tropical predatory fish was sug-
gested to be due to multiple feeding strategies, which
typically occur in low latitude species-rich systems
(Layman et al., 2005). Large-sized tropical piscivores
usually feed on the most abundant items of prey,
typically detritivorous species, which gives them a
short trophic position, only two trophic steps away
from basal resources such as detritus (e.g., Watson
et al., 2013; Jardine, 2016).
Concerns may arise regarding the application of
nitrogen stable isotopes for estimation of trophic web
length using a single average trophic fractionation
value, as trophic fractionation is not truly constant
throughout the whole food web (Bunn et al., 2013). In
streams and rivers, it has been shown that trophic steps
between algae and grazing macroinvertebrates can
produce average trophic enrichment values as low as
0.6%, and 1.6%enrichment between grazing and
predator macroinvertebrates, whereas the trophic
enrichment between invertebrate and fish compart-
ments can range from approximately 2.2–3.9%.By
using an average trophic enrichment of 2.98%from a
meta-analysis specifically arrayed for lake systems
(Post, 2002b), we assumed that there were no differ-
ences in trophic enrichment created by climate regions
and that the number of trophic steps between inver-
tebrate and fish compartments was the same in both.
This seems reasonable as there is no evidence for
differential trophic fractionation in different regions of
the world (e.g., Bunn et al., 2013) and as we found
both grazing and predatory macroinvertebrates in both
the regions. Thus, we have no reason to suppose that
the observed differences can be caused by factors
other than the higher average number of trophic steps
in the temperate than in the subtropical lakes. In fact,
our study might overestimate the maximum trophic
position in some Uruguayan lakes as herbivorous and
omnivorous fish usually enrich their N signature by
4%with respect to algae (Bunn et al., 2013). This
probably explains the surprisingly elevated trophic
position observed here when using the lower average
trophic enrichment value of Post,(2002b). Another
potential methodological limitation in the use of
stable isotopes in trophic position estimates is the fact
that stable isotopes reflect dietary assimilation in the
last sampling weeks/months (Heady & Moore, 2012),
whereas there are well-known seasonal changes in
feeding strategies of fish in both subtropical and
temperate regions, for example, towards higher veg-
etal consumption by several omnivores in summer
(Persson, 1986; Gonza
´lez-Bergonzoni et al., 2016).
We aimed to avoid the bias of different time frames in
the fish stable isotopes by conducting the sampling
during the same season (the end of the growing/
reproductive season) in both the regions.
As expected from earlier studies (e.g., Lazzaro
et al., 2003; Meerhoff et al., 2007; Gonza
´lez-Ber-
gonzoni et al., 2012), we also observed higher fish
species richness in the subtropical lakes. Fish richness
was positively correlated with both lake surface area
and pelagic primary producer biomass as expected
from the richness–productivity and richness–ecosys-
tem size relationships (Rosenzweig, 1995; Lawton,
1999; Dodson et al., 2000). According to the proposed
insertion and addition mechanisms (Post, 2002a),
additional (including higher) trophic levels might be
expected as more fish species occur in the subtropical
food webs. However, we observed shorter FWLs in the
subtropical lakes, suggesting that other mechanisms
prevailed. One such mechanism could be a different
degree of omnivory, which is a predominant charac-
teristic of subtropical and tropical fish assemblages
(e.g., Jepsen & Winemiller, 2002; Lazzaro et al., 2003;
Meerhoff et al., 2007). An increase in the proportion of
herbivorous fish species has been observed with the
decreasing latitude and increasing water temperature
in a variety of aquatic ecosystems worldwide (Gonza
´-
lez-Bergonzoni et al., 2012), concurring at community
level with predictions of the Metabolic Theory of
Ecology (Brown et al., 2004) suggesting that energy
limitation may lead to enhanced omnivory to satisfy
the boosted metabolic needs (Brown et al., 2004; Arim
bFig. 1 Stable isotope-based biplots showing the convex hull
areas encompassing all fish species. Left temperate lakes, right
subtropical lakes. The diagrams show trophic position (inferred
from d
15
N) against d
13
C signals. For fish, each point represents
the mean value of 2–20 individuals of different sizes. Herb.
