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INTRODUCTION
Cladocera are one of the most important components
of zooplankton in lacustrine ecosystems. This group is also
well-known to promptly respond to environmental changes
(Jeppesen et al., 2001). Previous studies have highlighted
that temperature and altitude are among the main factors
determining Cladocera communities (Campanelli, Mortari
and Henry, 2016; Green, 1995; Padhye et al., 2016; Sweet-
man, 2010; Zawiska et al., 2015). In addition, these studies
have shown comparable sensitivities to changes in lake
water trophic state, water depth, conductivity and pH (Ko-
rhola and Rautio, 2001). These responses to environmental
variables makes Cladocera one of the most powerful pale-
olimnological indicators and for this reason they have been
widely used for the reconstruction of past lacustrine envi-
ronments (Bjerring, 2007; Kienast et al., 2011; Korosi,
2012; Luoto et al., 2009; Mirosław-Grabowska and Zaw-
isza, 2014; Nováková et al., 2013 Sarmaja-Korjonen and
Hyvärinen, 2008; Schmidt, 2000; Szeroczyńska, 1991; Sze-
roczyńska et al., 2007; Szeoczyńska and Zawisza, 2011
a,b). Subfossil remains of Cladocera are commonly used in
paleolimnological studies in Eurasia and America (Bjer-
ring, 2007; Mirosław-Grabowska and Zawisza, 2014; Pa-
terson, 1994; Szeroczyńska et al., 2007). However, only a
few paleolimnological studies based on water fleas were
conducted in Central America (Cuna et al., 2014; Sze-
roczyńska et al., 2015; Zawisza et al., 2012, 2014, 2016).
So far, the majority of studies focused on the living Clado-
cera and their taxonomy (Elías-Gutiérrez et al., 1999, 2006,
2008; Sinev, 2015; Sinev and Silva-Briano, 2012; Sinev
and Zawisza, 2013).
The knowledge of Cladocera species composition, dis-
tribution and ecology in freshwater lakes of Central Amer-
ica is crucial for the development of reliable bioindicators,
and for paleolimnological investigations. The main objec-
tive of the present study was to analyze and identify sub-
fossil Cladocera species in northern Central America, in
particular in Guatemala, El Salvador and Honduras, and
to explore their relationship to lake environmental char-
acteristics such as altitude, lake area, depth, pH, trans-
parency, conductivity and dissolved oxygen. The obtained
results will provide the basis for the reconstruction of re-
gional and global climatic and envoronemntal changes at
long-term scale.
Advances in Oceanography and Limnology, 2016; 7(2): 151-162 ARTICLE
DOI: 10.4081/aiol.2016.6266
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License (CC BY-NC 4.0).
Ecology of Cladocera species from Central America based on subfossil assemblages
Marta Wojewódka,1* Edyta Zawisza,1 Sergio Cohuo,2 Laura Macario-González,2 Antje Schwalb,2 Izabela Zawiska,3
Liseth Pérez4
1Institute of Geological Sciences, Research Centre in Warsaw, Polish Academy of Sciences, Twarda 51/55, 00818 Warsaw, Poland;
2Institut für Geosysteme und Bioindikation, Technische Universität Braunschweig, Langer Kamp 19c, 38106 Braunschweig, Germany;
3Institute of Geography and Spatial Organization, Polish Academy of Sciences, Twarda 51/55, 00818 Warsaw, Poland; 4Instituto de
Geología, Universidad Nacional Autónoma de México (UNAM), Ciudad Universitaria, 04510, Ciudad de México, México
*Corresponding author: m.wojed@twarda.pan.pl
ABSTRACT
Cladocera species composition was analyzed in surface sediments of 29 lakes in Central America (Guatemala, El Salvador and Hon-
duras). The material studied was collected with an Ekman grab in autumn 2013 from lakes located in lowland, highland and mountain re-
gions. The study revealed high variability in qualitative and quantitative composition of subfossil Cladocera. A total of 31 Cladocera species
(5 planktonic and 26 littoral) were identified, as well as 4 morphotypes that could not be identified (NRR 1-4). Planktonic Bosminidae and
Daphniidae were the most abundant families. Daphniidae were restricted to water bodies in mountain regions, whereas Bosminidae were
widely distributed in lakes with different abiotic conditions. Moreover, Bosminidae species also occurred in highly mineralized waters (>
900 µS cm–1). The great majority of the identified Cladocera species belonged to the littoral family Chydoridae. Chydorus cf. sphaericus
was the most common species (found in 20 lakes), which probably reflects its tolerance to a wide spectrum of habitat conditions. Cluster
analysis discriminated 6 groups of Cladocera species with a high correlation level within groups (≥0.8), which showed different types of
correlation with lake characteristics and environmental variables. Canonical correspondence analysis (CCA) showed that altitude and sec-
ondly water electrical conductivity were the most important drivers of Cladocera species composition in the region studied. Furthermore,
CCA analysis indicated lowland lakes with low water transparency were also characterized by peculiar species assemblages.
Key words: Subfossil Cladocera; Central America; waterfleas ecology; Guatemala; El Salvador; Honduras.
Received: September 2016. Accepted: November 2016.
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METHODS
Study sites
The study included 29 waterbodies located between 13°
and 17° N geographical latitude and from 87° to 91° W lon-
gitude in Guatemala, El Salvador and Honduras (Fig. 1).
The study area is located in the Central American Bioregion
of the American Neotropical Ecozone, which is character-
ized by two distinct seasons: a dry winter and a moist sum-
mer season (Taylor and Alfaro, 2005). The subtropical ridge
(belt of high atmospheric pressure) from the northern At-
lantic is controlling the climate of the region, whereas the
Intertropical Convergence Zone (ITCZ) and polar fronts of
mid-latitude origin have a secondary impact (Taylor and
Alfaro, 2005). One of the main factors affecting the micro-
climate of the area is topography (Karmalkar et al., 2011;
Taylor and Alfaro, 2005). The considerable differences in
mean annual temperature and precipitation which charac-
terize the entire region mainly depend on altitude. The
Guatemalan lowlands are characterized by a mean annual
temperature of 25-28°C, whereas temperatures in highland
and mountain regions are around 12-15°C (Atlas Climato-
logico for 1928-2003, the National Institute for Seismology,
Volcanology, Meteorology and Hydrology of Guatemala;
www.insivumeh.gob.gt). Annual precipitation in the area
varies considerably during the year and ranges from <1000
mm in the plains to >2500 mm in the mountains (Taylor
and Alfaro, 2005).
The lakes studied are located at altitudes ranging from
sea level (El Muchacho at 3 m asl) to high altitude lakes
(Magdalena and Chicabal at 2863 and 2726 m asl, respec-
tively, Tab. 1). Lake area and depth also were quite vari-
able. The largest lake were Atitlán and Yojoa (125 and
~79 km2, respectively, Tab. 1), while several lakes have
an area <0.10 km2, such as Madre Vieja (0.10 km2), Verde
Fig. 1. Map of the study area showing the location of lakes sampled in Central America, i.e. Guatemala, Honduras and El Salvador.
