Chironomids, diatoms and microcrustaceans that inhabit aquatic ecosystems of the Northern Neotropics are abundant and diverse. Some species are highly sensitive to changes in water chemical composition and trophic state. This study was undertaken as a first step in developing transfer functions to infer past environmental conditions in the Northern lowland Neotropics. Bioindicator species abundances were related to multiple environmental ]]>
state gradient and steep gradients of altitude (~0-1 560m.a.s.l.) and precipitation (~400-3 200mm/y), from NW Yucatán Peninsula (Mexico) to southern Guatemala. We related 14 limnological variables to relative abundances of 282 diatom species, 66 chironomid morphospecies, 51 species of cladocerans, 29 non-marine ostracode
species and six freshwater calanoid copepods. Multivariate statistics indicated that bicarbonate is the strongest driver of chironomid and copepod distribution. Trophic state is the second most important factor that determines chironomid distribution. Conductivity, which is related to the precipitation gradient and marine influence on the Yucatán Peninsula, is the main variable that shapes diatom, ostracode and cladoceran communities. Diatoms, chironomids and cladocerans displayed higher diversities (H=2.4-2.6) than ostracodes and copepods (H=0.7- 1.8). Species richness and diversity were greater at lower elevations (<450m.a.s.l.) than ]]>
Los quironómidos, diatomeas y microcrustaceos que habitan ecosistemas acuáticos en el norte de los Neotrópicos son abundantes y diversos. Algunas especies son altamente sensibles a cambios en la composición ]]>
Palabras clave: microcrustáceos, quironómidos, diatomeas, ecosistemas acuáticos, norte de los Neotrópicos, autecología, diversidad. ]]>
Natural and anthropogenic factors influence physical and chemical lake variables and aquatic biota, especially environmentally sensitive phytoplankton, phytobenthos, zooplankton and zoobenthos communities. Such factors include water extraction, pollution, eutrophication, flow modification, changes in water level, habitat degradation, climate warming, and changes in evaporation and precipitation (Dudgeon
et al. 2006). Continental waterbodies are some of the most endangered ecosystems in the world (Sala et al. 2000), especially those in developing countries (Pérez et al. 2011a). Waterbodies in the Northern Neotropics are important resources for local inhabitants. They provide drinking water, sites for recreation, navigation, and habitat for both aquatic and terrestrial fauna and flora (Dudgeon et al. 2006). Despite their ]]>
et al. 2011a). Many local inhabitants around the largest lakes in Guatemala, Lakes Izabal, Petén Itzá, Amatitlán and Atitlán, rely on local fisheries for subsistence and to generate income in local markets. Such activities have affected the trophic state of these lakes. Lake Petén Itzá, located in the Maya Biosphere Reserve in Northern Guatemala still displays high diversity of aquatic bioindicators, but cultural eutrophication in the ]]>
et al. 2004, Pérez et al. 2010a), putting many species at risk. Lake Amatitlán is highly productive and has suffered from cultural eutrophication for decades (Pérez et al. 2011a). Aquatic bioindicator diversities in the lake are probably low because of the hypereutrophic conditions. Cyanobacteria dominate the phytoplankton community in the lake, and high rates of decomposition ]]>
et al. 2011a).
Aquatic organisms that are sensitive to changes in water chemical composition, pollution and trophic state, i.e. aquatic bioindicators such as diatoms, chironomids ]]>
et al. 2000, Walseng et al. 2006). Diatoms are unicellular golden-brown algae (Bacillariophyta) characterized by silica shells (frustules) that are well preserved in lake sediments. Diatoms live in planktonic and benthic habitats (Battarbee et al. 2001). ]]>
et al. 1995). They are ubiquitous inhabitants of Neotropical aquatic ecosystems. Nevertheless, there have been few studies in the region concerning their taxonomy and autecology (Pérez et al. 2010a). ]]>
et al. 2000). Ostracode valves and cladoceran exoskeletons preserve well in lake sediments. Body parts of freshwater copepods (<2.0mm long), however, are poorly preserved. Nevertheless, ]]>
et al. 2003). Microcrustaceans, diatoms and ]]>
Consistent taxonomy, ]]>
et al. 1991, Smith 1993, Pérez et al. 2011b), total phosphorus concentration (Hausmann & Kienast 2006), lake level (Sylvestre 2002), air temperature (Walker et al. 1997, Brooks & Birks 2001), pH and organic matter concentration (Rosén et al. 2000), and changes in precipitation and trophic state (Massaferro et al. ]]>
et al. 2010a).