Invert. and Carn. Inv. are the averages of all invertebrate
specimens as assigned to each particular trophic group
according to the literature (herbivorous, invertivorous, or
carnivorous). Gaster and Bival are the averages of Gastropoda
and Bivalvia in each lake (baseline signals of littoral and pelagic
food webs in the calculations). Error bars represent ±1SE.
Lakes are ordered by decreasing fish richness in both the regions
(Table 2)
Hydrobiologia
123
Table 3 Fish species from the Uruguayan (subtropical) lakes used for the stable isotope analyses
Species Cisne Diario Garcı
´a Clotilde Blanca
nMean TrPo nMean TrPo nMean TrPo nMean TrPo nMean TrPo
Australoheros facetus* Jenyns, 1842 1 3.1 3.69 10 5.8 3.62 1 2.6 3.34
Hoplias malabaricus* Bloch, 1794 3 5.2 3.23 5 30.2 4.31
Oligosarcus jenynsii* Gu
¨nther, 1864 2 12 3.66 10 12.7 3.55 10 8.6 4.02 9 16.9 4.65
Rhamdia quelen* Baird & Girard, 1854 4 4 3.59 6 3.9 3.69
Synbranchus marmoratus* Bloch, 1795 6 24.3 3.85
Characidium rachovii Regan, 1913 6 2.7 3.24
Corydoras paleatus Jenyns, 1842 1 3.5 4.03
Astyanax sp. Baird & Girard, 1854 8 5.8 3.30 3 2 3.4 10 3.5 3.63
Cheirodon interruptus Jenyns, 1842 1 2.76 10 4 3.16 6 4.7 3.53
Cnesterodon decemmaculatus Jenyns, 1842 10 2.6 3..47 3 2.5 3.66 10 2.4 3.57 1 1.8 3.79
Diapoma terofali Ge
´ry, 1964 10 4.6 3.25 10 5.6 3.26
Gymnogeophagus cf. meridionalis 8 3.4 3.37 15 3.7 3.78
Hyphessobrycon anisitsi Eigenmann, 1907 2 3.7 3.53
Hyphessobrycon boulengeri Eigenmann, 1907 1 3.7 3.76
Heptapterus mustelinus Valenciennes, 1835 1 2.6 3.9
Heterocheirodon yatai Casciotta,
Miquelarena & Protogino, 1992
2 4.1 3.22
Hyphessobrycon luetkenii Boulenger, 1887 8 5 3.51
Jenynsia multidentata Jenyns, 1842 10 2.8 3.49 10 4.3 3.78 9 3.6 4.06 11 3.6 4.38
Phalloceros caudimaculatus Hensel, 1868 3 2.2 3.21 2 2.2 3.42
Pimelodella australis Eigenmann, 1917 2 4 3.89
Pseudocorynopoma doriae Perugia, 1891 6 4.5 3.29
Steindachnerina biornata Braga & Azpelicueta, 1987 10 9.9 2.67 9 11.7 2.55 6 10.1 3.13
Hypostomus commersoni Valenciennes, 1836 2 4.1 4.69
Hisonotus sp. Eigenmann, 1889 5 5.2 3.2
Parapimelodus valenciennis Lu
¨tken, 1874 1 15.1 2.95
The number of analyzed specimens (n), mean body length, and estimated trophic position (TrPo) are shown. * Potentially piscivorous species. Lakes are ordered by decreasing
fish richness (Table 2)
Hydrobiologia
123
et al., 2007a). A diverse diet that incorporates a higher
amount of different items (Arim et al., 2007a), and
enhanced feeding on lower trophic positions (Beisner
et al., 1997; Petchey et al., 1999), could potentially
satisfy the greater energy demands of organisms at a
given trophic position under higher ambient
temperatures.