Numbers indicate the names of the lakes: 1, Atitlán; 2, Calderas; 3, Chicabal; 4, Comandador; 5, El Muchacho; 6, El Pino; 7, El Rosario;
8, Grande; 9, Ipala; 10, Lachuá; 11, Las Pozas; 12, Magdalena; 13, Sacnab; 14, Salpetén; 15, Quexil; 16, Chiligatoro; 17, Jucutuma; 18,
Madre Vieja; 19, Ticamaya; 20, Yojoa; 21, Apastepeque; 22, Aramuaca; 23, Chanmico; 24, El Espino; 25, Jocotal; 26, Los Negritos;
27, Metapan; 28, Olomega; 29, Verde.
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Subfossil Cladocera of Central America 153
(0.10 km2), Chiligatoro (0.04 km2), El Rosario (0.02 km2),
Magdalena (0.01 km2) (Tab. 1). The study covered both
very shallow (≤3 m depth, such as Comandador, El
Muchacho, El Rosario, Grande, Magdalena, Jucutuma,
Ticamaya, Jocotal, Los Negritos, Olomega), and very
deep lakes (>300 m), such as Lachuá (a 378 m deep
karstic lake), Atitlán (a 340 m deep crater lake) and Chi-
cabal (330 m, Tab. 1).
Sampling and analyses
Sediments were collected in autumn 2013 using an
Ekman sediment sampler. The geographical location of the
lakes was determined by a handheld navigator (GPSmap
60c). Water transparency was determined using a Secchi
disk, and the maximum lake depth was identified using a
portable depth sounder (Echosounder Eagle Mach 1).
Physical and chemical parameters of the surface waters
(i.e., pH, conductivity, dissolved oxygen) were measured
with a WTW multi set 350i multiparametric probe. The
area of each lake (Tab. 1) was calculated by the measure
tool of Google Earth. Lake sediment samples were col-
lected both from the littoral as well as from the open-water
(pelagic) zone. In eight shallow lakes, where there was no
pelagic zone (i.e., Comandador, El Muchacho, El Rosario,
Grande, Jucutuma, Ticamaya, Jocotal, Los Negritos), sam-
ples were collected only from the littoral zone (Tab. 1).
Lakes El Pino, Ipala, Quexil, Madre Vieja, Chanmico, El
Espino, Metapan and Verde, were sampled only in the pro-
fundal zone due to the shape of the lake basin. Crater lake
Aramuaca (107 m depth) was sampled only in the littoral
zone (Tab. 1).
Tab. 1. Location, morphometry and selected limnological variables measured at water surface at the waterbodies sampled in Central
America.
ID Name Country Geographic Altitude Area Samples Zmax Secchi pH Conductivity O2 HCl
coordinates
N W (m asl) (km2) L P (m) (m) - (µS cm–1) (mgL–1)
1 Atitlán Guatemala 14.6837 91.2239 1556 125.00 + + 340 4.2 8.9 442 5.7 +
2 Calderas 14.4117 90.5913 1790 0.35 + + 26 2.9 9.2 100 4.9 -
3 Chicabal 14.7875 91.6561 2726 0.21 + + 330 1.6 9.0 12 5.4 -
4 Comandador 13.9600 90.2544 20 0.65 + 1.7 0.5 7.4 251 5.6 -
5 El Muchacho 13.8892 90.1918 3 0.36 + 2 0.4 9.1 439 5.9 -
6 El Pino 14.3447 90.3941 1038 0.64 + 18 2.8 8.3 100 2.0 -
7 El Rosario 16.5255 90.1601 126 0.02 + 3 0.2 7.2 987 1.7 +
8 Grande 13.8903 90.1703 5 0.95 + 2 0.2 7.4 110 3.7 -
9 Ipala 14.5571 89.6394 1495 0.56 + 25 3.6 8.0 100 2.8 -
10 Lachuá 15.9184 90.6732 170 4.00 + 378 4.4 7.9 906 4.8 +
11 Las Pozas 16.3432 90.1660 152 2.16 + + 35 3.1 8.3 277 5.4 +
12 Magdalena 15.5426 91.3956 2863 0.01 + + 3 2.8 8.8 331 6.2 +
13 Sacnab 17.0583 89.3725 170 4.28 + + 9 1.8 9.0 412 6.1 +
14 Salpetén 16.9815 89.6755 105 2.77 + + 32 1.7 7.0 4520 5.8 +
15 Quexil 16.9231 89.8099 120 2.20 + 32 2.7 8.5 204 4.5 -
16 Chiligatoro Honduras 14.3756 88.1830 1925 0.04 + + 5.5 0.9 7.4 100 1.9 -
17 Jucutuma 15.5123 87.9028 27 4.34 + 2 2.0 7.3 100 1.0 -
18 Madre Vieja 14.3569 88.1376 1866 0.10 + 3.4 0.9 8.5 100 2.7 -
19 Ticamaya 15.5506 87.8897 17 2.91 + 2 0.8 7.2 100 1.6 -
20 Yojoa 14.8606 87.9847 639 79.70 + + 22 3.3 8.3 100 2.7 -
21 Apastepeque Salvador 13.6925 88.7448 509 0.38 + + 47 6.1 8.6 100 2.8 -
22 Aramuaca 13.4294 88.1065 76 0.40 + 107 6.7 8.4 100 4.1 -
23 Chanmico 13.7786 89.3541 477 0.78 + 51 0.9 9.2 100 3.4 +
24 El Espino 13.9530 89.8652 689 0.99 + 5.5 0.4 8.5 85 6.6 -
25 Jocotal 13.3371 88.2519 26 8.70 + 3 1.5 8.0 595 3.0 -
26 Los Negritos 13.2831 87.9370 102 0.69 + 2 0.3 9.2 40 5.2 -
27 Metapan 14.3094 89.4655 450 16.00 + 6 0.2 8.4 255 3.1 -
28 Olomega 13.3072 88.0551 66 25.20 + + 2.5 0.9 7.7 105 2.5 -
29 Verde 13.8915 89.7872 1609 0.10 + 12 2.7 7.5 83 4.5 -
L, littoral zone; P, pelagic zone; Zmax, maximum lake depth; HCl, reaction with acid during preparation. The World Geodetic System of 1984 (WGS84)
datum was used for the Cladocera samples.
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154 M. Wojewódka et al.
Sediment samples were placed in plastic bottles
(100 mL) immediately after collection, and stored under
refrigeration. Samples were then transported to the Pale-
olimnology Laboratory of Universidad National Au-
tonomous de Mexico (UNAM), where subsamples for
subfossil Cladocera analysis were obtained and preserved
in cooling condition.
Subfossil Cladocera were analyzed at the Bioindicator
Laboratory at the Warsaw Research Center of the Institute
of Geological Sciences, the Polish Academy of Sciences.
Each sample consisting of 1 cm3 of wet sediment was pre-
pared according to standard methods (Frey, 1986). Sedi-
ments were treated with 10% HCl to eliminate carbonate
and then heated in 10% KOH for 30 min. The residue was
centrifuged and sieved through a 38 µm sieve, transferred
into a test tube and filled up to 5 cm3 with distilled water.