There has been little research on the autecology of lacustrine organisms in the Northern Neotropics. Most studies have focused on taxonomy and biogeography. Studied groups include cladocerans (Elías-Gutiérrez et al. 2006, 2008) and copepods (Suárez-Morales & Elías-Gutiérrez ]]>
et al. (2010a,b,c, 2011b) recently conducted studies on the freshwater ostracode fauna of the Yucatán Peninsula and surrounding areas. There are, however, few studies on diatoms and chironomids. This study presents information on chironomid, diatom, cladoceran, copepod and ostracode taxa from 63 waterbodies in the Northern Neotropics, along with associated environmental data. Our objective was to determine the factors that govern the distributions of these bioindicators so they could be used to infer late Quaternary environmental conditions and ]]>
Materials and methods
Study site: The Yucatán Peninsula (Mexico, Guatemala and Belize, Fig. 1) and surrounding areas are rich in aquatic ecosystems that have different origins (tectonic, volcanic, karstic) and possess diverse water chemical composition. Chemical characteristics of waterbodies are mainly influenced by bedrock geology, climate and saltwater intrusion at coastal sites (Pérez et al. 2011a). The Yucatán Peninsula (
Fig. 1) is a marine carbonate platform. The region is of interest to ecologists and paleoecologists alike, because it displays steep, increasing NW-S precipitation (~400- 3 200mm/y) and altitude (~0-1 560m.a.s.l.) gradients (Pérez et al. 2011a). A dry season (January-May) and a rainy season (June- October) characterize the Yucatán Peninsula and surrounding areas. Short-duration showers usually occur from November to ]]>
et al. 2002). Most of the study area is located in a dry tropical climate zone that is rich in aquatic ecosystems and displays high aquatic biodiversity (Lutz et al. 2000, Pérez et al. 2011a).
Sampling and habitat ]]>
Two fieldtrips were carried out in the Yucatán Peninsula (Mexico), Guatemala and Belize (14°13’00”-21°25’00” N and 87°20’00”- 91°03’00” W) in 2005-2006 and 2008. A single sampling was carried out for each lake. Chironomids, diatoms and microcrustaceans (cladocerans, copepods, ostracodes) were collected from 63 aquatic ecosystems (Fig. 1, Table 1a, b). These ecosystems included deep (10-340m) and shallow (<10m) lakes (
Table 1a), “cenotes” (sinkholes), coastal lagoons, ponds, rivers, and wetlands (Table 1b). Surface sediment samples (lake deepest point, littoral zones, other water depths) were retrieved using an Ekman grab. Ostracodes and cladocerans that live in macrophyte-rich littoral zones were collected with 250μm and 100μm-mesh hand nets, respectively. Physical and chemical variables and the chemical and isotopic composition of lake waters were studied to better characterize the habitat. Water samples were collected from at least three depths above ]]>
in situ using a WTW Multi Set 350i. Most measurements were done at midday. Water samples were collected in duplicate for laboratory analysis of Ca, Na, Mg, K, Cl, HCO3, SO4, and for 18O ]]>
13CDIC analysis. 18O values were used as an indicator of the balance between evaporation and precipitation and 13C values as a productivity proxy (Schwalb 2003). Cations were measured using an ICP-OES Jobin Yvon JY 50 P Spectrometer. Bicarbonate was determined by titration with 0.1N HCl. Anions were measured using a 761 Compact IC Methrom at the Institut für Umweltgeologie, Technische Universität Braunschweig, Germany. Carbon and oxygen isotopes in waters were analyzed on a VG/ Micromass PRISM Series II isotope ratio mass spectrometer and a Finnigan-MAT DeltaPlus XL isotope ratio mass spectrometer with a GasBench II universal on-line gas ]]>
Bioindicator analysis: Surface sediments (~3g wet sediment) for chironomid analysis were (1) deflocculated in 10% KOH, (2) heated to 70°C for 10 minutes, (3) heated in water to 90°C for 20 minutes, and (4) sieved using 212μm and 95μm-mesh sieves. Chironomid head capsules were extracted from ]]>
et al. (2010a). We identified taxa to the morphospecies level because taxonomic data are generally lacking for the Northern Neotropics.