Regarding the carbon range, we found similar
values at the base of the trophic web in the two
climatic zones, indicating a similar use of carbon
sources (i.e., phytoplankton and periphyton) by pri-
mary consumers. However, at the secondary consumer
level (CR3), the carbon range was significantly
broader in the subtropical lakes, pointing to a mixture
of simultaneously occurring strategies where some
taxa have a lower integration of carbon sources, while
other co-occurring taxa integrate several carbon
sources (Fig. 3). Fish reliance on periphyton as a
major carbon source has previously been demon-
strated in shallow temperate lakes; its importance
depends, however, on water clarity and the consequent
relative importance of benthic primary and secondary
production (Vander Zanden & Vadeboncoeur, 2002;
Jones & Waldron, 2003). In our subtropical systems,
many species occupied an intermediate position
(secondary consumers) in the food web (i.e., several
fish species and shrimps) and may act as additional
pathways for the different carbon sources (Post &
Takimoto, 2007). Therefore, intermediate consumers
could enhance the transfer of basal carbon to higher
trophic positions without adding more trophic links to
the web. In addition, higher functional redundancy in
warmer lakes was evidenced here by a closer nearest
neighbor distance (NDD), meaning that more species
occupied similar trophic web positions in the subtrop-
ical compared to the temperate lakes.
As a consequence of the shorter FWL in the
subtropical lakes and the suggested differences in
energy pathways in the different climate zones, the
shapes of the food webs (depicted by the convex hull
shapes and community-wide metrics) differed
between the two climatic regions studied (see
Fig. 2). Our results suggest that temperate trophic
webs are characterized by multichain omnivory [IGP
module, sensu Vadeboncoeur et al. (2005)], with one
top predator integrating the different carbon sources
fuelling the web (mainly represented here by phyto-
plankton and periphyton and with an intermediate
d
13
C value). Conversely, in the subtropical lakes, the
Table 4 Fish from the Danish (temperate) lakes used for the stable isotope analyses
Species Vaeng Tranevig Gammelmose Denderup
nMean TrPo nMean TrPo n Mean TrPo nMean TrPo
nAbramis brama L. 28 9.2 3.68 11 24.2 4.47
Esox lucius* L. 7 33.8 4.87 1 50.8 5.82 1 38 4.59 4 14.4 3.37
Perca fluviatilis* L. 43 12.7 4.36 17 13.5 4.35 32 16.2 3.95
Rutilus rutilus L. 60 15 4.38 12 14.7 4.34
Scardinius erythrophthalmus L. 31 9 3.33 21 13.5 4.13 6 12.9 4.33
Carassius carassius L. 1 15 3.61
Gymnocephalus cernua L. 1 7 3.26 4 34.6 4.23
Tinca tinca L. 2 41 4.36 8 45.4 4.76 7 45.4 3.52
Anguilla anguilla* L. 9 44.3 4.3
The number of analyzed specimens (n), mean body length, and estimated trophic position (Tr Po) are shown. * Potentially piscivorous species. Lakes are ordered by decreasing
fish richness (Table 2)
Hydrobiologia
123
Fig. 2 Trophic diversity for the set of shallow lakes in
Denmark (triangles) and Uruguay (circles), depicted by Total
Convex Hull area (full lines) and Standard Bayesian Ellipses
(SEA; dotted lines). Both representations graphically captured
the higher trophic positions in the temperate systems. However,
only the SEA analysis was able to statistically express the
differences (Table 2)
Fig. 3 Conceptual models of trophic web functioning in the
temperate (left) and subtropical (right) lakes inferred from d
13
C-
TP biplots and community-wide metrics. The arrows above the
model indicate lowering of one trophic position occurring
concomitantly with a widening of the carbon range at the third
level of the chain. R1 and R2, phytoplankton and periphyton,
respectively; PC, primary consumers; SC, secondary con-
sumers; IC, intermediate consumers; TP, top predators; CR,
total carbon range; CR3 and CR2, the carbon range that reaches
the trophic positions of primary and secondary consumers;
FWL, food-web length
Hydrobiologia
123
occurrence of a combination of multichain and single-
chain omnivory, and the resultant more complex
energy transfer pathways, might explain the commu-
nity metrics (particularly CR3) and the shapes
observed. The higher strength of the IGP module,
together with a more reticulated topology of the
trophic web in the warmer lakes (Meerhoff et al.,
2007), may account for both the lower realized trophic
web length and the wider CR in higher trophic
positions (and the same basal range) in such lakes.
Our results should be interpreted with caution due
to possible limitations of the applied methodology (for
instance, the assumption of a constant fractionation
rate or the appropriateness of baseline value calcula-
tions) or by excluding effects of fish foraging behavior
(Lazzaro et al., 2009) and fish-induced stoichiometry
alterations as those described by Danger et al. (2009).