Samples were stained with safranin. Three to four slides
obtained from of 0.1 cm3 liquid suspension each were ex-
amined at the microscope for each sample. The identifi-
cation of Cladocera taxa followed Elías-Gutiérrez et al.
(2006, 2008), Hudec (2000), Kotov (2009), Kotov et al.
(2003), Rajapaksa and Fernando (1987), Rey and Vasquez
(1986), Sinev (1998, 2001, 2015a, 2015b), Sinev and
Dumont (2016), Sinev and Zawisza (2013), Van Damme
et al. (2011). The Cladocera relative abundance diagram
was prepared using the C2 program (Juggins 2005, 2007).
In order to determine the relation between species dis-
tribution and lake characteristics (area, altitude, maximum
depth) and water variables (pH, Secchi transparency, dis-
solved oxygen), cluster analysis and canonical correspon-
dence analysis (CCA; ter Braak, 1986) were performed.
Cluster analysis is based on the similarity measure per-
formed on qualitative data (Hammer et al., 2011), while
CCA is a combination of mutual averaging algorithm with
a multiple regression (ter Braak, 1986) which performed
on combined quatitative Cladocera and environmental
data. Statistical analyses were conducted using the PAST
software (Hammer et al., 2001).
RESULTS
Environmental variables
In general, the surveyed lakes were characterized by
relatively low water transparency, with exception of lakes
Aramuaca and Apastepeque, which showed Secchi depth
>6 m (Tab. 1). Secchi depth values ranging between 2.7-
4.4 m were measured in 10 lakes, i.e. Lachuá, Atitlán,
Ipala, Yojoa , Las Pozas , Calderas, El Pino, Magdalena,
Quexil and Verde (Tab. 1). The waters of Lake Jucutuma
(2.0 m depth) were characterized by visibility reaching
the bottom, while four lakes were characterized by clarity
of 1.5-1.8 m (Sacnab, Salpetén, Chicabal, Jocotal). The
other lakes (Comandador, El Muchacho, El Rosario,
Grande, Chiligatoro, Madre Vieja, Ticamaya, Chanmico,
El Espino, Los Negritos, Metapan, Olomega) were char-
acterized by Secchi disk visibility <1.0 m (Tab. 1).
The lakes investigated did not show considerable dif-
ferences in pH values, which ranged from neutral (7.0 in
Lake Salpetén) to alkaline (9.2 in Lake Chanmico and
Lake Los Negritos, Tab. 1). Circumneutral water pH was
recorded for lakes El Rosario, Ticamaya, Jucutuma,
Comandador, Chiligatoro, Grande, Olomega, Verde and
Lachuá. Waters of five lakes were strongly alkaline (pH
≥9.0), i.e., Sacnab, El Muchacho, Calderas, Los Negritos,
and Chanmico. The other 14 lakes were characterized by
slightly alkaline waters, with pH values ranging from 8.0
to 9.0 (Tab. 1). Electric conductivity ranged from 12 µS
cm–1, measured at Lake Chicabal, to 4520 µS cm–1 in Lake
Salpetén (Tab. 1). High conductivity was recorded in the
waters of El Rosario and Lachuá (Tab. 1). Values between
~400 and 600 µS cm–1 were determined in lakes Jocotal,
Atitlan, El Muchacho, and Sacnab (Tab. 1). In the remain-
ing lakes this parameter was <350 µS cm–1 (Tab. 1). Ten
of the sampled lakes were characterized by the dissolved
oxygen content of over 5.0 mg L–¹, i.e., El Espino, Mag-
dalena, Sacnab, El Muchacho, Salpetén, Atitlán, Coman-
dador, Las Pozas, Chicabal and Los Negritos (Tab. 1). The
amount of dissolved oxygen in nineteen lakes ranged from
1.0 mg L–¹ (Jucutuma) to 4.9 mg L–¹ (Calderas). The low-
est dissolved oxygen concentration (<2.0 mg L–¹) were
recorded in lakes Chiligatoro, El Rosario, Ticamaya and
Jucutuma (Tab. 1).
Subfossil Cladocera
A total of 31 Cladocera taxa belonging to three fami-
lies – Daphniidae, Bosminidae and Chydoridae – were
found in the sediments of the lakes studied. Some Clado-
cera remains that could not be identified to species level
belong to four different morphotypes and were referred
to as “Not Recognized Remains” (NRR) 1, 2, 3 and 4, re-
spectively (Fig. 2). Species relative abundances are pre-
sented in Fig. 3. Frequency (n), mean and maximum
relative abundance of each Cladocera species are collated
in Tab. 2.
The species richness per lake ranged from one in Lake
Calderas to 12 species (lakes Atitlán and Verde), and in-
cluded both planktonic and littoral forms. Only in the sed-
iments of the deep Aramuaca crater lake no subfossil
cladocerans remains were found. Planktonic species were
represented by five taxa, i.e., Bosmina longirostris
(O.F.Müller, 1785), Bosmina (E.) longispina (Leydig,
1860), Bosmina (E.) coregoni (Baird, 1857), group of
Daphnia longispina (O.F. Müller, 1785), group of Daph-
nia pulex (Leydig, 1860), which occurred in 17 lakes
(Fig. 3). Cladocera communities from lakes El Rosario
and Calderas were entirely dominated by planktonic
species (Fig. 3), while the share of Bosminidae and/or
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Subfossil Cladocera of Central America 155
Daphniidae exceeded 90% in lakes Ipala, El Pino and
Apastepeque (Fig. 3). Pelagic species were dominant (60-
88% of total Cladocera abundance) in lakes Salpetén, Yojoa,
El Espino, Atitlán, Sacnab, Chicabal, Lachuá (Fig. 3).
The remaining lakes (16) were dominated by littoral
species of Chydoridae, which also represented the most
species-rich group. In fact, 26 littoral Cladocera species
and four NRR (Fig. 3 and Tab. 2) were identified in the
sediments studied, with the NRR most likely belonging
to also to littoral Chydoridae. Chydorus cf. sphaericus
(O.F. Müller, 1776) (20 lakes), Alona glabra (Sars, 1901)
(Ovalona glabra, following Sinev, 2015a) (13 lakes) and
Cladocera comparable to (13 lakes) and Alona quadran-
gularis type (O.F. Müller, 1776) (12 lakes) were the most
common taxa (Fig. 3 and Tab. 2). In five lakes (Las Pozas,
Quexil, Verde, Chiligatoro, Magdalena), both littoral and
planktonic species were present. The share of littoral
species ranged from 60% to 80% in lakes Las Pozas,
Quexil, Verde and Chiligatoro. In the sediments of lakes
Las Pozas and Quexil, eight and nine littoral species were
identified, respectively, and two planktonic species were
detected. In Las Pozas, Alona ossiani (Sinev, 1998), was
the most abundant littoral species (approx. 20%), whereas
in Quexil – Chydorus cf. sphaericus (ca. 15%) and Alona
quadrangularis type (ca. 15%, Fig. 3) were dominant.
