Hydrobiologia

DOI 10.1007/s10750-015-2298-x

PHYTOPLANKTON & SPATIAL GRADIENTS

Cyanobacterial water bloom of Limnoraphis robusta

in the Lago Mayor of Lake Titicaca. Can it develop?
Jarka Komárková . Haydée Montoya .
Jiřı́ Komárek

Received: 19 December 2014 / Revised: 16 April 2015 / Accepted: 18 April 2015

Ó Springer International Publishing Switzerland 2015

Abstract Cyanobacterial blooms are commonly nitrogen-poor habitats. In 2014, filaments of this
associated with high concentrations of nutrients in cyanobacterium appeared also in plankton and peri-
waters. An exception among the species forming phyton in the Bay of Puno, Lake Titicaca, Peru.
heavy water blooms is Limnoraphis robusta Komárek Accessible data on water chemistry, chlorophyll
et al. (Fottea 13:39–52, 2013). Until now, heavy water a concentration, and phytoplankton composition were
blooms of this species were found only in tropical, compared with those from Lake Atitlán, Guatemala,
rather oligotrophic waters. Filaments of L. robusta where this cyanobacterium formed a thick brownish
contain diazocytes and thus are able to fix molecular layer on the water surface in 2008, 2009 and 2011.
nitrogen during night. This ability gives L. robusta an Except for shallow bays, both lakes (Atitlán and Lago
advantage over other phytoplankters to explore Mayor of Titicaca) are still oligotrophic in some
periods, and phytoplankton growth is limited by lack
of nitrogen. In this paper, we are discussing factors
Guest editors: Luigi Naselli-Flores & Judit Padisák /
Biogeography and Spatial Patterns of Biodiversity of
which might allow development of heavy bloom of
Freshwater Phytoplankton this cyanobacterium in the Lago Mayor and other clear
parts of the Lake Titicaca.
Electronic supplementary material The online version of
this article (doi:10.1007/s10750-015-2298-x) contains supple- Keywords Titicaca Lake
Cyanobacterial water
mentary material, which is available to authorized users.
bloom
Limnoraphis robusta
Diazocytes
Atitlán
J. Komárková (&) Lake
N:P ratio
Biology Centre, Institute of Hydrobiology, Czech
Academy of Sciences, Na Sádkách 7,
370 01 České Budějovice, Czech Republic
e-mail: [email protected]
Introduction
J. Komárková
J. Komárek
Institute of Botany, Czech Academy of Sciences,
Water bloom of cyanobacteria is a conspicuous
Dukelská 135, 37982 Třeboň, Czech Republic
e-mail: [email protected] phenomenon and thus thousands of references are
registered in literature. Appearance of water blooms is
H. Montoya commonly joined to increasing concentrations of
Universidad Nacional Mayor de San Marcos - Museo de
nutrients in waters, mainly connected with human
Historia Natural, Av. Arenales 1256,
Apartado 14-0434 Lima 14, Peru activities—discharge of sewage to recipients, imple-
e-mail: [email protected] mentation of fertilizers in agriculture, inappropriate