Nevertheless, they provide empirical evidence for
previously raised hypotheses suggesting that the
structure and interactions of the trophic webs in
subtropical lakes are more complex than those in cold
temperate ones (Lazzaro et al., 2003; Meerhoff et al.,
2007; Jeppesen et al., 2012).
We are also proposing here a conceptual model
rising the principal differences between trophic webs
in both the regions and the underlying forcing
mechanisms occurring (Fig. 3); however, we still lack
complete understanding of how such differences in
food-web shape affect, for instance, the biomass of
particular communities and biotic interactions at given
trophic levels as well as how lake ecosystem func-
tioning, resilience, and stability (Post & Takimoto,
2007) are affected.
Acknowledgments We are grateful to Anne Mette Poulsen
for manuscript editing and to Tinna Christensen for improving
the figures. We also thank Frank Landkildehus, Kirsten
Landkildehus Thomsen, and Mette E. Bramm in Denmark;
and Juan M. Clemente, Claudia Fosalba, Soledad Garcı
´a,
Nicolas Vidal, Natalia Barbera
´n, Malvina Masdeu, Mariana
Vianna, and Alejandra Kroger in Uruguay, for valuable field
assistance. The project was supported by the Ministry of
Science, Technology and Innovation of Denmark. EU-WISER
and EU-REFRESH, ‘‘CLEAR’’ (a Villum Kann Rasmussen
Centre of Excellence project), CRES, CIRCE, and The Research
Council for Nature and Universe (272-08-0406 and FNU
16-7745) supported EJ. CI was supported by a PhD
Scholarship from Aarhus University-Danish Research Agency.
NM was supported by Maestrı
´a en Ciencias Ambientales, and
NM, MM, and CI were supported by PEDECIBA. NM, MM,
FTM, and CI were supported by SNI (ANII) and MM also by
ANII-FCE 2009-2749 and the L
´Ore
´al-UNESCO (supported by
DICYT) for Women in Science national award. We deeply
acknowledge the constructive comments of two anonymous
reviewers and the handling editor Katya Kovalenko.
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... Phytoplankton growth can also be controlled directly (grazing) or indirectly (trophic cascades) by zooplankton and fish communities (see, for example, the reviews by Sommer et al., 2012 andGer et al., 2016). Most of the data available on this issue are for temperate freshwater ecosystems, but it has been shown that the food webs in shallow lakes display significant differences between subtropical and temperate areas (Iglesias et al., 2017). For example, omnivory is a dominant characteristic of subtropical and tropical fish communities, and omnivorous fish upregulate and downregulate phytoplankton, particularly by the direct ingestion of these microorganisms or by cascade effects (e.g., Lazzaro, 1997;Lazzaro et al., 2003: Ferrao-Filho et al., 2020Mayer, 2020;Moustaka-Gouni and Sommer, 2020). ...
Preprint
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Given the increasing eutrophication of water bodies in Africa due to increasing anthropogenic pressures, data are needed to better understand the responses of phytoplankton communities to these changes in tropical lakes. These ecosystems are used by local human populations for multiple purposes, including fish and drinking water production, potentially exposing these populations to health threats if, for example, an increase in toxic cyanobacterial blooms is associated with increasing eutrophication. To test the short-term response of the phytoplankton community to the addition of nutrients (phosphorus and nitrogen, alone or in combination) and Nile tilapia, we developed an in situ mesocosm experiment in a freshwater lagoon located near Abidjan (Ivory Coast). We found that phytoplankton growth (estimated by chlorophyll-a quantification) was highly stimulated when both nitrogen and phosphorus were added, while there was no clear evidence for such colimitation by these two nutrients when considering their concentrations in the lagoon. Phytoplankton growth was accompanied by significant changes in the diversity and composition of this community and did not lead to an increase in the proportions of cyanobacteria. However, the addition of fish to some mesocosms resulted in a drastic decrease in phytoplankton biomass and a dominance of chlorophytes in this community. Finally, these experiments showed that the addition of nitrogen, alone or combined with phosphorus, stimulated microcystin production by cyanobacteria. In addition, no evidence for microcystin accumulation in the fish was found. Taken together, these data allow us to discuss strategies for controlling cyanobacterial blooms in this tropical ecosystem.