Lake Verde and Lake Chiligatoro were characterized by
the presence of 12 and 6 species, respectively. Chydorus
cf. sphaericus (ca. 25%) and group of Anthalona verru-
cosa (Sars, 1901) (ca. 15%) were the dominant species of
the littoral zone in Lake Verde, while Alona ossiani (ca.
35%) and Simocephalus sp. (Schoedler, 1858) (ca. 20%)
were the most abundant species in Lake Chiligatoro (Fig. 3
and Tab. 2). In Lake Magdalena, the deep-water species
accounted for a minor portion of cladocerans, and Chy-
dorus cf. sphaericus was the dominant species (ca. 90%).
Planktonic taxa were completely absent in the sediments
Fig. 2. Unidentified subfossil remains (NRR) of Cladocera. A) Probably headshield of Euryalona sp. B) Headshield NRR1. C) Postab-
domen of Leydigiopsis ornata. D) Probably headshield of Leberis sp. E) NRR3, probably shell of Cladocera from group of Coronatella
monacantha. F) shell NRR4. Scale bars: 500 µm.
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156 M. Wojewódka et al.
of eleven lakes (Fig. 3). Lakes Comandador, Los Negritos,
Ticamaya and Jocotal were dominated by Chydorus cf.
sphaericus, which represented from 36% to 50% of the
Cladocera communities. This taxon was also common in
Madre Vieja (15%), Metapan (23%) and Olomega (16%).
In Lake Madre Vieja, Alona ossiani was the most abun-
dant species (ca. 42%), Camptocercus dadayi (Stingelin,
1913) was the dominant species in Metapan (ca. 31%),
and NRR1 (ca. 32%) (Figs. 2 and 3) were dominant in
Olomega. In Lake Jucutuma, Acroperus sp. (Baird, 1843)
(ca. 22%) and Camptocercus dadayi (ca. 22%) were dom-
inant, whereas Alona quadrangularis type (ca. 43%) and
Alona glabra (ca. 29%) dominated in Lake Grande. Lake
El Muchacho and Lake Chanmico were characterized by
low species diversity (3) and low frequency of individu-
als. Group of Leydigia acanthocercoides (Fischer, 1854)
was dominant in Lake El Muchacho (ca. 52%), whereas
Leberis sp. (Smirnov, 1989) was the most prominent
species in Lake Chanmico (50%, Fig. 3). The largest num-
ber of subfossil Cladocera remains was determined for
Lakes Sacnab (22,000 ind. cm–3) and Ipala (21,000 ind.
cm–3), where open-water species dominated. The maxi-
mum number of water fleas in the waterbodies dominated
by littoral forms was ca. 10,000-11,000 ind. cm–3, as
recorded in Madre Vieja, Quexil and Verde.
Statistical analysis
The “cophenetic coefficient” in the cluster analysis was
0.8009 and well reflected the similarities within the data.
The dendrogram shown in Fig. 4 (see also Tab. 3) defined
six Cladocera groups. The highest correlation coefficient
between species was determined for Alona rustica (Scott,
1895) (group of Flavalona rustica, following Sinev and
Dumont, 2016) and Simocephalus sp. (0.99, Group 6), and
for Daphnia pulex-group and Bosmina longirostris (0.94,
Group 1, Fig. 4a and Tab. 3). The species Bosmina (E.)
coregoni, Bosmina (E.) longispina, Alona quadrangularis
Fig. 3. Relative abundances (%) diagram for the subfossil Cladocera species identified in surface sediments from freshwater ecosystems
of Central America. Lakes are ordered by decreasing contribution of planktonic forms. NRR1, unidentified remains type 1; NRR2,
unidentified remains type 2, probably headshield of Leberis sp.; NRR3, unidentified remains type 3, probably of Coronatella of monacan-
tha-group); NRR4, unidentified remains type 4.
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Subfossil Cladocera of Central America 157
type, Alona glabra and Leberis sp. (Group 2) resulted to
be correlated at the similarity level of 0.92. In the three
other groups the correlation coefficient between species
ranges between 0.8 and 0.86 (Fig. 4a).
The CCA analysis was conducted using the species in-
cluded the six distinguished clusters and an additional set
of other Cladocera species that were not included in any
cluster. Due to their rarity and low contribution to total
Cladocera remains, NRR were not included in the analysis.
The CCA ordination biplot is presented in Fig. 4b. Arrows
show environmental variables, and their length and direc-
tion indicate the strength and direction of their influence on
the species composition (ter Braak, 1986).
Axis 1 and 2 explained almost 80% of the variability
(axis 1=49.98%, axis 2=29.29%). Altitude, transparency, pH
and the maximum depth were positively correlated with axis
1, while conductivity and lake area were negatively corre-
lated with the first canonical axis (Fig. 4b). The location of
Group 1 in quadrant I, and of Group 3, Group 6 and the
Daphnia longispina-group in quadrant IV underlines the
positive correlation of the abundances of these species
groups with altitude and negative correlation with conduc-
tivity. Moreover, the occurrence of Graptoleberis testudi-
naria (Fischer, 1848) and Group 1 also seem to be strongly
determined by the Secchi disk visibility (Fig. 4b). Species and
groups of Cladocera located in quadrants II and III were cor-
related negatively with altitude (Fig. 4b) and positively with
conductivity and lake area (Fig. 4b and Tab. 3). Group 2 and
Alonella excisa (Fischer, 1854) were placed in the 2nd quar-
ter. Species of Group 4 and 5 and Epheromorphus sp. (Frey,
1982), Leydigia louisi louisi (Jenkin, 1934), Leydigiopsis
ornata (Daday, 1905), Notalona sculpta (Sars, 1901) were
located in the 3rd quarter. According to Fig. 4b, these species
dominated in lowlands and in the waters with low visibility
(negative correlation with Secchi disk visibility and alti-
tude). Chydorus cf. sphaericus was located between quad-
rants III and IV, which may indicate a weak relation with all
of the considered environmental variables.
DISCUSSION
Thirty-one Cladocera species were identified in surface
sediments of the lakes studied. The number of species
found in individual lakes was generally small. In fact, the
maximum number of species found in lakes Atitlán and
Verde was only 12. Compared to European lakes, which
are normally inhabited by over 30 species (Dumont, 1994),
the species diversity of Cladocera was low in the consid-
ered region of Central America. These findings seems to
confirm that the number of Cladocera species found in one
waterbody in the Neotropics is in general low and usually
ranges from several to over a dozen species (Cuna et al.,
2014; Peréz et al., 2013; Zawisza et al., 2012). The differ-
ences in the number of cladoceran species between the con-
tinents may result from species competition (Feniova et al.,
2011; Shurin, 2000), fish or invertebrate predation (Korhola
and Rautio, 2001), as well as from different geological his-
tory of the area (Korhola and Rautio, 2001).
The identified Cladocera included both littoral and
pelagic species. Planktonic species of Daphniidae and
Bosminidae were the most abundant. Remains of the
Daphnia pulex-group and the Daphnia longispina-group
were mainly associated to lakes located at altitudes above
Tab. 2. Number of occurrences, maximum and mean percentage
contribution of cladoceran species identified in the sediments of
the surveyed waterbodies.