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management of land and the like. Much attention is collection of samples from the littoral zone of floating
paid to cyanobacterial water blooms because of their isles of dry Schoenoplectus californicus (C.A. Mayer)
dangerous toxicity, their mass production often evok- Soják, ssp. totora. We collected two samples of
ing anoxia connected with adverse impacts upon fish phytoplankton: at 9 o’clock when entering the Bay and
stocks and basic changes in water quality. Problems at about 13 o’clock when going back from the Bay.
associated with toxins (which can be present both in Conditions at the time of sampling statement were as
the biomass and water) are especially important when follows: the temperature of water was 14 and 19°C, pH
the water body is used as a source of drinking water 6.7 and 8.0.
(Chorus & Bartram, 1999; Roegner et al., 2014). The planktic community in fresh samples was
Common representatives of such water blooms are checked using the laboratory microscope and then
different species of coccal—Microcystis, Woroni- studied in greater detail in formalin preserved (1.5%)
chinia—and filamentous cyanobacteria—Plank- material under a microscope Olympus BX51 and
tothrix, Trichodesmium, Dolichospermum (formerly documented by microphotographs using a digital
planktonic Anabena), Anabaenopsis, Aphanizomenon camera (Olympus DP 70).
or Cylindrospermopsis. All of the species of these are Data on Lake Titicaca that we are introducing to
indicators of eutrophy or hypertrophy of the lakes, compare the situation with the lakes were extracted
reservoirs, fishponds or pools and sometimes also of from papers referring to results of short expeditions or
large rivers. Some of the species are cosmopolitan longer lasting monitoring (2–3 year series of data,
(Microcystis aeruginosa (Kützing) Kützing, Dolichos- analyses of silicate, oxygen, and primary production)
permum circinale (Rabenh. ex Born.et Flah.) Wacklin realized by different groups of scientists from abroad
et al., Planktothrix agardhii (Gomont) Anagn. et cooperating with Peruan and Bolivian authorities
Komárek), some are typical for temperate regions (D. (Richerson et al., 1977; Richerson et al., 1986; Dejoux
flos-aquae (Bréb. ex Born. et Flah.) Wacklin et al., & Iltis, 1991; Dejoux, 1992) and from web sites of
Woronichinia naegeliana (Unger) Elenkin), brackish corporations interested in monitoring eutrophication
waters (Nodularia, Trichodesmium) or tropical and of the Lake using satellite photography. Important data
subtropical zones (Cylindrospermopsis raciborskii on nutrient chemistry are already old and moreover
(Woloszynska) Seenayya et Subba Raju, Raphidiopsis roughly estimated, however, as we know, more
mediterranea Skuja). comprehensive ones are not available. Even if there
An exception among the species forming heavy exists a detailed monitoring of fish production and
water blooms is Limnoraphis robusta, because heavy composition of the fish stock, only actual data
water blooms of this cyanobacterium were up until applicable to fish research such as concentrations of
now found in waters more or less oligotrophic. In this the oxygen and water and air temperature (data
article, we describe the present situation in the Bay of provided by IMARPE, Instituto del Mar del Perú,
Puno, Lake Titicaca, Perú, at the end of summer period Station Puno) are available and have not changed
2013/2014, as it concerns the contemporary cyanobac- substantially.
terial water bloom and phytoplankton composition. To Data on physical, chemical and biological fac-
enable a possible prognosis of appearance of Limno- tors at Lake Atitlán were measured in spring 2012
raphis in the clear parts of the Titicaca Lake, we and for 3 years prior (Rejmánková et al., 2011).
compare environmental conditions and available data Regular monitoring started there in 1976 (Dix et al.,
with the situation at the Lake Atitlán, Guatemala, 2003) and has continued until the present. Several
where a heavy water bloom of L. robusta appeared expeditions have been organized to gain detailed
several times during recent years. information about primary production, nitrogen
fixation and nutrients limiting growth of Limno-
raphis. Results of such studies may be viewed at
Materials and methods http://www.atitlanscience.blogspot.com/. For com-
parison of species compositions of the Atitlán phy-
The data and plankton samples were collected on toplankton in 1983, we used data bestowed to us by
March 29th 2014 from the Puno Bay of Lake Titicaca Gertrud Cronberg, a scientist from Institute of
using the plankton net of 20 lm Mesh, and by direct Limnology, Lund, Sweden.

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Results The Puno Bay, where we collected our samples,

