Sources of nutrients behind recent eutrophication of Lago de Tota, a high mountain Andean lake

Abstract

Lago de Tota, the largest lake in Colombia, is the primary source of water for 250,000 people and a focus of regional economic activity in agriculture, aquaculture, and tourism. Recently, agencies and stakeholders report a shift from the naturally oligotrophic state toward eutrophy. However, the relative contributions of different inputs, including agricultural runoff, aquaculture and municipal wastewaters are unknown, hampering efforts to mitigate nutrient loading. We examined spatial and temporal variation in the trophic state of the lake over one year, as well as stable C and N isotopic profiles of aquatic producers and consumers in relation to two main potential sources (fertilizer and trout feed). We found that Lago de Tota is moderately eutrophic (average chlorophyll-a: 6.4 µg/L, TN: 1.5 mg/L and TP: 0.06 mg/L) with a 32% reduction of transparency over the last 15 years. δ¹⁵N and δ¹³C of aquatic organisms and surface sediments were enriched relative to prehistoric sediments, indicating that human sources dominate the C and N cycles of the lake. δ¹⁵N of macrophytes (15.7‰), particulate organic matter (12.5‰), and invertebrates (20.2‰) were enriched relative to trout food (4.6‰), but similar to chicken manure (13.7‰), suggesting that farming in the watershed may be a more important source of N than aquaculture. Our results indicate that Lago de Tota is on a trajectory toward eutrophication with potentially severe consequences for water resources in a rapidly developing mountain region.

Full text

Vol.:(0123456789)
1 3
Aquatic Sciences (2018) 80:39
https://doi.org/10.1007/s00027-018-0588-x
RESEARCH ARTICLE
Sources ofnutrients behindrecent eutrophication ofLago de Tota,
ahigh mountain Andean lake
NelsonJavierAranguren‑Riaño1· JonathanB.Shurin2 · AdrianaPedroza‑Ramos1· ClaudiaLilianaMuñoz‑López1·
RicardoLópez3· OmarCely3
Received: 6 October 2017 / Accepted: 6 August 2018
© Springer Nature Switzerland AG 2018
Abstract
Lago de Tota, the largest lake in Colombia, is the primary source of water for 250,000 people and a focus of regional eco-
nomic activity in agriculture, aquaculture, and tourism. Recently, agencies and stakeholders report a shift from the naturally
oligotrophic state toward eutrophy. However, the relative contributions of different inputs, including agricultural runoff,
aquaculture and municipal wastewaters are unknown, hampering efforts to mitigate nutrient loading. We examined spatial
and temporal variation in the trophic state of the lake over one year, as well as stable C and N isotopic profiles of aquatic
producers and consumers in relation to two main potential sources (fertilizer and trout feed). We found that Lago de Tota is
moderately eutrophic (average chlorophyll-a: 6.4µg/L, TN: 1.5mg/L and TP: 0.06mg/L) with a 32% reduction of transpar-
ency over the last 15years. δ15N and δ13C of aquatic organisms and surface sediments were enriched relative to prehistoric
sediments, indicating that human sources dominate the C and N cycles of the lake. δ15N of macrophytes (15.7‰), particu-
late organic matter (12.5‰), and invertebrates (20.2‰) were enriched relative to trout food (4.6‰), but similar to chicken
manure (13.7‰), suggesting that farming in the watershed may be a more important source of N than aquaculture. Our
results indicate that Lago de Tota is on a trajectory toward eutrophication with potentially severe consequences for water
resources in a rapidly developing mountain region.
Keywords Eutrophication· Water quality· Aquaculture· Stable isotopes· Colombia
Introduction
Eutrophication is a consequence of both lake aging (Lin-
deman 1942) and human activities that increase nutrient
loading. Cultural eutrophication remains a pervasive global
threat to water security, economic development and the
delivery of ecosystem services from freshwater environ-
ments (Carpenter etal. 1998; Smith and Schindler 2009).
High elevation lakes in many regions may be less vulnerable
to the effects of anthropogenic eutrophication because
cold temperatures and steep slopes make their watersheds
unsuitable for many agricultural and industrial activities
that generate nutrient runoff. Mountain lakes may receive
a larger proportion of nutrients from atmospheric transport
in dissolved and particulate forms (Sickman etal. 2003).