Group or species n Max Mean
(%) (%)
Bosmina longirostris 9 100.0 43.8
Bosmina (E.) coregoni 8 31.3 17.0
Bosmina (E.) longispina 10 80.0 36.2
Daphnia longispina-group 8 67.9 25.6
Daphnia pulex-group 2 7.0 7.0
Chydorus cf. sphaericus 20 89.5 19.7
Acroperus sp. 3 22.2 12.2
Alona glabra 13 28.6 6.7
Alona quadrangularis type 12 42.9 10.7
Alona cf. intermedia 1 5.6 -
Alona manueli 6 40.0 9.6
Alona ossiani 8 42.4 16.4
Alona rustica 1 4.3 -
Alonella excisa 3 4.3 2.5
Alonella nana 3 13.6 7.1
Alonella pulchella 4 6.1 3.7
Anthalona verrucosa-group 5 14.3 5.9
Camptocercus dadayi 6 30.8 13.7
Disparalona dadayi 2 11.9 9.0
Dunhevedia sp. 3 14.3 8.4
Ephemeroporus sp. 2 10.5 9.0
Euryalona sp. 11 25.0 11.3
Graptoleberis testudinaria 3 3.6 2.5
Kurzia sp. 4 13.3 7.2
Leberis sp. 5 50.0 16.6
Leydigia louisi louisi 10 34.4 7.8
Leydigia acanthocercoides-group 6 51.7 15.9
Leydigiopsis ornata 2 11.1 8.1
Notalona sculpta 7 15.9 7.1
Pleuroxus denticulatus 4 11.1 6.4
Simocephalus sp. 2 22.4 19.0
NRR1 4 31.8 11.4
NRR2 1 25.0 -
NRR3 1 4.3 -
NRR4 1 4.3 -
n, occurrence; NRR1-4, not recognize remains type 1 to 4; NRR2, prob-
ably headshield of Leberis sp.; NRR3, probably Coronatella monacan-
tha (Sars 1901) group.
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Fig. 4. Results of multivariate statistical analysis applied to qualitative and quantitative results of species composition of subfossil
Cladocera, and environmental variables. A) Cluster analysis showing species grouping according to reciprocal correlation level; the
groups were distinguished for species that showed a high level of similarity >0.8; species composition of each group is presented in
Tab. 3; B) Canonical correspondence analysis (CCA) for species relative abundances and environmental variables; length and direction
of arrows show respectively the strength and direction of a certain environmental variable.
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Subfossil Cladocera of Central America 159
1000 m asl. CCA analysis showed the preference of the
Daphnia pulex-group for clear waters, such as lakes Ati-
tlán and Ipala, that showed transparency of 4.2 m and 3.6
m, respectively. Moreover, the contribution of Daphniidae
was negatively correlated with conductivity and was
higher in waters with conductivity ≤100 µS cm–1. The re-
sults show the preference of Daphniidae for highlands and
mountain areas and clean, low-mineralized and nutrient-
poor waters. Similar environmental preferences by Daph-
niidae were also suggest by Hart (2004) and by Mergeay
et al. (2005) for African lakes. The occurrence of Daph-
niidae species in lakes of Central American highlands was
also observed by Peréz et al. (2013).
Bosminidae species were observed along the whole al-
titudinal gradient of the lake studied, from lowland, to high-
land and mountain lakes. CCA analysis revealed a negative
correlation of Eubosmina (Bosmina (E.) coregoni, Bosmina
(E.) longispina) and a positive correlation of Bosmina lon-
girostris with altitude. Eubosmina was found in six lowland
lakes, but also in two lakes located at >1000 m asl (Atitlán
and Ipala), in Lake Yojoa (639 m asl) and in Lake Apaste-
peque (509 m asl). This suggests that even though Eu-
bosmina prefered lakes located at a lower altitude, this is
probably not the main factor determining the distribution
of this genus. On the other hand, Eubosmina mainly oc-
curred in waters with high conductivity. These species were
dominant in highly mineralized (4520 µS cm–1) and brack-
ish (salinity=2.5‰) waters of Lakes Salpetén, as well as in
El Rosario and Lachuá, which showed conductivity values
>900 µS cm–1. The presence of Eubosmina, along with
Bosmina longirostris in Lake Salpetén, confirms the toler-
ance of Bosminidae to waters with high mineral content
and/or salinity (Aladin, 1991). The obtained results also
confirm the wide distribution of planktonic Daphniidae and
Bosminidae in Central America (Elías-Gutiérrez et al.,
1999; Korovchinsky, 2006).
Chydoridae was the most species rich group of Clado-
cera in the sediment studied. Chydorus cf. sphaericus was
the most common species, as it was present in 20 out of
the 29 surveyed lakes located both in lowland and moun-
tain areas. The relative abundance of Chydorus cf. sphaer-
icus in the lake located at the highest altitude (Lake
Magdalena, 2863 m asl) was almost 90%. CCA analysis
showed that none of the measured environmental factors
had a significant effect on the distribution of the species
in the region studied of Central America. This confirmed
the ubiquity of Chydorus cf. sphaericus and its wide range
of tolerance to environmental and ecological conditions
(Flössner, 2000; Fryer, 1968; Korhola and Rautio, 2001;
Zawisza and Szeroczyńska, 2011).
The genus Alona was mostly represented by Alona
glabra and the Alona quadrangularis type. These species
were found in 13 and 12 lakes, respectively, which were
characterized by different conductivity, oxygenation,
water visibility and altitude. The Alona quadrangularis
type was the unique littoral species found in Lake
Salpetén, which may indicate its tolerance to waters with
higher mineralization. The genus Alona was also repre-
sented by Alona manueli (Sinev and Zawisza, 2013) and
Alona ossiani, which, based on the cluster analysis, were
grouped together, along with Alonella nana (Baird, 1843),
Alonella pulchella (Herrick, 1884), the Anthalona verru-
cosa-group and Disparalona dadayi (Birge, 1910). The
multivariate analysis showed a negative correlation be-
tween Group 3 and lake conductivity, which most likely re-
sulted from the presence of species included in Group 3 in
lakes with conductivity ≤100 µS cm–1 and with medium
conductivity (204-331 µS cm–1). Lake Sacnab (412 µS
cm–1) and Lake Lachuá (906 µS/cm) are exceptions, and
two species from Group 3 (i.e., Alona ossiani and Alona
manueli, respectively) were present.
Sinev (1998) showed that Alona ossiani belongs to the
Alona affinis complex, which is considered an olig-
otrophic species in Eurasia (Kamenik et al., 2007; Ko-
rhola and Rautio, 2001). On the other hand, Alona
manueli (an endemic species of Central America) and
Alonella pulchella were identified in oligotrophic lakes in
Mexico (Cuna et al., 2014; Sinev and Zawisza, 2013).