suffers intensive eutrophication due to the release of
Lake Titicaca treated and untreated waste waters from the city of Puno
(150,000 inhabitants). The hydrological system of the
Lake Titicaca (Appendix 1—supplementary material) Bay differs substantially from that of the Lago Mayor as
is situated at the Altiplano—Andean Plateau the Bay is only 15–25 m deep and due to everyday winds
(200,000 km2) at 3 809 m a.s.l. The lake extends for is polymictic (Richerson, 1991). Because of lowering of
15% of a drainage region of 50,000 km2. Two the water level and increasing runoff from new fields
countries share the Lake: Perú (55%) and Bolivia round the Lake, since 2003, Puno Bay lost a vast region of
(45%). Average and maximum depth are 105 and free water which changed into marsh, overgrown with
283 m, respectively. The retention time was calculat- Schoenoplectus and partly used for agriculture (Fockel-
ed as 70 years (Richerson et al., 1977). The lake is mann & Heege, 2011, EOWORLD).
endorheic and monomictic. While average surface The photograph on Appendix 2—supplementary
temperature in Lago Mayor reaches 14°C in summer, material shows the phytoplankton composition of the
temperature drops to 11°C during the period of morning sampling. At that time, the surface of the
homothermia. A thermocline at 40–50 m in Lago water near the shore was covered with a dense layer of
Mayor develops between October and June. In the M. aeruginosa combined with floating carpet of
1980s, oxygen reached the bottom of the Lago Mayor Lemna sp. Water was blue-green in colour and the
all year. In some years, the mixing of the column does flocs of Microcystis were readily distinguishable. The
not proceed and in some periods atelomixis can appear water was different in composition during our midday
(Richerson et al., 1977). A typical feature of deep return. Water was green, containing a large mass of
tropical lakes is the small temperature difference green algae (Appendix 3—supplementary material).
between epilimnion and hypolimnion which can be The water bloom was spread over the whole water
only 2–4°C. This enables inner mixing of the water column due to afternoon winds and had apparently
column and lifting the nutrients to the photosynthetic disappeared from the surface.
active layer (Lewis, 2000). The rainy season starts in
December and lasts until March with a maximum in Planktic cyanobacteria in Puno Bay
January. According to Hutchinson (1957), the Titicaca
Lake corresponds to a deep monomictic tropical lake The population of M. aeruginosa (Appendices 4 and 5—
(Richerson et al., 1977). Because of endorheic char- supplementary material) consisted of macroscopically
acter, the lake changes its water level a little according visible, floating, typical mucilaginous colonies. The
to the rainfall regime and its waters are semi-salty Microcystis population of Titicaca corresponded mor-
(0.1%, Richerson et al., 1977). The whole lake consists phologically to other populations of this species from
of three main basins: Lago Mayor or Grande, Chu- western coasts of the American continent. It probably
cuito, Great Lake (7000 km2), Lago Menor, Huiñay- belongs to the cosmopolitan M. aeruginosa genome
marca, Small Lake (1400 km2) and Bahı́a de described by van Gremberghe et al., (2011). M.
Puno, Puno Bay (564 km2). Lago Menor and the aeruginosa belongs to the most dangerous cyanobacteria
Puno Bay are separated by narrow straits and forming water blooms in respect to its production of toxic
exchanges of water masses between these basins and compounds (hepatotoxic microcystins) and to its high
Lago Mayor are not intensive (Rieckermann et al., production of macroscopic biomass corresponding to
2006). The map shows also shallow areas which are drastically increased concentrations in nutrients, espe-
temporally polymictic (Richerson, 1986). The whole cially in the presence of ammonia (Chorus & Bartram,
lake has 87 islands some of them are densely inhabited 1999). Microcystis bloom is always connected with
with 43 of them spread over the Lago Mayor. heavy eutrophication. Its morphology, structure of
Moreover, there exist the so-called ‘‘floating islands colonies, its vitality and ability to survive unfavourable
of the Uros’’ made from stems of Schoenoplectus conditions classify this species to the most spread water
(Wikipedia), where a part of the population also lives. blooms all over the world.