... once the system has shifted to a turbid state (Beklioğlu, et al., 2011). Food webs are substantially different (Iglesias, et al., 2017), and several critical feedback mechanisms known to stabilise clear water conditions in shallow cold temperate lakes may not be as important or even present in their warm tropical and subtropical counterparts. For instance, the effects of macrophytes on trophic interactions seem to be much more complex in tropical and subtropical lakes, where large numbers of small omnivorous fish live closely associated with them (Meerhoff, et al., 2003). ...
Thesis
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Freshwater lakes are among the most important ecosystems for both human and other biological communities. They account for about 87% of surface freshwater in the planet, thus constituting a major source of drinking water. They also provide a wide range of ecosystem services that go from the sustenance of a rich biodiversity to the regulation of hydrological extremes; from the provision of a means for recreation to the support of local economies, e.g., through tourism and fisheries, just to cite a few. Lakes are now also widely recognised as natural early warning systems, their responses potentially being effective indicators of local, regional and global scale phenomena such as acidification and climate change, respectively. This is because of their high sensitivity to environmental factors of the most diverse nature that can rapidly alter the course of their evolution. Examples of this are the observed abrupt shifts between alternative stable states in shallow lakes, which led them to become the archetype, go-to example in alternative stable state theory. Therefore, attaining a good scientific understanding of the many processes that take place within these ecosystems is fundamental for their adequate management. Among the tools that serve this purpose, ecological models are particularly powerful ones. Since their introduction in the 1960s, the development of mechanistic ecological models has been driven by their wide spectrum of potential applications. Nevertheless, these models often fall into one of the two following categories: overly simplistic representations of isolated processes, with limited potential to explain real-world observations as they fail to see the bigger picture; or overly complex and over-parameterised models that can hardly improve scientific understanding, their results being too difficult to analyse in terms of fundamental processes and controls. Moreover, it is now well known that an increased complexity in the mechanistic description of ecological processes, does not necessarily improve model accuracy, predictive capability or overall simulation results. To the contrary, a simpler representation allows for the inclusion of more links between model components, feedbacks which are usually overlooked in highly-complex models that partially couple a hydro-thermodynamic module to a biogeochemical one. However, ecological processes are now known to have the potential to significantly alter the physical response of aquatic ecosystems to environmental forcing. For example, steadily increasing concentrations of coloured dissolved organic carbon, a process known as brownification (also browning), as well as the intense phytoplankton blooms that characterise lakes undergoing severe nutrient enrichment, a process known as eutrophication, have been shown to have the potential to alter the duration of the stratified period, thermal structure and mixing regime of some lakes. In this thesis, with the aim of addressing the limitation of partially-coupled models to account for such feedbacks, we further develop a process-based model previously reported in scientific literature. Subsequent studies have already built upon this model in the last few years. In Chapter 2, we do so too by integrating hydro-thermodynamics and biogeochemistry in a reduced complexity framework, i.e., customising the model so that each version only includes the fundamental processes that, brought together, sufficiently describe the studied phenomena. Two case studies served the purpose of testing the adaptability and applicability of the developed model under different configurations and requirements. Limnological data for these two studies were measured at high spatial and temporal resolutions by means of an automated profiling system and recorded as part of two large-scale mesocosm experiments conducted in 2015 and 2016 at the IGB LakeLab in Lake Stechlin, Brandenburg, Germany. Meteorological datasets were also made available to us for both periods by the German Federal Environment Agency. The scope of the first experiment, which we describe in Chapter 3, was that of detecting any changes attributable to eutrophication and browning, in the competition for nutrients and light between four different groups of lake primary producers. These four groups are phytoplankton, periphyton, epiphyton and macrophytes. The model version for this study, therefore, includes equations for all four groups. By tailoring the model to these very specific needs with relative ease, we demonstrate its versatility and hint at its potential. The second experiment, described in Chapter 4, sought to shed light on the largely unknown