However, in the tropics, human settlement and farming can
extend to high elevations, leading to potential eutrophication
in mountain lakes at elevations that are less impacted by
watershed development at temperate latitudes (Catalan and
Donato Rondón 2016). Transitions to eutrophy may be dif-
ficult to reverse due to hysteresis driven by elevated internal
phosphorus loading from anoxic sediments (Carpenter etal.
2015), and the tendency for polymixis to make regenerated
P readily available (Lewis 1987). Anticipating and prevent-
ing such transitions may therefore be more effective than
restoring water quality once lakes enter a degraded state
(JØrgensen etal. 2013).
Lago de Tota (Boyacá, Colombia, Fig.1) is the largest
freshwater lake in Colombia with a surface area of 5620
Aquatic Sciences
* Jonathan B. Shurin
jshurin@ucsd.edu
1 Unidad de Ecología en Sistemas Acuáticos UDESA,
Universidad Pedagógica y Tecnológica de Colombia,
Avenida Central del Norte 39-115, Tunja, Boyacá, Colombia
2 Section ofEcology, Behavior andEvolution, University
ofCalifornia San Diego, 9500 Gilman Dr. #0116, LaJolla,
CA92093, USA
3 Corporación Autónoma Regional de Boyacá, Corpoboyacá,
Antigua vía a Paipa # 53-70, Tunja, Boyacá, Colombia

N.J.Aranguren-Riaño et al.
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39 Page 2 of 9
hectares and 1920million m3 of volume, located at an ele-
vation of 3015m in the eastern slope of the northern end
of the Andes mountain range. Lago de Tota is of tectonic-
glacial origin (Rangel and Aguirre 1983), and its watershed,
which reaches to 3700m of elevation, is heavily influenced
by past glaciation. Tota Lake is the primary source of water
for the city of Sogamoso (population: 113,000) as well as
a number of smaller towns and villages Agriculture in the
watershed consists primarily of green onion farming that has
expanded in recent decades. A number of large aquaculture
pens for rainbow trout cultivation are also present within
the lake, which is an attraction for regional tourism. The
lake has experienced a continuous descending trend in its
seasonal water levels associated with sustained extractions
for irrigation, industry, and urban supply and climate forc-
ing (Cañon and Valdes 2011). A 1983 report determined
that the oligotrophic state of Lago de Tota was at risk due
to agricultural and aquacultural activities in the watershed
and the lake (CAR 1983). Despite its size and importance,
no consistent sampling program is in place for monitoring
water quality in the lake.
Anecdotal evidence suggests a trend toward eutrophi-
cation in Lago de Tota. Beds of macrophytes, particularly
Egeria densa, have reportedly expanded, creating barriers
to navigation in the littoral zone. Water transparency has
also reportedly declined. Figure2 shows a comparison of
average Secchi disc transparency and the density of algal
cells from samples recorded in two sampling campaigns con-
ducted between 2002 and 2005 and 2012–2015. The results
of the second survey are reported in Muñoz-López etal.
(2017), while the earlier survey is unpublished data of N.A.
Between the two time periods, algal density increased more
Fig. 1 A map showing the location of Lago de Tota and our sampling sites, and a photo of the lake (photo credit: Marika Schulhof)
Fig. 2 a Comparison of algal
density (organisms/ml, where
organisms consist of single cells
as well as colonies) and b Sec-
chi disk transparency in samples
collected in two time periods
(2002–2005 and 2012–2015) in
Lago de Tota. Abundance was
estimated by chamber sedimen-
tation method and observation
under an inverted microscope
(Utermöhl 1958) as described
in Muñoz-López (2017). The
difference between the two
time periods is significant by
two-tailed t test (both variables
P < 0.0001)

Sources ofnutrients behindrecent eutrophication ofLago de Tota, ahigh mountain Andean lake
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Page 3 of 9 39
than five-fold and water transparency declined from 10 to
7m (Fig.2). The limited available information suggests a
path toward increasingly eutrophic state in Lago de Tota.