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The second species of planktic cyanobacteria and possess rather large gas vesicles in cells. The
containing aerotopes and heterocytes has been de- aerotopes are distributed in segments of filaments or
scribed as Nodularia inca (Montoya et al., 2015) along the whole filament evocating almost black
(Appendix 6—supplementary material). This new colour to portions or of the whole filament. Filaments
species of Nodularia from Titicaca Lake has a are embedded within 2–5 lm wide, transparent
characteristic morphology (irregularly coiled, solitary sheaths which sometimes are not developed. Tri-
trichomes with aerotopes in cells) and does not chomes contain a high amount of various carotenoids
correspond to previously known planktic species. causing a yellow–brown coloration of the massive
Coiled trichomes are known in Nodularia only in water bloom. The specific capability of Limnoraphis is
marine Baltic halophilic populations. The most known fixation of molecular nitrogen due to the presence of
cases are the water blooms from the Baltic Sea, SW diazocytes. This cyanobacterium has not been known
Australia and from the Caspian Sea (Komárek, 2013). as a water bloom forming species up to the beginning
The Baltic Sea filaments of Nodularia spumigena of the 21st century and occurred only sporadically in
Mertens ex Born. et Flah. were proven to intensively tropical unpolluted reservoirs (Komárek & Komár-
fix nitrogen (Hübel & Hübel, 1980). Species of ková-Legnerová, 2007; Komárek et al., 2013). In
Nodularia were also described from both American March 2014, L. robusta was found in the net plankton
continents (Nordin & Stein, 1980; Alvarez & Bazán, of Puno Bay as individual trichomes among other
1994; Pérez et al., 1999). The toxin nodularin has been planktic species rather frequently. We recorded it both
detected in the water bloom forming species of the in samples of phytoplankton taken in the morning
genus Nodularia. The slightly saline character of (filaments were smooth, without epiphyton, Appendix
Titicaca water could meet the special needs of this 2—supplementary material) and in the afternoon,
cyanobacterium. The population from Lake Titicaca is when the bottom sediments were lifted up (sheaths
evidently adapted to the planktic mode of life. As were overgrown with diatoms and filaments of
follows from literature (Richerson et al., 1977, 1986), Heteroleibleinia, Appendix 3—supplementary mate-
straight filaments of another species of Nodularia have rial). Many filaments in samples of periphyton taken at
been found in Titicaca already in 1937 (Tutin 1940) the edges of floating islands ‘‘Uros’’ were clearly blue-
and determined as N. harveyana (Thwaites) Thuret. green in colour and almost without gas vesicles
That time the abundance of this species in water was (Appendix 8—supplementary material). Also fila-
signed as ‘‘frequent’’. Also Richerson et al., (1977, ments cultivated in Petri dishes did not show gas
1986) found it during the large monitoring from 1973 vesicles (Appendix 9—supplementary material).
to 1982–1983 (Appendix 10—supplementary materi-
al). We detected such an organism in plankton inside Other species
flakes of mud lifted from the bottom during the
afternoon sampling (Appendix 7—supplementary Apart of the populations of Cyanobacteria, dominant
material). This species has no aerotopes and lives at species in the Puno Bay were the dinoflagellate
the bottom of slightly saline pools and lakes Ceratium hirundinella (O.F. Müller) Dujardin and
(Komárek, 2013), therefore, it is probable that a large, mainly the green algae Pediastrum boryanum (Turpin)
spiral and planktic N. inca was misinterpreted. Meneghini, P. duplex Meyen and Elakatothrix gelati-
Even if we registered very low abundance of nosa Wille. In small numbers, we found diatoms,
planktic spiral N. inca in Puno Bay, this cyanobacterial Fragilaria crotonensis Kitton, the dinoflagellate Peri-
species can also cause dangerous eventually toxic dinium willei Huitfeldt-Kaas and green algae, Pan-
water blooms. dorina morum (O.F. Müller) Bory, Oocystis lacustris
The third cyanobacterium found was L. robusta Chodat, O. parva W. et G. S. West, Sphaerocystis sp.,
(syn. Lyngbya hieronymusii var. robusta, see Komárek Coelastrum microporum Nägeli, and narrow filaments
& Komárková-Legnerová, 2007) (Appendices 2, 3 and of planktic Mougeotia which co-dominated in lake
8, 9—supplementary material). In comparison with Atitlán in 2012 (Table—Appendix 10—supplemen-
above-mentioned species, this is a large oscillatori- tary material). Most of these species are characteristic
alean species with thallus up to 22 lm wide and for waters of mesotrophic quality. Their concentra-
several centimetres long. Filaments are not branched tions were not high in comparison with the heavy mass