effects of an increase in the diffuse luminance of the night sky that is due to artificial light at night (artificial skyglow) on lake metabolic rates, i.e., gross primary productivity, ecosystem respiration and net ecosystem productivity (the difference between the first two). For this purpose, an empirical equation for dissolved oxygen concentration was included, the parameters of which were estimated by means of a Markov Chain Monte Carlo sampling method within a Bayesian statistical framework, showing the compatibility, with these statistical methods, of our otherwise fully deterministic model. In Chapter 5, we present a theoretical study on the ecological controls of light and thermal patterns in lake ecosystems. A series of simulations were performed to determine in which cases ecological processes such as eutrophication and brownification may have an observable effect on the physical response of lakes to environmental forcing, which we assessed along a latitudinal gradient. Results show that, in general, across all examined latitudes, and consistent with previous studies, accounting for phytoplankton biomass results in higher surface temperatures during the warm-up phase, slightly lower water temperatures during the cool-down phase, and a shallower thermocline throughout the entire stratified period. This effect is relatively more important in eutrophic lakes where intense blooms are likely. This importance, however, decreases as lakes get browner. Finally, in line with the overall scope of the SMART EMJD, in Chapter 6 we illustrate the case of Ypacaraí Lake, the most important lake in landlocked Paraguay, hoping to provide an example of how interdisciplinary research and international intersectoral collaboration can help bridge the gap between science and management of freshwater ecosystems. This lake presents very special hydro-ecological conditions, such as very high turbidity that can impair phytoplankton growth despite its nutrient-based trophic state indices having consistently fallen within the hyper-eutrophic range in recent years. A strong interest in its complex functioning, through modelling, was taken early on. This led to a collaborative research line being established among several public and private institutions in Italy, Germany and Paraguay. Results so far include: • three concluded UniTN Master theses in Environmental Engineering, partly developed in Paraguay, the first two in collaboration with the “Nuestra Señora de la Asunción” Catholic University (UCNSA) and the third one with the National University of Asunción (UNA); • a collaborative UCNSA-UniTN research proposal submitted for consideration to receive funding through the PROCIENCIA Programme of the National Council of Science and Technology of Paraguay (CONACYT); and • the first multidisciplinary review that has ever been published about the case of Ypacaraí Lake, which highlights the importance of such a collaborative and integrative approach to further advance scientific knowledge and effectively manage this ecosystem.
... A change in diet toward more herbivory with increasing water temperature has been observed at individual, population, and community levels (González-Bergonzoni et al. 2016) following intraannual variations. Food webs in tropical and subtropical lakes are thus more truncated than food webs in similar temperate shallow lakes, as found in comparative studies (Iglesias et al. 2017). Different indicators of fish predation suggest a stronger effect of fish on prey communities such as zooplankton under warmer climates . ...
Article
Despite its well-established negative impacts on society and biodiversity, eutrophication continues to be one of the most pervasive anthropogenic influence along the freshwater to marine continuum. The interaction between eutrophication and climate change, particularly climate warming, was explicitly focused upon a decade ago in the paper by Moss et al. (2011), which called for an integrated response to both problems, given their apparent synergy. In this review, we summarise advances in the theoretical framework and empirical research on this issue and analyse the current understanding of the major drivers and mechanisms by which climate change can enhance eutophication, and vice versa, with a particular focus on shallow lakes. Climate change can affect nutrient loading, through changes at the catchment and landscape levels by affecting hydrological patterns and fire frequency, and through temperature effects on nutrient cycling. Biotic communities and their interactions can also be directly and indirectly affected by climate change, leading to an overall weakening of resilience to eutrophication impacts. Increasing empirical evidence now indicates several mechanisms by which eutrophying aquatic systems can increasingly act as important sources of greenhouse gases to the atmosphere, particularly methane. We also highlight potential feedbacks between eutrophication, cyanobacterial blooms, and climate change. Facing both challenges at the same time is more pressing than ever. Meaningful and strong measures at the landscape and water body levels are therefore required if we are to ensure ecosystem resilience and safe water supply, conserving biodiversity, and decreasing the carbon footprint of freshwaters.