Moreover, this studied provided the first record of
Alonella pulchella in the tropical region, as previously this
species was recorded only in Canada (Korosi and Smol,
2012). The obtained results seem to confirm the prefer-
ence of these species for waters of low trophic status. The
negative correlation of Group 3 with the lake area may in-
dicate the preference of these species for smaller lakes
with well-developed littoral zone. In particular, Alonella
Tab. 3. Groups of species correlated with each other at the minimum level of 0.8 and distinguished based on the cluster analysis.
Group Species composition
1 Daphnia pulex-group, Bosmina longirostris
2 Bosmina (E.) coregoni, Bosmina (E.) longispina, Alona glabra, Alona quadrangularis type, Leberis sp.
3 Alona manueli, Alona ossiani, Alonella nana, Alonella pulchella, Anthalona verrucosa-group, Disparalona dadayi
4 Euryalona sp., Kurzia sp., Leydigia acanthocercoides-group
5 Acroperus sp., Alona cf. intermedia, Camptocercus dadayi, Dunhevedia sp., Pleuroxus denticulatus
6 Alona rustica, Simocephalus sp.
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nana, was present in only three small lakes with area
≤0.1 km2. This suggests that, similarly to what observe in
Europe, Alonella nana may prefer small lakes (Fryer,
1968; Korosi and Smol, 2012). Furthermore, the presence
of Alona ossiani in mountain lakes may indicate a pro-
nounced tolerance toward the harsher climatic conditions
determined by altitude. The Eurasian species Alona affi-
nis, is considered to tolerate lower temperatures (Kamenik
et al., 2007; Locke and Sprules, 2000) and the results of
the present study indicated that Allona ossiani shows sim-
ilar characteristics in Central America.
Leydigia louisi louisi and Leydigia acanthocercoides-
group played a significant role in Lake El Muchacho (al-
most 90%), which was characterized by a water
transparency of only 0.4 m. Moreover, these species were
relatively abundant (>10%) in other lakes with water trans-
parency below 0.9 m. The CCA analysis confirmed the
preference of these species for waters with lower Secchi
visibility. The presence of a species characteristic of Central
America such as Leydigiopsis ornata, which is a typical
benthic species (Van Damme and Dumont, 2010), was
recorded only in 2 shallow (<2.5 m water depth) and
scarcely transparent lakes, which were characterized
(Secchi depth <1 m). Graptoleberis testudinaria, which
was recorded in the sediments of Lakes Atitlán, Quexil and
Verde, preferred waters with higher Secchi visibility
(≥2.7 m), as showed also by the CCA analysis. However,
the results of the multivariate statistical analysis are highly
controversial, because Garptoleberis testudinaria is com-
monly considered to be associated with aquatic vegetation
(Fryer, 1968; Rybak and Błędzki, 2016). This suggests that
other factors not included in our analysis control the distri-
bution of this species.
Pleuroxus denticulatus (Birge, 1879) remains were
identified in the sediments from four lakes (Chicabal,
Jucutuma, Ticamaya, Los Negritos) and its maximum
contribution to the Cladocera communities did not exceed
12% (average=6.4%). The presence of only one Pleuroxus
species in the lakes of the study area and its local distri-
bution confirms the rarity of this Cladocera group in the
tropical region (Korovchinsky, 2006).
Canonical correspondence analysis outlined altitude
as a key driver of the cladoceran fauna of in Central
America. Other significant environmental factors affect-
ing the Cladocera distribution were water transparency
and conductivity. Among the environmental variables
considered in this study, the less significant in affecting
the waterflea population in the study area was the concen-
tration of dissolved oxygen.
CONCLUSIONS
This study showed a relatively typical distribution of
Cladocera in lakes of the Neotropic region. In summary,
our results indicate that: i) the most common Cladocera
species of the study area was Chydorus cf. sphaericus,
likely in relation to the ability of this species to adapt to dif-
ferent ecological conditions; ii) planktonic species of Daph-
niidae and Bosminidae were the most abundant; iii)
Daphniidae species were recorded primarily in highland
lakes; iv) Eubosmina and the Alona quadrangularis type
showed pronounced tolerance to waters with high miner-
alizatiovn level; e) Alona ossiani, Alona manueli, Alonella
nana and Alonella pulchella were negatively correlated
with water conductivity; vi) the presence of Alonella nana
was restricted to lakes with a smaller surface area; vii)
Alona ossiani was an important subdominant species in
shallow lakes located at high altitudes; viii) among the en-
vironmental variables considered, altitude was a key driv-
ing factor for distribution of the Cladocera fauna whereas
dissolved water oxygenation was almost insignificant.
These results provide basic information on Cladocera
communities in freshwater ecosystems of Central Amer-
ica, a region where research carried out so far is insuffi-
cient to provide robust taxonomical and ecological
information.
ACKNOWLEDGMENTS
The study was funded by the Polish Ministry of Science
(Grant NCN 2014/13/B/ST10/02534) and the German Re-
search Foundation (DFG, SCHW 671/16-1). Furthermore,
scientific cooperation was supported by the Polish - Ger-
man governments (MNiSW-DAAD, 2016-2017). We
would like to thank Prof. A.Y. Sinev and Prof. A.A. Kotov
for their help with identification of specimens. Special
thanks is due to to Cuauhtémoc Ruiz (Instituto Tecnológico
de Chetumal), Ramón Beltrán (Centro Interdisciplinario de
Ciencias Marinas, Mexico), and Lisa Heise (Universidad
Autónoma de San Luis Potosí, Mexico) for their excellent
work on field. We also like to thank all people involved in
this work: Margarita Caballero (Instituto de Geofísica,
UNAM), Alexis Oliva and the team from the Asociación
de Municipios del Lago de Yojoa y su área de influencia
(AMUPROLAGO, Honduras), María Reneé Alvarez, Mar-
garita Palmieri, Eleonor de Tott (Universidad del Valle de
Guatemala, Guatemala), Consejo Nacional de Áreas Pro-
tegidas (CONAP, Guatemala), Néstor Herrera and Minis-
terio de Medio Ambiente (San Salvador, El Salvador).
CONACYT (Mexico) provided fellowship (218604,
405326) for the third and fourth authors.
REFERENCES
Aladin NV, 1991. Salinity tolerance and morphology of the os-
moregulation organs in Cladocera with special reference to
Cladocera from the Aral Sea. Hydrobiologia 225:291-299.
Bigler C, Heiri C, Krskova R, Lotter AF, Sturm M, 2006. Dis-
No
n c
om
me
rci
al
us
e o
nly
Subfossil Cladocera of Central America 161
tribution of diatoms, chironomids and Cladocera in surface
sediments of thirty mountain lakes in south-eastern Switzer-
land. Aquat. Sci. 68:154-171.
Bjerring R, 2007. Lake response to global change: nutrient and
climate effects using cladoceran (Crustacea) subfossils as
proxies. PhD Thesis, National Environmental Research In-
stitute University of Aarhus, Denmark.
Campanelli Mortari R, Henry R, 2016. Horizontal distribution
of Cladocera in a subtropical lake marginal to a river. J. Pa-
leolimnol. 75:109-120.