Three potential anthropogenic sources of nutrients may
contribute to the eutrophication of Lago de Tota. First,
untreated waste water originates from the town of Aquita-
nia (population 15,000) through the outlet of the La Mugre
stream on the eastern shore of the lake. Second, the domi-
nant land use in the watershed consists of extensive onion
farms fertilized by gallinaza, a fertilizer consisting mainly of
chicken manure. Third, twelve aquaculture pens for cultivat-
ing rainbow trout (Oncorhynchus mykiss, Walbaum 1792)
are present in the lake, concentrated mainly at the northern
end of the larger basin (Lago Grande). Lack of information
about the contributions of these three sources to declining
water quality in the lake hampers the implementation of
strategies to remediate the loading of nutrients and reduce
the risk of a transition to a eutrophic state with degraded
water quality.
We examined temporal and spatial variation in the trophic
state and limnological conditions of Lago de Tota over one
year. We also compared stable isotopic ratios for C and N
of particulate organic matter (POM, consisting mainly of
phytoplankton), littoral amphipods (Hyalella sp.), macro-
phytes and superficial sediments with two putative sources
of eutrophication: the chicken manure used to fertilize onion
farm fields throughout the water shed, and the feed provided
to rainbow trout in aquaculture pens situated in the surface
waters of the lake. Our goals were to determine (1) the cur-
rent trophic state of Lago de Tota and how it varies spatially
among sites and the two main basins of the lake (Lago Chico
and Lago Grande) and throughout the year, and (2) how
the isotopic signatures of contemporary organisms compare
to two of the main anthropogenic sources of nutrients that
have been implicated as potential drivers of eutrophica-
tion. Despite its tremendous importance to the regional and
national economy, little research has been conducted on the
Lago de Tota ecosystem. Our study represents a first attempt
at understanding the causes of ongoing changes in the lake
and its watershed.
Materials andmethods
We sampled ten stations in Lago de Tota eight times between
9th of September, 2014 and 3rd of September, 2015. Sam-
ples were collected approximately monthly until 25th of
November, 2014, and again after 13th of July, 2015. The
first sampling period occurred during the period of rela-
tively high water levels, and the second during lower lev-
els. Sampling stations were distributed throughout the two
main basins of the lake and in order to cover gradients of
proximity to the main population center (Aquitania, a town
of around 15,000 on the eastern shore of “Lago Chico”, the
smaller basin of the lake) and the zone with the greatest
concentration of trout aquaculture activity (the northern end
of “Lago Grande”, the larger basin). At each station, we
recorded water column depth and Secchi depth transparency.
Samples of a common benthic amphipod (Hyalella sp.) were
collected from several locations with a sweep net from the
littoral zone on the last sampling date, and surface sediments
were collected with a grab sampler. Samples of the fertilizer
used on onion crops and the feed used in trout farms were
acquired from farmers.
We collected water samples for nutrient, isotope and
chlorophyll analysis from the depth of Secchi transparency
(between 5 and 7m) using a Van Dorn sampler. Nutrient
samples were fixed in the laboratory with concentrated sul-
furic acid (approximately 12.5µL for sample to reduce pH
to 2) and refrigerated at 4°C until analysis (APHA 1976).
These were analyzed through flow injection analysis follow-
ing persulfate digestion using a QuikChem® autoanalyzer
equipped with TN and TP modules (Lachat instruments
USA, 2013). Chlorophyll-a samples were filtered in the field
using Advantec Glass Fiber that were kept in the dark at
− 70°C (APHA 1976). Chlorophyll was extracted from the
filter in the lab with ketone and the extracts were analyzed
through ultraviolet–visible spectroscopy using Jeffrey and
Humphrey’s (1975) trichromatic equation.
A sample of Particulate Organic Matter (POM) was fil-
tered into a pre-combusted Advantec (Vernon Hills, IL,
USA) 0.47µm Glass Fiber filters for stable C and N analysis.
Samples of macrophytes, particulate organic matter (POM),
littoral amphipods (Hyallela sp.), sediments, trout food and
agriculture fertilizer were dried in an oven at 50–60°C
for 12h, then ground, weighed to target weight for each
material, and encapsulated in tin (Sn) capsules for Carbon
(δ13C) and Nitrogen (δ15N) analysis at the U.C. Davis Stable
Isotope Facility. Isotope samples were analyzed using an
Elementar Vario EL Cube or Micro Cube elemental analyzer
and PDZ Europa ANCA-GSL elemental analyzer interfaced
to a PDZ Europa 20–20 isotope ratio mass spectrometer.