Sediment samples for diatom ]]>
3, then with 33% H2O2, followed by successive rinsing and decanting with distilled water. Sub-samples of the homogenized solution were diluted by adding distilled water and were left to settle onto coverslips until dry. The coverslips were fixed onto glass slides with Naphrax® mountant (refraction index=1.73). Counting was performed generally on three slides using a Nikon NS600 microscope at 1000x magnification. The total number of valves counted per sample varied from 50 in nearly sterile samples to >1000 in rich samples. Diatom identification and taxonomy ]]>
Surface sediments were initially analyzed for cladocerans using low magnification on a light microscope. Remains were isolated, identified, and counted and specimens were kept ]]>
et al. (2008) and Van Damme et al. (2011). Calanoid copepods that live in open waters and littoral zones ]]>
et al. (2008). The details of the method used for ostracode analysis is in Pérez et al. (2011b). At least 100 adult ostracode valves were extracted from 50mL of wet ]]>
stacked sieves (630-, 250-, 63μm mesh). Both hard and soft parts were analyzed and used for identification to species level when possible. Identification followed Furtos (1933, 1936a, b), Brehm (1939), Keyser (1976), and Pérez et al. (2010a, b, c, 2011 b). Samples are stored at the Institut für Geosysteme und Bioindikation, Braunschweig, Germany. All bioindicator data are presented as relative abundances.
Species richness (S), i.e. the total number of species, and biodiversity, i.e. the Shannon Wiener Index (H) (Krebs 1989), were determined for each taxonomic group (chironomids, diatoms, cladocerans, copepods and ostracodes) in all waterbodies. Multivariate analysis was used to characterize species autecology by relating species relative abundances to water variables. Prior to statistical analysis,
14 environmental variables (water depth, water temperature, conductivity, dissolved oxygen (DO), pH,18O, 13CDIC, Ca, K, Mg, Na, Cl, HCO3, SO4) from all waterbodies were standardized (x-mean/st dev) and species relative abundances were log-transformed. Rare species, i.e. those present in <3 waterbodies, and samples containing few or no specimens, were excluded from analysis. Species included in the multivariate analysis are shown in bold in tables 2, 3 and 4. Thirty-eight ]]>
3, 13C, water depth) and diatoms (DO, pH, temperature, conductivity, 13C, 18O, water depth), four for cladocera (DO, temperature, HCO3, conductivity), and six for copepods (temperature, HCO3, Na, Cl, 18O, water depth) and ]]>
3, Na, conductivity, water depth). Forward selection of the environmental variables followed Hausmann & Kienast (2006) and Mischke et al. (2007).
Detrended Correspondence Analysis ]]>
(CCA) were used to relate counts (relative abundance) of chironomids, diatoms, cladocerans and ostracodes to environmental variables, whereas Redundancy Analysis (RDA) was used for copepod counts. This was accomplished using Canoco for Windows 4.55 (Ter Braak & Šmilauer 2002). We first estimated the length of environmental gradients using a DCA and then used a CCA and RDA to discern the environmental factors that control bioindicator distributions in the study area. Generally, if a gradient is short ]]>
Results
We collected 66 chironomid species ]]>
Table 2), 282 diatom species that belong to the orders Centrales and Pennales (Table 3), 51 cladoceran species belonging to the orders Anompoda and Ctenopoda, six copepod species (Calanoida), and 29 ostracode species Podocopina, Table 4). Photographs of selected species are shown in
figure 2. Figures 3, 4, 5 and 6 display the relative abundances and altitude ranges of the aquatic bioindicators.
Chironomids:
Figures 3 a, b, c display the relative abundances of the most common chironomid morphospecies, i.e. >10 individuals per waterbody and present in >2 aquatic ecosystems. The dominant tribe was Chironomini and consisted of 32 morphospecies (Table 2). Widely distributed taxa, i.e. present in >15 aquatic environments, included Cladotanytarsus sp.1, ]]>
Chironomus anthracinus, Cladopelma sp., Dicrotendipes sp., Goeldochironomus sp., Micropsectra sp., Parachironomus sp., Paratanytarsus sp.1, Polypedilum sp. And Polypedilum sp. 2. Chironomus ]]>
, Dicrotendipes sp., Goeldochironomus sp. And Labrundina sp. had the highest relative abundances in most aquatic environments. Most chironomid species were collected at lower elevations (<450m a.s.l.). Only 15 species were collected in aquatic ecosystems in the Guatemalan highlands. Dominant species in highland lakes were Apedilum sp., Apsectrotanypus sp. and Chironomus anthracinus.