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development of the Microcystis bloom. This type of Hendzel et al., 1994). After such concentration is
species composition corresponds well with previous available, the population of Limnoraphis starts to
analyses of phytoplankton composition (Richerson activate its diazocyte zones producing the missing
et al., 1977; Iltis, 1991a, b, Appendix 10—supple- nitrogen. That way other phytoplankton autotrophs were
mentary material). The assemblage of non-blooming limited by nitrogen except for species fixing the N, thus
algae does not differ substantially between deep promoting a specific niche for Limnoraphis. Here
tropical lakes (Carney et al., 1987; Talling & Le- relatively voluminous filaments overcame more effec-
moalle, 1998) and dominance of individual taxono- tive, small organisms that are able to fix N2 such as
mical groups is frequently ruled by seasonal changes Aphanizomenon or Dolichospermum. An explanation
(Richerson et al., 1977). According to analyses of can be that Limnoraphis is able to utilize lower actual
biomass and chlorophyll content of phytoplankton by concentrations of available nutrients. Processes of N2-
Iltis (Iltis, 1991a, b) from 1985 and 1987, Lago Mayor fixation via heterocytes must be more energy consuming
was classified as oligotrophic and Lago Menor as than simple acceptance of N2 by any ready vegetative
mesotrophic, however, he mentioned appearance of cell. Another advantage is more effective buoyancy, as
cyanobacteria in comparison with results of Tutin Limnoraphis contains more and larger gas vesicles per
(1940) from 1937. Iltis also registered large ecological cell than other heterocytous species. The recent situation
diversity of sampling stations due to the vast size and in Atitlán confirms this hypothesis, as in more polluted
variety in bottom profile of the lake and in position of and shallow bays, the Limnoraphis is already mixed
the stations with regard to the source of with Aphanizomenon (Chandra et al., 2014).
eutrophication. Also other N2-fixing organisms can be present.
Woodhouse et al., (2013) analysed populations of
Limnoraphis bloom from Atitlán in 2009. They studied
Discussion the genes encoding the bacterial nitrogenases combined
with 16S rRNA. They found the support for non-
Lake Atitlán in Guatemala suffered recently with a heterocytous fixation of N due to the presence of nif H
bloom of L. robusta (Rejmánková et al., 2011; Komárek genes in the samples. The largest portion of the nitrogen
et al., 2013), which was also found in our samples. The fixation activity belonged to Limnoraphis, however,
bloom appeared as a heavy yellow–brown layer at the another fixers were also present (Desulfovibrio, Clos-
surface of the Lake, especially during the end of the tridium, and Methylomonas). For the formation of the
stratification in 2008 and 2009, and again after the water bloom, they were negligible, but they could
hurricane in 2011. In spite of the bloom being not fully enhance the concentration of N-compounds in water.
developed, trichomes of Limnoraphis are continually As the Lake is very attractive and preferred for
present in the phytoplankton. The bloom in Atitlán recreation, appearance of the water bloom could
developed as a result of the long-term lasting input of become a disaster for the local population. Moreover,
sewage into this large, deep oligotrophic lake. Accord- 40% of people depend on the Lake, using its water for
ing to comparison of recent data with those from consumption. At the Atitlán region, the effort of the
previous years, the concentration of soluble phosphorus researchers and of Guatemalan authorities to prevent
(SRP) has increased three-fold during the period of water bloom and to manage inflow of waste waters
observation (Dix et al., 2003). The bloom developed in increased recently (www.unidosporlagoatitlan.org), but
spite of rather low concentration of nutrients in water, final resolution of the problems is still far from solved.
which corresponded to the almost oligotrophic state of Water blooms of Limnoraphis have been described
the Lake (total N 153–453 lg l-1, diluted inorganic N also from Clear Lake and Lake Sacramento—San
7.8–20 lg l-1, total P 32–96 lg l-1 and soluble reac- Joaquin Delta of South California (Mioni et al.,
tive P 6–20 lg l-1 (Castellano & Dix, 2009). Re- 2011–2012), and appearance of probable Limnoraphis
jmánková et al. (2011), proved the ability of was described from China (Suda et al., 1998).
Limnoraphis in Atitlán to fix the nitrogen from air Another appearance of Limnoraphis in Guatemala
during night (in average 2.2 nmol C2H4 g Ch a-1 h-1). has probably been registered already in Lake Amati-
A necessary concentration of phosphorus for the start of tlán in 1983 by Swedish scientist Gertrud Cronberg
N2 fixation was found to be 7 lg of P–PO4 (Smith, 1990; (personal communication). She determined the