Stable isotope mixing models
In order to estimate the proportional contributions of
chicken manure and trout feed to POM, macrophytes and
invertebrates, we used a Bayesian mixing model based
on δ13C and δ15N implemented in the R package “simmr”
(Parnell 2016). Mixing models estimate consumer diets
and the incorporation of different sources of nutrients into
biological materials based on measured isotopic ratios.
Bayesian model frameworks incorporate variability in
both source and consumer isotopic ratios, and enrich-
ment fractions, in estimating proportional contributions to
properly account for all sources of error and uncertainty.

N.J.Aranguren-Riaño et al.
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39 Page 4 of 9
The models require assumptions about means and varia-
tion in C and N isotopic fractionation between consumers
and their sources which are based on values reported in
the literature (Phillips etal. 2014). The two sources in our
model were chicken manure and trout feed. For POM and
macrophytes, we assumed no fractionation upon uptake
(Moore etal. 2014), and the observed average and stand-
ard deviation of the measured δ13C and δ15N values of
the two sources. For invertebrates, we assumed an aver-
age trophic enrichment for 15N of 3.4‰ (standard devia-
tion = 1.0) and 0.4‰ for 13C (standard deviation = 1.3),
following Post (2002). Estimates of proportional contri-
butions of the two sources were based on 1000 Monte
Carlo Markov Chain simulations.
The trophic state of Lago de Tota was determined
by the Trophic State Index (TSI) of Carlson (1977),
modified for the tropics by Toledo etal. (1983) based
on Chlorophyll-a, Secchi disc transparency and total
phosphorus concentrations. The criteria for trophic state
assignments were: TSI > 44 = mesotrophic condition;
TSI > 54 = eutrophic condition.
Results
During the period of our study, the daily average TN con-
centration of Lago de Tota was 1.5mg/L (range 0.8 to
2.0mg/L), TP averaged 0.06mg/L (0.02–0.09mg/L) and
the average chlorophyll-a was 6.4µg/L (3.4–9.9µg/L). The
N/P ratio by weight ranged among dates 18.1 to 35.7 among
sampling dates (averaged across sites on each date), with an
average value of 25.3.
The concentrations of chlorophyll and nutrients varied
in space and time (Fig.3). Chlorophyll-a concentration
was greater in the first sampling period in 2014 than in
2015, and often higher in Lago Chico (the smaller east-
ern basin) than Lago Grande. The highest chlorophyll
concentrations were often observed near the outflow of
the La Mugre stream near the town of Aquitania on the
eastern shore. The lowest nutrient concentrations were
observed in 2014. Higher TN concentrations were often
found in Lago Chico, while TP was often greater in Lago
Grande, the larger western basin of the lake (Fig.3). The
trophic index of the lake varied between mesotrophic and
eutrophic states during the duration of the study (Fig.4).
The Secchi disc transparency indicated that the lake was
Fig. 3 Maps of Total Nitrogen (TN), Total Phosphorous (TP) and
chlorophyll-a concentration in the surface waters of Lago de Tota at
ten stations on eight sampling dates. The size of each circle is pro-
portional to the concentration, and raw values are provided in the
Supplementary Information. The point on the bottom right of each
row indicates the size of the point corresponding to the concentration
shown in mg/L (for TN and TP) and µg/L (for chlorophyll-a)

Sources ofnutrients behindrecent eutrophication ofLago de Tota, ahigh mountain Andean lake
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Page 5 of 9 39
persistently eutrophic at all sites, while chlorophyll-a and
TP most often fell within the mesotrophic range (Fig.4).
Both C and N isotopes were most enriched in littoral
amphipods and macrophytes, followed by POM and the
lowest in superficial sediments (Fig.5). Chicken manure
had isotopic ratios very similar to those of POM and mac-
rophytes, with similar δ13C to trout feed but more enriched
δ15N values. Trout feed and farm soils showed similar δ13C
to both POM and macrophytes, but were more depleted
δ15N by around 7–10‰. Amphipods had more enriched
δ13C and δ15N values than either of the sources, or any of
the other materials analyzed. Sediments from a paleo-lim-
nological study by Cardozo etal. (2014) (dated between
4000 and 2000 YBP, and labeled “Ancient sediments”
in Fig.5) were much more depleted in heavy isotopes of
both C and N, with δ15N values centered around 2 and
δ13C around − 30. The C:N atomic ratio of the surface
sediments (10.1, SD = 2.2) were similar to those of the
ancient sediments (11.7, SD = 0.9) sampled by Cardozo
etal. (2014). The C:N ratios of the other materials were
8.9, SD = 2.0 (macrophytes), 9.1, SD = 2.0 (POM), 3.9,
SD = 0.5 (amphipods), and 11.2, SD = 1.8 (soil).