Cuna E, Zawisza E, Caballero M, Ruiz-Fernández AC, Lozano-
García S, Alcocer J, 2014. Environmental impacts of Little
Ice Age cooling in central Mexico recorded in the sediments
of a tropical alpine lake. J. Paleolimnol. 51:1-14.
Dumont HJ, 1994. On the diversity of the Cladocera in the trop-
ics. Hydrobiologia 272:27-38.
Elías-Gutiérrez M, Ciros-Pérez J, Suárez-Morales E, Silva-Bri-
ano M, 1999. The freshwater Cladocera orders Ctenopoda
and Anomopoda) of Mexico, with comments on selected
taxa. Crustacean 72:171-186.
Elías-Gutiérrez M, Kotov AA, Garfias-Espejo T, 2006. Clado-
cera (Crustacea: Ctenopoda: Anomopoda) from southern
Mexico, Belize and Northern Guatemala.Zootaxa 119:
1-27.
Elías-Gutiérrez M, Suárez-Morales E, Gutiérrez-Aguirre MA,
Silva-Briano M, Granados-Ramírez JG, Garfias-Espejo T,
2008. [Cladocera y Copepoda de las aguas continentales de
México].[Book in Spanish]. Universidad Nacional Autónoma
de México: 322 pp.
Feniova IY, Razlutsky VI, Palash AL, 2011. Temperature effects
of interspecies competition between Cladoceran species in
experimental conditions. Inland Water. Biol. 4:65-71.
Flössner D, 2000. [Die Haplopoda und Cladocera (ohne
Bosminidae) Mitteleuropas].[Book in German]. Backhuys
Publisher, Leiden: 428 pp.
Frey DG, 1986. Cladocera analysis, p. 667-692. In: B.E.
Berglund (ed.), Handbook of Holocene palaeoecology and
palaeohydrology. J. Wiley & Sons, Chichester.
Frolova L, Nazarova L, Pestryakova L, Herzschuh U, 2014.
Subfossil Cladocera from surface sediment in thermokarst
lakes in northern Siberia, Russia, in relation to limnological
and climatic variables, J. Paleolimnol. 52:107-119.
Fryer G, 1968. Evolution and adaptive radiation in the Chydoridae
(Crustacea: Cladocera): a study in comparative functional mor-
phology and ecology. Philos. T. R. Soc. B 254:221-385.
Green J, 1995. Altitudinal distribution of tropical planktonic
Cladocera. Hydrobiologia 307:75-84.
Hammer O, Harper DAT, Ryan PD, 2001. Past Paleontological
Statistics Software Package for Education and Data Analy-
sis. Palaeontol. Electron. 4:4-9.
Hart RC, 2004. Cladoceran periodicity patterns in relation to se-
lected environmental factors in two cascading warm-water
reservoirs over a decade, Hydrobiologia 526:99-117.
Hudec I, 2000. Subgeneric differentiation within Kurzia (Crus-
tacea: Anomopoda: Chydoridae) and a new species from
Central America. Hydrobiologia 421:165-178.
Jeppesen E, Leavitt P, De Meester L, Peder Jensen J, 2001.
Functional ecology and paleolimnology: using Cladocera
remains to reconstruction anthropogenic impact. Trends
Ecol. Evol. 16:191-198.
Juggins S, 2005. New features in C2 version 1.4. University of
Newcastle.
Juggins S, 2007. User guide C2 Software for ecological and pa-
leoecological data analysis and visualisation User guide Ver-
sion 1.5. University of Newcastle.
Kamenik C, Szeroczyńska K, Schmidt R, 2007. Relationships
among recent Alpine Cladocera remains and their environ-
ment: implications for climate-changes studies. Hydrobiolo-
gia 594:33-46.
Karmalkar AV, Bradley RS, Diaz HF, 2011. Climate change in
Central America and Mexico: regional climate model valida-
tion and climate change projections. Clim. Dyn. 37:605-629.
Kienast F, Wetterich S, Kuzmina S, Schirrmeister L, Andreev
AA, Tarasov P, Nazarova L, Kossler A, Frolova L, Kunitsky
VV, 2011. Paleontological records prove boreal woodland
under dry inland climate at today’s Arctic coast in Beringia
during the last interglacial. Quat. Sci. Rev. 30:2134-2159.
Kotov AA, Elías-Gutiérrez M, Guadalupe Nieto M, 2003. Ley-
digia louisi louisi Jenkin, 1934 in the Neotropics, L. louisi
mexicana n. subsp. in Central Mexican highlands. Hydrobi-
ologia 510:239-255.
Kotov AA, 2009. A revision of Leydigia Kurz, 1875
(Anomopoda, Cladocera, Branchiopoda), and subgeneric
differentiation within the genus. Magnolia Press: 84 pp.
Korhola A, 1999. Distribution patterns of Cladocera in subarctic
Fennoscandian lakes and their potential in environmental re-
construction. Ecography 22:357-373.
Korhola A, Rautio M, 2001. Cladocera and other Branchiopod
crustaceans, p. 5-41. In: J.P. Smol, J.B. Birks and W.M. Last
(eds.), Tracking environmental change using lake sediments.
Zoological indicators. Kluwer Academic, Dordrecht.
Korosi JB, Smol JP, 2012. An illustrated guide to the identifica-
tion of cladoceran subfossil from lake sediments in north-
eastern North America: part 2 - the Chydoridae, J.
Paleolimnol. 48:587-622.
Korovchinsky NM, 2006. The cladocera (Crustacea: Bra-
chiopoda) as a relict group. Zool. J. Linn. Soc. 147:109-124.
Locke A, Sprules WG, 2000. Effects of acidic pH and phy-
tolankton on survival and condition of Bosmina longirostris
and Daphnia pulex. Hydrobiologia. 437:187-196.
Luoto T, Sarmaja-Korjonen K, Nevalainen L, Kauppila T, 2009. A
700 year record of temperature and nutrient changes in a small
eutropied lake in southern Finland. Holocene 19:1063-1072.
Mergeay J, Verschuren D, De Meester L, 2005. Daphnia species
diversity in Kenya, and a key to the identification of their
ephippia. Hydrobiologia 542:261-274.
Mirosław-Grabowska J, Zawisza E, 2014. Late Glaciale early
Holocene environmental changes in Charzykowskie Lake
(northern Poland) based on oxygen and carbon isotopes and
Cladocera data. Quat. Int. 328-329:156-166.
Nováková K, Van Hardenbroek M, van der Knaap WO, 2013.
Response of subfossil Cladocera in Gerzensee (Swiss
Plateau) to early Late Glacial environmental change. Palaeo-
geogr. Palaeoclimatol. Palaeoecol. 391:84-89.
Padhye SM, Kotov AA, Dahanukar N, Dumont HJ, 2016. Bio-
geography of the ‘water flea’ Daphnia O.F. Müller, (Crustacea:
Branchiopoda: Anomopoda) on the Indian subcontinent. J.
Limnol. 75:1476.