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Invasive apple snails adversely impact the ecological function of non-native habitats, resulting in eutrophication as well as reduced biodiversity, which diminishes ecosystem goods and services, thereby [negatively] impacting human well-being. The onus here is to define the diet of an invasive apple snail (Pomacea canaliculata) in native (Maldonado, Uruguay) versus non-native habitats (Hangzhou, China, and Oahu, HI, USA). Diets for apple snails, in five sites, within both native and non-native habitats were defined via SIAR (Stable Isotope Analysis in R) with δ13C and δ15N stable isotope data collected therein. SIAR models indicate P. canaliculata shift diet from generalist (where myriad plant species comprise relatively small proportions of overall diet) to a specialist diet (where plants species constitute much larger proportions of said diet). What may be more telling is that in (anthropogenically disturbed) portions of the native habitat, and progressively more so in non-native habitats, invasive apple snail diets are increasingly composed of aquatic plants. The inherent and pronounced dietary differences amongst pristine and anthropogenically disturbed native habitats, as well as non-native habitats, provide a mechanism that may elucidate the variable ecological impacts of invasive apple snails within native and non-native habitats.
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To investigate the potential long-term consequences of environmental warming in subtropical systems, we compare the trophic structure of shallow lakes in tropical and subtropical regions. In total, 25 meso-eutrophic lakes with piscivorous fish were sampled during summer along a latitudinal gradient in South America. The fish catch per unit of effort and the omnivorous fish to zooplankton biomass ratios were significantly lower in the tropical lakes. Despite the lower fish biomass, no significant difference was found in zooplankton or phytoplankton communities or in the zooplankton to phytoplankton biomass ratio between the two sets of lakes. Nevertheless, regression models based on the combined dataset show higher cyanobacteria and total phytoplankton biomass at lower zooplankton to phytoplankton biomass ratio and higher omnivorous fish to zooplankton biomass ratio. Cyanobacteria biomass was dominated by non bloom-forming taxa and was inversely related to the biomass of calanoid copepods suggesting that these herbivores may play an important role in controlling edible cyanobacteria in warm shallow lakes. Overall, our results, however, suggest that warming will have relatively minor impacts on the pelagic trophic structure of shallow subtropical lakes supporting the idea of weaker trophic cascades in warm (sub)tropical lakes in comparison to temperate ones.
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Body size is usually considered a good indicator of trophic position in fish communities. Indeed, the proverbial wisdom that “Big Fish Eat Little Fish” is consistent with observations from marine systems where systematic removal of the largest individuals has occurred, with cascading effect in the ecosystems. Trophic cascades are also well documented in temperate lakes but may not be as pronounced in (sub)tropical lakes due to higher degree of fish omnivory. We analysed fish communities along a climatic gradient and showed the classical correlation between body size and relative trophic position disappears in warmer climates where large fish appear to be feeding systematically on the lowest trophic levels. This concurs with experimental findings demonstrating that omnivorous fish tend to include more plant and less animal matter in their diet at higher temperatures. Accordingly, the community-wide trophic web indicators, calculated based on stable isotopes (δ¹³C and δ¹⁵N), showed that the average degree of trophic diversity declined from cold to warm lakes and that the trophic webs become more truncated towards warmer climates. This has implications for lake restoration approaches in warmer climates and in temperate lakes within the context of global warming.
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The effects of energy on food web structure have been debated for at least 80 years. Nevertheless, the empirical evidence is meager, especially from terrestrial ecosystems. We analyzed long‐term temporal variation in food chain length in a semiarid continental ecosystem, where productivity shows large interannual variations. Incidence of nonherbivorous prey in predator diet was used as a proxy of trophic position, allowing us to analyze the effect of productivity on food chain length within the assemblage of top predators (which comprises the most abundant and persistent top predators in the system) and to compare observed patterns at the species and assemblage levels. At the species level, the relationship between trophic position and productivity took different forms, varying in magnitude and shape. This pattern contrasts with the consistent increase in food chain length, with productivity observed at the assemblage level. Our results indicate that productivity can be a main determinant of food chain length, but not necessarily because of energy limitation. Further, the increase in food chain length with available energy probably represents an aggregate attribute, driven to a large extent by predators with higher consumption rates, rather than being the result of compensatory responses among predators.
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Emergent properties of food webs, including food-chain length (FCL), may differ across latitudinal gradients because of strong differences in biodiversity and productivity between warm and cold regions. Theory predicts long food chains in the tropics because of high species richness and productivity, but empirical data suggest otherwise. Here I show that an opportunistic top predator common to coastal rivers and streams, the Australian Longfinned Eel (Anguilla reinhardtii), feeds similar to 1 trophic position higher in temperate systems (4.7 +/- 0.3 [SD]) than in tropical systems (3.8 +/- 0.5). This result suggests shorter food chains that contain a diverse array of large-bodied herbivores and omnivores that act as prey for generalist predators, such as eels, in tropical systems. The resulting altered size spectrum limits the size and trophic position of top predators that can be supported in the face of constraints from known limits to FCL, including productivity, ecosystem size, and disturbance. This framework has general application for food webs and suggests unique structural and functional attributes of highly threatened tropical freshwater ecosystems.