The stable C and N isotopic signatures of different
organismal groups also varied through time. Figure6
shows the δ13C and δ15N profiles for each sampling date,
with POM, chicken manure and trout feed highlighted
in color. The δ15N of POM was more similar to chicken
manure than trout feed during most of the sample period,
Fig. 4 Trophic status indices based on chlorophyll-a, total phosphorus and Secchi disc transparency for the ten sample sites in Lago de Tota. The
horizontal lines at 44 and 54 indicate the boundaries between oligotrophic, mesotrophic and eutrophic states
Fig. 5 Carbon and Nitrogen stable isotopes of organisms (inverte-
brates, macrophytes and POM consisting mainly of phytoplankton),
superficial and ancient sediments, along with two potential anhropo-
genic sources (chicken manure and trout feed). Each type of mate-
rial is averaged over multiple samples collected through time over
the course of our survey. The arrows show the difference in position
between POM and the two potential sources, and the ancient sedi-
ments as an indicator of the pre-settlement isotopic ratios of the lake.
Ancient settlement ratios were taken from sediment cores collected
by Cardozo etal. (2014) dated between 2000 and 4000 YBP

N.J.Aranguren-Riaño et al.
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39 Page 6 of 9
but became more depleted on certain dates (e.g., Septem-
ber 24, 2014).
The Bayesian stable isotope mixing model estimated
that chicken manure contributed 87.2% of POM mass (SD
= 3.5%), 98.3% (SD = 1.1%) of macrophyte biomass, and
97% (SD = 2.1%) of invertebrate biomass (Fig.7).
Discussion
Our study shows several indications that nutrient inputs
have contributed to recent eutrophication of Lago de Tota,
and that the lake may therefore be at risk for transition to a
persistent eutrophic lake with a large increase in algal abun-
dance and macrophyte bed expansion in recent decades.
First, deep mountain lakes of the tropics such as Tota are
typically oligotrophic (Löffler 1962; Lewis 1987; Catalan
and Donato Rondón 2016). However our research indicated
that chlorophyll and nutrient levels of Lago de Tota were
in the mesotrophic to eutrophic range, which is evident in
the increase of the phytoplankton biomass expressed as
biovolume (Muñoz-López etal. 2017). Second, carbon and
nitrogen stable isotopic signatures of phytoplankton, mac-
rophytes and invertebrates were all enriched relative to val-
ues for aquatic ecosystems with low levels of anthropogenic
nutrient impacts, as well as pre-settlement sediments from
Lago de Tota. In addition, δ15N of aquatic organisms were
also elevated compared to the feed used in trout aquaculture
in the lake, but similar to chicken manure applied to green
onion crops in the watershed. These results indicate that
onion agriculture in the watershed may contribute the bulk
of nutrients supporting elevated productivity in the Lake.
Nitrogen isotopic ratios have a long history as indicators
of eutrophication and runoff in aquatic ecosystems (Cabana
and Rasmussen 1996; Fry 2006), and the δ15N of organ-
isms in Lago de Tota provide strong indication of major
human influence. For instance, Cabana and Rasmussen
(1996) showed that herbivorous zooplankton consumers
have δ15N ratios around 2–5 in lakes with the lowest human
population density in their watersheds, while in the most
impacted lakes have invertebrate ratios are around 10–13.
Littoral amphipods from Lago de Tota have δ15N around
20, indicating high anthropogenic contributions. A survey of
species-specific δ15N signatures of pelagic zooplankton from
Lago de Tota showed a range from 16.0 for Ceriodaphnia
to 20.2 for Boeckella (Nidia Gil, unpublished data). Thus,
the δ15N of the Tota Lake pelagic and benthic invertebrates
is on par with some of the most eutrophic lakes globally.