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Limnoraphis under the name Lyngbya birgei G. N-compounds in the running in rivers may be a serious
M. Smith, which is the most related species to contributor (Richerson et al., 1977).
Limnoraphis (Komárek, 2013). That organism was In Titicaca, Carney (1984) and Wurtsbaugh et al.
very probably L. robusta as L. birgei should occur in (1985) studied the nutrient limitation of phytoplankton
temperate zones in cold lakes. Other species that together with N2 fixation both in the Lago Mayor and
Cronberg had found were characteristic of relative in some bays of this main basin in 1981–1982. NH4?
assemblages we registered recently in Atitlán in 2012, significantly stimulated carbon fixation and chloro-
and also with those of Lake Amatitlán 20 and 30 years phyll production in shallow portions of the Lago
ago (Table in Appendix 11—supplementary material). Mayor and at three deep stations. Nitrogen fixation by
Eutrophication of lake Amatitlán can serve as a heterocytous blue-greens was stimulated by PO43-and
warning case. The lake is of the same geographical Fe2-, while NH4? inhibited it. Species composition of
character as Atitlán: deep, volcanic, and monomictic. the studied material should correspond to analysis
In 1983, it used to be a clear lake exploited as a centre done by Richerson et al., (1986), which means that the
for recreation. Nowadays, the lake is at its final N-fixing organisms belonged to (Anabaena) D.
hypertrophic state. Both basins of this lake suffer spiroides (Klebahn) Wacklin et al., Anabaena affinis
dense water blooms of M. aeruginosa and M. panni- and Nodularia sp. (Table 1). The results are basically
formis Kom. et al., both producing dangerous micro- the same as Rejmánková et al., (2011) obtained in the
cystins. The sole cause was the inflow of wastewaters experiments carried out in 2009 at the Lake Atitlán
from nearby Guatemala City. It seems that the with Limnoraphis. According to the available lit-
Limnoraphis bloom appeared before the bloom of erature (Richerson et al., 1977; Wurtsbaugh et al.,
Microcystis, or possibly before some other heterocy- 1985; Dejoux & Iltis, 1991), concentrations of avail-
tous species belonging to Aphanizomenon or Doli- able P and N in the main basin of Lago Mayor were
chospermum, during the process of eutrophication. comparable with those of Atitlán (Table 1) and the
Redfield ratio was always below the optimal value for
Redfield N:P ratio and lakes Titicaca and Atitlán phytoplankton biomass composition, while basic
concentrations of available nutrients were still low.
Redfield ratio N:P (16:1 in molar, 7:1 in mass) A question can be introduced as to whether a heavy
represents an average specific ratio for phytoplankton. water bloom of Limnoraphis can develop also in the
The ratio is not stable during the development of the Lago Mayor. Chemical data on water of Lago Mayor,
population. While a low ratio (relatively higher even if they are already old, are indicative of
concentration of SRP) is necessary during the expo- possibility that the state of the lake is still good and
nential growth, slow development of the population water is almost oligo-mesotrophic. Unfortunately we
demands higher concentrations of N (Klausmeier did not have opportunity to get samples of phyto-
et al., 2004). plankton from Lago Mayor, but we assume that at least
Both Lake Titicaca and lake Atitlán belong to the periphyton at the edges of ‘‘Uros’’ floating isles would
group of large tropical or subtropical lakes where very contain filaments of Limnoraphis. Tutin (1940) re-
low values of the N: P ratio were found (e.g. Talling, ported appearance of Lyngbya aestuarii in plankton of
1969; Lake Victoria; Lewis, 1974; Lake Llano) and Lago Mayor already in 1937. It is very probable that
thus the growth of phytoplankton is ruled by the this species was L. robusta, as the size of filaments is
concentration of available nitrogen. Its supply is very near to Limnoraphis. L. aestuarii, however, is a
frequently replenished by N2 fixation (for Titicaca marine or brackish cyanobacterium growing in the
Lake see Vincent et al., 1985). The concentration of littoral zone of sea coasts.
phosphorus is often sufficient but cannot be utilized. There are more lakes which can be endangered by
The reason for high P in tropical lakes and also in the development of Limnoraphis. According to the
Titicaca and Atitlán is volcanic subsoil. In the case of data published by IMARPE (Instituto del Mar del
N-compounds, apart from low supply of nitrogen in Perú, Villalobos et al. 2012) which is monitoring fish
the soil, strong denitrification in tropical regions is production all over lake Titicaca and also of the lakes
enabled by high water temperature even in deep layers in the vicinity in relation to basic chemistry, trans-
of the lakes (Lewis, 2000). Also low concentrations of parency and chlorophyll content, this can concern

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Table 1 Data on concentrations of available nutrients (DIN SRP by mass) in the lakes Titicaca and Atitlán. Concentrations
dilute inorganic nitrogen, SRP soluble reactive phosphorus), of chlorophyll demonstrate still oligo- to mesotrophic state of
chlorophyll a concentrations and values of Redfield ratio (DIN: the lakes
Sampling time DIN lg l-1 SRP lg l-1 DIN:SRP Chlor a lg l-1
0–30 m 0–30 m 0–30 m 0–30 m