Chironomus anthracinus dominated the chironomid community in hypereutrophic Lake Amatitlán, Southern Guatemala. Chironomids inhabiting mainly the Petén lowlands were Stempellina sp. and Coelotanypus/Clinotanypus. Chironomus plumosus was the dominant species in Progreso Lagoon, Belize, and Cladopelma ]]>
sp. was collected in all studied aquatic ecosystems in the Belizean lowlands. Species typical of the Yucatán lowlands were Cladotanytarsus sp. 1, Goeldochironomus sp. and Polypedilum sp.1 and sp. 2.
Diatoms: Diatoms were the most abundant and diverse taxonomic group studied. Figures a, b show the most abundant diatom species (>2 waterbodies). Pennate diatoms displayed the highest number of families and species. In contrast, centric diatoms were only represented by four families (Tables 3 a-e). Naviculaceae represents 162 of the 282 diatom species and were mainly ]]>
Brachysira procera, Cyclotella meneghiniana, Denticula kuetzingii, Encyonema densistriata, Mastogloia smithii and Nitzschia amphibia. Nitzschia amphibia and
Ulnaria delicatissima var. angustissima were found in all highland lakes. Aulacoseira granulata, Fragilaria crotonensis, Ulnaria acus and Ulnaria ulna were present in three of four sampled highland lakes. The dominant species in hypereutrophic Lake Amatitlán were Cyclotella meneghiniana and ]]>
Discostella aff. pseudostelligera. Fragilaria crotonensis isa species restricted to the highlands and the Eastern lowlands in Guatemala, whereas Staurosirella pinnata was only collected in Lake Izabal, in the Eastern lowlands of Guatemala. Interestingly, few waterbodies have a predominantly monospecific diatom flora, e.g. Lake Rosario (93.6% Nitzschia amphibioides), Lake ]]>
Fragilaria crotonensis), Almond Hill Lagoon 81.2% N. amphibia) and the pond called Belize 2 (72.6% Encyonema densistriata).
Microcrustaceans: Cladocera were the most diverse group of microcrustacea, with 51 species belonging to ]]>
Tables 4 a, b). Figures 5 a, b and figure 6 show the relative abundances of the most widespread cladoceran, copepod and ostracode ]]>
Cladocerans: Most collected cladoceran species belong to the order Anomopoda, family Chydoridae (Table 4 a). The greatest numbers of species were collected in lakes, ponds, and coastal waterbodies, whereas few species were collected in “cenotes” and rivers, where shells without soft parts were generally ]]>
Bosmina huaronensis, Ceriodaphnia dubia, Daphnia mendotae, Daphnia pulicaria, Moinodaphnia minuta and Simocephalus congener. Daphnia pulicaria and Simocephalus congener are restricted to highland lakes. Daphnia ]]>
was the only species collected in highly productive Lake Amatitlán. Ceriodaphnia cf. rigaudi and Bosmina huaronensis displayed high relative abundance (>35%) in the Eastern lowlands of Guatemala. Dunhevedia odontoplax was the only species restricted to the Petén and Belize lowlands, and like Ceriodaphnia dubia, was ]]>
Diaphanosoma brevireme, Simocephalus serrulatus, Bosmina tubicen, Ilyocryptus spinifer, Macrothrix elegans, Macrothrix cf.
spinosa, Anthalona verrucosa, Chydorus brevilabris and Chydorus eurynotus. Rare cladoceran species collected in only one waterbody of the lowlands include Coronatella circumfimbriata (Loché), Dadaya macrops (Jamolún), Karualona karua (Cenote), Kurzia longirostris (Chacan-Bata)
and Oxyurella ciliata (Cayucón).
Copepods: Only calanoid copepods were studied, and only six species belonging to the families Diaptomidae and Pseudodiaptomidae were identified (Table 4 b, Fig. 6). ]]>
Arctodiaptomus dorsalis, Leptodiaptomus siciloides and Prionodiaptomus colombiensis. Arctodiaptomus dorsalis was the only species collected in hypereutrophic Lake Amatitlán. Leptodiaptomus siciloides and P. colombiensis are rare species that live in the highlands and ]]>
Arctodiaptomus dorsalis was widely distributed in the lowlands, but mostly dominated aquatic ecosystems in the Petén lowlands. Mastigodiaptomus nesus is restricted to the Belize and Yucatán lowlands, whereas Pseudodiaptomus marshi inhabits the Petén and Belize lowlands. Except for Mastigodiaptomus ]]>
, which was found in Cenote Juarez, no calanoid copepods were collected from “cenotes” and rivers.