Paterson MJ, 1994. Paleolimnological reconstruction of recent
changes in assemblages of Cladocera from acidified lakes
No
n c
om
me
rci
al
us
e o
nly
162 M. Wojewódka et al.
in the Adirondack Mountains (New York). J. Paleolimnol.
11:189-200.
Peréz L, Lorenschat J, Massaferro J, Pailles Ch, Sylvestre F, Holl-
wedel W, Brandorff GO, Brenner M, Islebe G, Lozano MS,
Scharf B, Schwalb A, 2013. Bioindicators of climate and
trophic state in lowland and highland aquatic ecosystems of
the Northern Neotropics. Rev. Biol. Trop. 61:603-644.
Rajapaksa R, Fernando CH, 1987. Redescription and assignment
of Alona globulosa Daday, 1898 to a new genus Notoalona
and a description of Notoalona freyi sp.nov. Hydrobiologia
144:131-153.
Rey J, Vasquez E, 1986. [Contribution à la connaissance des
Cladocères néotropicaux: redescription de Leydigiopsis or-
nata Daday, 1905. (Crustacea, Cladocera)].[Article in
Fench]. Ann. Limnol. 22:169-176.
Rybak JI, Błędzik LA, 2016. Freshwater Crustacean zooplank-
ton of Europe. Springer: 918 pp.
Schmidt R, Müller J, Drescher-Schneider R, Krisai R, Sze-
roczyńska K, Barić A, 2000. Changes in lake level and tro-
phy at Lake Vrana, a large karstic lake on the Islanad of Cres
(Croatia), with respect to palaeoclimate and anthropogenic
impacts during the last approx. 16,000 years. J. Limnol.
59:113-130.
Shurin JB, 2000. Dispersal limitation, invasion resistance, and
the structure of pond zooplankton comunities. Ecology
81:3074-3086.
Sinev AY, 1998. Alona ossiani sp. n., a new species of the Alona
affinis complex from Brazil, deriving from the collection of
G.O. Sars (Anomopoda Chydoridae). Arthropoda Sel.
7:103-110.
Sinev AY, 2001. Redescripton of Alona glabra Sars, 1901, a
South American species of the pulchella group (Bran-
chiopoda: Anomopoda: Chydoridae). Arthropoda Sel.
10:273-280.
Sinev A, Zawisza E, 2013. Comments on cladocerans of crater
lakes of the Nevado de Toluca Volcano (Central Mexico),
with the description of a new species, Alona manueli sp.
Nov. Zootaxa 3647:390-400.
Sinev A Y, 2015a. Revision of the pulchella-group of Alona s.
lato leads to its translocation to Ovalona Van Damme et Du-
mont, 2008 (Branchiopoda: Anomopoda: Chydoridae).
Zootaxa 4044:451-492.
Sinev AY, 2015b. Morphology and phylogenetic position of
three species of genus Camptocercus Baird, 1843 (Clado-
cera: Anomopoda: Chydoridae). Zootaxa 4040:169-186.
Sinev AY, Dumont HG, 2016. Revision of the costata-group of
Alona s. lato (Cladocera: Anomopoda: Chydoridae) con-
firms its generic status. Eur. J.Taxon. 223:1-38.
Sinev AY, Silva-Briano M, 2012. Cladocerans of genus Alona
Baird, 1843 (Cladocera: Snomopoda: Chydoridae) and re-
lated genera from Aguascalientes State, Mexico. Zootaxa.
3569:1-24.
Sweetman JN, Rühland KM, Smol JP, 2010. Environmental and
spatial factors influencing the distribution of cladocerans in
lakes across the central Canadian Arctic treeline region. J.
Limnol. 69:76-87.
Szeroczyńska K,1991. Impact of prehistoric settlements on the
Cladocera in the sediments of Lakes Suszek, Błędowo, and
Skrzetuszewskie. Hydrobiologia 225:105-114.
Szeroczyńska K, Tatur A, Weckstrom J, Gąsiorowski M, No-
ryśkiewicz A, Sienkiewicz E, 2007. Holocene environmen-
tal history in northwest Finnish Lapland reflected in the
multi-proxy record of small subartic lake. J. Paleolimn.
38:25-47.
Szeroczyńska K, Zawisza E, 2011a. Subfossil faunal and floral
remains (Cladocera, Pediastrum) in two northern Lobelia
lakes in Finland. Knowl. Manag. Aquat. Ect. 403:09.
Szeroczyńska K, Zawisza E, 2011b. Records of the 8200 cal BP
cold event reflected in the compositionof subfossil Clado-
cera in the sediments of three lakes in Poland. Quat. Int.
233:185-193.
Szeroczyńska K, Zawisza E, Wojewódka M, 2015. Initial time
of two high altitude crater lakes (Nevado De Toluca, Central
Mexico) recorded in subfossil Cladocera. Stud. Quatern.
32:109-116.
Taylor MA, Alfaro EJ, 2005. Climate of Central America and
the Caribbean, p. 181-189. In: J.E. Oliver (ed.), Encyclope-
dia of world climatology. Springer, Dordrecht.
ter Braak CJF, 1986. Canonical correspondence analysis: a new
eigenvector technique for multivariate direct gradient analy-
sis. Ecology 67:1167-1179.
Van Damme KV, Dumont HJ, 2010. Cladocera of the Lençóis
Maranhenses (NE - Brazil): faunal composition and a reap-
praisal of Sars’ method. Braz. J. Biol. 70:755-779.
Van Damme KV, Sinev AY, Dumont HJ, 2011. Separation of An-
thalona gen.n. from Alona Baird, 1843 (Branchiopoda:
Cladocera: Anomopoda): morphology and evolution of
scraping stenothermic alonines. Zootaxa 2875:1-64.
Zawiska I, Słowiński M, Correa-Metrio A, Obremska M, Luoto
T, Nevalainen L, Woszczyk M, Milecka K, 2015. The re-
sponse of a shallow lake and its catchment to Late Glacial
climate changes - A case study from eastern Poland. Catena
126:1-10.
Zawisza E, Szeroczyńska K, 2011. Cladocera species composi-
tion in lakes in the area of the Hornsund Fjord (Southern
Spitsbergen)-Preliminary results, Knowl. Manag. Aquat. Ec.
402:04.
Zawisza E, Caballero M, Ruiz-Fernandez C, 2012. 500 years of
ecological changes recorded in subfossil Cladocera in a
high-altitude tropical lake Lago de La Luna, Central Mex-
ico. Stud. Quatern. 29:23-29.
Zawisza E, Correa-Metrio A, Caballero M, Lozano S, Sze-
roczyńska K, 2014. Paleoecology of tropical Lake Zirhauen
(Western Mexico) recorded in Cladocera remains. Abstract
book of the 8th Shallow lakes Conf., Antalya, Turkey.
Zawisza E, Cuna E, Caballero M, Ruiz-Fernandez AC, Sze-
roczyńska K, Woszczyk M, Zawiska I, 2016. Environmental
changes during the last millennium recorded in subfossil
Cladocera, diatoms and sediment geochemistry from Lake
El Sol (Central Mexico). Geol. Q. (in press).
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