The amphipods in our data set also show highly enriched
δ13C signatures, indicating that they may rely on unknown
Fig. 6 Stable carbon and nitrogen isotopes signatures through time.
The orange “+” symbol indicates the mean of POM samples, and
the chicken manure and trout feed are shown in blue and green,
respectively. The symbols indicate the other points indicate the type
of material as follows: POM (+), littoral amphipods (squares), mac-
rophytes (triangles), superficial aquatic sediments (×) and soil (dia-
monds)

Sources ofnutrients behindrecent eutrophication ofLago de Tota, ahigh mountain Andean lake
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Page 7 of 9 39
aquatic or terrestrial carbon sources. In addition, our δ15N
ratios of POM (12.5) and macrophytes (15.7) are similar to
or slightly higher than values observed in aquatic systems
with the greatest contributions wastewater to the dissolved
inorganic nitrogen (DIN) pool (Fig.5 in Cole etal. 2005).
Carbon is less often used as an indicator of eutrophication
than nitrogen; however, a variety of evidence suggests that
δ13C signatures are also reliable indicators of eutrophica-
tion in aquatic ecosystems. Oczkowski etal. (2014) show
that δ13C increased with coastal phytoplankton productivity
in experiments and observations (see also Voss and Struck
1997). The enriched C isotopic ratios of producers and
consumers observed in Lago de Tota also indicate elevated
productivity due to human influence, and are heavier than
those found in ancient sediments from before extensive agri-
cultural development in the watershed (Cardozo etal. 2014).
Carbon and nitrogen isotopic signatures also provide
some insight into the contributions of two putative sources
of nitrogen supporting eutrophication in Lago de Tota: onion
crops and trout aquaculture. We found that fertilizers used
in onion crops (chicken manure) and the food provided to
trout in aquaculture enclosures had similar δ13C signatures
between − 22 and − 24; however, chicken fertilizer was more
enriched in heavy nitrogen, with a mean δ15N of 13.7, com-
pared with trout feed with a ratio of 4.6. Bayesian mixing
models estimated a dominant role for terrestrial agriculture
relative to insitu trout aquaculture in supporting growth
of algae, aquatic plants and invertebrates. Although these
ratios and the mixing models suggest a greater contribution
of terrestrial agriculture than aquaculture as a source of N
to organisms in the lake, a number of outstanding questions
remain before the importance of different sources can be
confidently inferred.
First, the roles of urban waste waters in fertilizing Lago
de Tota remain unclear. The largest town in the watershed is
Aquitania on the eastern shore, with a population of 15,000.
Agriculture is the dominant land use in the watershed, with
extensive green onion crops extending to the shores of the
lake. Wastewater typically contains nitrogen with δ15N of 6
or greater (Moore etal. 2014), which is similar to the sig-
nature of trout feed and lower than that of chicken manure.
The spatial pattern of POM and nutrients suggest that the
town of Aquitania may be a contributor of nutrients, with
elevated levels occurring periodically in the eastern basin of
the lake near the outlet of the La Mugre stream. For instance,
nitrogen concentrations were substantially elevated at the
site closest to Aquitania on September 9 and October 31,
2014, and August 13, 2015 (Fig.3) compared to other sam-
pling stations in the lake. Urban wastewaters may therefore
play some role in eutrophication of the lake, but cannot be
included in the mixing models because their isotopic signa-
tures are unknown.
Fig. 7 Results of mixing models showing the posterior distributions
of estimated percent contributions of chicken manure and trout feed
to POM (a) and the tissues of macrophytes (b) and littoral inverte-
brates (c) based on Monte Carlo Markov Chain simulations. The anal-
yses were performed using the simmr package in R (Parnell 2016)

N.J.Aranguren-Riaño et al.