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The trophic structure of fish assemblages often varies seasonally, following the changes in food availability and supposedly water temperature. To unveil potential drivers of trophic shifts, we studied changes in fish trophic structure at both whole-assemblage and species levels at contrasting food availability and water temperatures in a subtropical stream. We analysed the diet of the most abundant omnivorous species (Bryconamericus iheringii) monthly along the year, searching for relationships with environmental variables changing seasonally (i.e. temperature and water level) and with fish reproductive stage. We ran a single-species food choice field experiment with fixed animal and vegetal food availability in contrasting seasons to test food availability as driver of diet shifts. At the assemblage level, we found a higher consumption of vegetal during summer, reflecting the increased proportion of vegetal in the diet of omnivores, which dominated the assemblage. At the species level, the enhanced vegetal consumption was related to increases in temperature and reduction in water level. Moreover, fish selected for vegetal during summer and for animal food in winter under experimental conditions. Our findings support the role of temperature driving food web dynamics by increasing fish herbivory towards warmer scenarios, with potential strong implications for whole-assemblage trophic structure.
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Using stable nitrogen and carbon isotope signatures, we investigated the trophic ecology and identified potential prey fish groups supporting the giant Arapaima within floodplain lakes of the Essequibo River basin in southwestern Guyana. Morphological descriptions of feeding structures and digestive tract are presented together with preliminary data on Arapaima diets. Stable isotope results suggest that algivorous/detritivorous and omnivorous fishes contributed most to Arapaima biomass, and generally, that was consistent with what is known about Arapaima diets. Stable nitrogen isotope ratios for piscivorous fishes in these lakes were higher than nitrogen isotope ratios for Arapaima, indicating that piscivorous fishes are unlikely to constitute a major source of energy for Arapaima. This population of Arapaima has an intestine averaging 1.45 times total body length, relatively small teeth, and numerous, closely-spaced gill rakers. These morphological features, together with isotope data, support our inference that Arapaima are secondary consumers and may be better characterized as omnivores and not top predators.
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1. Climate warming in (sub)arctic regions is expected to increase freshwater fish overwinter survival and dispersal, potentially with strong implications for macroinvertebrate assemblage composition and ecosystem processes. Several studies worldwide have shown large effects of top predators (usually fish) on macroinvertebrates in streams. However, the influence of top predators on trophic diversity, the range of food resources exploited and trophic niche redundancy is less well studied, particularly in cold regions. 2. Using stable isotopes (13C and 15N) and fish gut content analysis, we investigated the effect of top predators on macroinvertebrate food webs in streams in Greenland by comparing adjacent sites with and without fish (Gasterosteus aculeatus). 3. Food-web metrics estimated from stable isotope data showed that the presence of fish reduced the diversity of food sources exploited by macroinvertebrates as well as their trophic diversity. In addition, fish presence increased packing and trophic redundancy of macroinvertebrate taxa in the food web, possibly due to behavioural changes in foraging activity. Furthermore, predatory macroinvertebrate taxa were unable to attain the trophic position of fish so that food webs were one trophic level longer in streams with fish. Focusing on macroinvertebrate food webs alone, predatory macroinvertebrates did not change their trophic position in the presence of fish. 4. Filter feeders dominated the macroinvertebrate assemblage when fish were present, while the relative abundance of collector-gatherers was marginally higher in the fishless streams. This pattern was consistent with stronger selectivity for collector-gatherers by fish. 5. Climate-driven fish colonisation in currently fishless Greenland streams may induce a shift in macroinvertebrate food webs, with a reduction in both trophic diversity and the variety of food sources consumed. To some extent, this might counteract a change towards a broader use of food resources by macroinvertebrates that might otherwise be expected at higher temperatures. In addition, a shift in the macroinvertebrate assemblage towards dominance of filter feeders can be expected to promote an increase in periphyton biomass in streams with fish.