Titicaca, L. Mayor
Wurtsbaugh et al. (1985) 1981, range 3.5–2.5 3–24 About 5
Vincent et al. (1984) 1982, range 4.5–18 6.4 About 3 2.3–3.9
Richerson et al. (1986) 1981–1982 1.5
Carney et al. (1987) 1981–1982 0.6–5.9
Iltis 1988 1985 and 1987 Approximately 0.6–1
EOWORLD 2011 (Satellite) 2003 (March), range 1.0–4.0
EOWORLD 2011 (Satellite) 2004 (June) 2–8
EOWORLD 2011 (Satellite) 2005 (May) 1–1.5
Lake Atitlán, Center
Deevey 1957 1957 10.2 7.0 2 0.5
Weiss (1971) 1971 10 6.7 1.5
Castellano & Dix (2009) 2008 7.8–20 6–20
Rejmánková et al. (2011) 2008 (March) 20.1 18.8 1.1 1.8
2009 (March) 54.8 21.2 2.6 2.2
2009 (Nov., bloom) 21.6 11.4 1.9 19.4
Chandra et al. (2014) 2013 7–25 (90) 5–25 1.1–3.5 4.2

Laguna Arapa, which is situated to the north of the bloom), and for the change of ecological conditions
Lago Mayor. Values of transparency (13 m) and in water, but its regulation and control is easier than for
chlorophyll concentration (0.4–1.6 lg l-1) are in the toxic and more dangerous members of the genera
range of oligotrophy and very much like data we Dolichospermum, Aphanizomenon or Microcystis.
obtained in Lake Atitlán before the bloom appeared. Even if we presume that water quality in the central
Because of large numbers of waterfowl, the transport deep basin is still low in concentration of nutrients,
of cyanobacteria must be very easy. water bloom was apparent and photographed by Earth
Several variables can trigger expansive growth of Observations Laboratory at Johnson Space Center on
Limnoraphis such as low water temperature, nutrient May 5, 2004 (ISS009-E-5696). The water bloom was
limitation (concentration of soluble phosphorus lower not permanent and it was evident that the main regions
than 7 lg l-1), and also high concentrations of of the bloom corresponded to highest density of
nutrients corresponding to eutrophy, where because settlement (Lago Menor, shores of the Lago Mayor
of high concentrations of N-sources, the leading near Ancoraimes, Achacachi, and also near Pusi at the
element becomes phosphorus. It seems that low water northern shore of the Lago Mayor). However, the
temperature is a serious cause, because cultivated species composition of the bloom has not been
clones of Limnoraphis we used for experiments did not analysed.
grow very well in low temperatures (18–19°C), while Water bloom of Microcystis and carpets of Lemna
growth in warmer conditions (23°C) was more inten- are continually detected in Puno Bay (www.
sive (unpublished results). On the other side, filaments visibleearth.nasa.gov/view.php?id=4843).
of Limnoraphis survive in Puno Bay and look sound It is very important to acquire information about
and ready to grow. which species is responsible for water bloom in the
The mass production of Limnoraphis is a negative main basin. Growth of each species is supported by a
phenomenon particularly for touristic activities (re- group of different factors and has another influence on
pugnant appearance of the yellow–brown water the environment and water utilization. In the

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population of L. robusta in Atitlán, for example, no bloom of this has been studied in the Lake Atitlán,
known tox-genes were found (Rejmánková et al., Guatemala. According to the comparative situation in
2011). However, in the world-wide population of M. other lakes, water bloom of Limnoraphis could appear
aeruginosa, the situation is different. in the main oligo-mesotrophic basin of the Great Lake
It seems that even if the N:P ratio remains low, only (Lago Mayor) or in some other places, which are still
in that case where the concentrations of the limiting almost clear. Intensive scientific research on the Lake
element remain in low values, the niche for the that could reveal, control and prevent appearance of
development of intensive water bloom of Limnoraphis such disaster is strongly recommended.
exists. When the concentrations of NO3- and espe-
cially HN4? increase, green algae and (responding to Acknowledgments This study was realized under the support
of the bilateral international collaboration between the Czech
Si concentration) diatoms would start to grow. Under
Academy of Sciences and CONCYTEC (Peru) 2013–2014. We
higher concentrations of P, Limnoraphis would be thank Dr. Gertrud Cronberg, Institute of Limnology, Lund,
replaced with heterocytous blue–greens. This is Sweden, for offering us her unpublished data about the
recently case of the Lake Atitlán, where cell numbers composition of phytoplankton of the Atitlán and Amatitlán
lakes from the year 1983. We are indebted to our referees both
of Limnoraphis in polluted bays are almost equal to
for comments on the text and helpful cultivation of our English.
those of toxic Aphanizomenon in 2013 (Chandra et al.,
2014).
The extremely extensive and deep basin of Lake
Titicaca has much higher retention capacity than
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