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39 Page 8 of 9
Second, stimulation of microbial processes such as deni-
trification within the lake may elevate δ15N relative to pri-
mary sources. Dentrification in low oxygen conditions pro-
duces substantial enrichment in δ15N (Altabet etal. 1995),
therefore the signatures of organisms in Lago de Tota may
reflect processing of nitrogen within the lake that leads to
enrichment with 15N rather than external sources. We found
that the surface waters of lake were generally saturated with
oxygen; however, denitrification in the sediments may affect
the N isotopic signatures of POM or macrophytes. Frac-
tionation on uptake may also enrich the nitrogen isotopes
of phytoplankton or macrophytes (Fry 2006). In addition,
Lago de Tota may be more sensitive to internal phosphorus
loading due to its long renewal time of 30years (Cañón and
Rodríguez 2002). Phosphorus recycling from anoxic sedi-
ments may maintain high productivity even if external inputs
are limited (Carpenter etal. 1999). The observed daily aver-
age TN:TP ratio by weight among all of our samples ranged
from 18.1 to 35.7 with a mean of 25.3. Phosphorus limi-
tation of phytoplankton growth typically occurs at TN:TP
ratios above ~ 22 by mass (Guildford and Hecky 2000), indi-
cating that primary productivity of Lago de Tota is most
likely phosphorus limited. Thus, although the nitrogen in
producers may be of primarily terrestrial origin, the major
sources of P to the lake remains remain to be determined.
Finally, the contributions of agriculture and aquaculture
to the nutrient budget of Lago de Tota may vary spatially
and temporally. For instance, while the δ15N of POM was
on average closer to that of chicken manure, during some
sampling periods the ratio became more depleted and more
similar to that of trout feed. For instance, on September 24,
2014 the δ15N of POM was closer to that of trout feed, sug-
gesting that aquaculture may play a significant role during
certain periods of the year. Sustained spatial and temporal
sampling is needed to construct a detailed budget of nutri-
ents throughout the watershed in order to identify and under-
stand the causes of changes occurring in Lago de Tota.
The composition of the phytoplankton community also
indicates that Lago de Tota is entering a eutrophic state.
A recent survey by Muñoz-López etal. (2017) of Lago de
Tota over a year found that limnological conditions were
related to nutrients dynamics, particularly Total Nitrogen,
which is influenced by seasonal level water variation. Sec-
ond, they surveyed the functional traits of phytoplankton
community and showed that the dominant morphological
functional groups are typical of enriched systems, For exam-
ple flagellated algae and diatoms contributed more biovol-
ume in the smaller basin “Lago Chico” where trophic state
indicators like TP were generally greater. These groups are
often associated with high TP concentration in eutrophic
lakes of Colombia (Duque and Donato-Rondón 1992) and
other regions (Kruk etal. 2010). In addition, Muñoz-López
etal. (2017) found that photic zone depth was the strongest
environmental predictor of the functional traits of the Lago
de Tota phytoplankton community over an annual cycle,
indicating that changes in lake trophic status has a large
influence on the traits of pelagic primary producers.
High-altitude lakes like Lago de Tota are typically oligo-
trophic with cold temperatures and low nutrients concentra-
tions (Catalan and Donato Rondón 2016). Allochthonous
organic matter and atmospheric deposition represent the
principal sources of carbon and nitrogen (Auguet etal. 2011;
Catalan and Donato Rondón 2016). Eutrophication of alpine
lakes has mainly been studied in the context of atmospheric
deposition of dissolved and particulate nutrients in temperate
regions (Sickman etal. 2003); however, in the tropics, high
elevation systems may be at risk from watershed sources as
well. For instance, Lake Titicaca in Bolivia has undergone
eutrophication as a result of expansion of mining activities
and accompanying urban population growth (Archundia
etal. 2017). Our results indicate that Lago de Tota is pres-
ently in a mesotrophic to eutrophic state, and may be at risk
of transition to a similar degraded state.
Despite its regional and national importance as a source
of water resources and focus of economic activities in agri-
culture, aquaculture and tourism, almost no information is
available about the status of Lago de Tota or its trajectory
through time. Our study is the first to show human disruption
of the nutrient cycles of the lake and its watershed, and our
data raise concern about the risk of potential catastrophic
loss of water resources in this mountain region. Studies of
potential nutrient retention mechanisms and wastewater
treatment to control runoff from farms and towns in the
watershed are badly needed to insure that Lago de Tota does
not undergo transition to a degraded eutrophic state. Such a
loss of water resources could be severely economically and
socially costly in a developing region that is vulnerable to
water and food insecurity.
Acknowledgements The Corpoboyacá and Fulbright Colombia pro-
vided funding for our project. We thank Alejandra Jiménez and Nidia
Gil for helpful assistance in field.
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