Ostracodes: Partial results on ostracode distribution in the Yucatán Peninsula and surrounding areas were published by Pérez et al. (2011b) and therefore only the most important results are presented here. Ostracoda was the group ]]>
Table 4 b, Fig. 6). Families with highest numbers of species included Cyprididae (n=11), Candonidae (n=6) and Limnocytheridae (n=5). The genera Limnocythere and Physocypria had the highest numbers of species (n=3). Ubiquitous species include Cypridopsis okeechobei, Cytheridella ]]>
, Darwinula stevensoni and Pseudocandona sp. (Fig. 6). There is a clear difference between highland and lowland assemblages and between fresh and brackish water assemblages. Species typical of the highlands are Candona sp., Chlamydotheca colombiensis, Ilyocypris cf. ]]>
gibba, Limnocythere sp. and Trajancypris sp. Physocypria denticulate inhabits aquatic ecosystems of the lowlands in Belize and Yucatán, whereas Physocypria globula is restricted to the Petén lowlands. Lowland rare species Cytherura sandbergi, Elpidium bromeliarum,
Eucypris sp., and Physocypria xanabanica, were collected in Celestún, Río Dulce, Laguna Rosario, and in the small pond Belize 1, respectively. Cypretta brevisaepta was abundant in Lake Oquevix and in a small pond nearby.
Species richness and diversity in ]]>
The species richness (S) and the Shannon Wiener diversity index (H) of diatoms, chironomids and microcrustaceans for the 63 studied aquatic ecosystems are shown in figures 7 a, b. Ostracodes were collected in 59 waterbodies, chironomids in 53 and cladocerans in 46. Copepods were found in only 30 aquatic environments. Lowland waterbodies (<450m.a.s.l.) displayed highest diversity values, up to H=2.6 (diatoms), and greatest species richness, as many ]]>
Chironomids and ostracodes were ]]>
Fig. 7 a). Sampled rivers lacked diatoms and cladocerans. Copepods were scarce in rivers, “cenotes” and coastal waterbodies. The Jamolún wetland was dominated by chironomids and cladocerans. Cladocerans and ostracodes were present in all the highland lakes. Lakes Amatitlán, Gloria, Petexbatún, Celestún and Laguna Rosada displayed H values of 0 for chironomids, cladocerans and calanoid copepods. Ostracodes yielded H values >0, in TÜM, a pond near Lake Oquevix, in the ]]>
bioindicators. Sabanita yielded an H>0 only for chironomids (H=1.8).
Chironomids were prominent mainly in lowland lakes. Up to 18 morphospecies were collected in Lake Yaxhá and in the pond Belize 2, and 16 species were collected in ]]>
Fig. 7 a). Hypereutrophic Lake Amatitlán had a monospecific chironomid assemblage of Chironomus anthracinus. Dicrotendipes sp. was the only species collected in Lake Petexbatún, southern Petén. Highest diversity was reported in Lakes Oquevix (H=2.50) and Yaxhá (H=2.54). ]]>
Diatoms were generally more diverse than other bioindicators in each waterbody. The number of diatom species per lake, if present, ranged from 7 to 28. Highest numbers of species (S>20) were reported in Lakes Petén Itzá, Yaxhá, Cobá, Yalahau, Milagros, San José Aguilar, ]]>
]]>
Highest cladoceran species richness was found in Crooked Tree Lagoon (33), Almond Hill Lagoon (21), Lakes Petén Itzá and Ocom, and in the Jamolún wetland (17). Few cladocerans were found in “cenotes” and coastal environments. The highest diversity index (H=2.4) was also found in Crooked Tree Lagoon. Male specimens were rare and reported for the cladoceran species Ceriodaphnia cf. rigauda,
Diaphanosoma brevireme, Ephemeroporus barroisi, Macrothrix elegans and Macrothrix paulensis.
Highest numbers of ostracode species (≤10) were collected in Lakes Bacalar and Milagros in Eastern Yucatán and in Ixlú River, Northern Guatemala (
Fig. 7 a). The largest and deepest lake, Petén Itzá, possessed nine ostracode species. Only a few waterbodies on the Yucatán Peninsula lacked ostracodes: Chacan Lara, Sabanita and Silvituc. Ostracodes were abundant on the Yucatán Peninsula, especially in the lowlands of Petén (S≥5). Rivers were characterized by relatively high numbers of species (S=5-10). Ostracodes in “cenotes” and in the Jamolún wetland were not as abundant as in other aquatic ecosystems. Ostracodes were highly diverse in rivers, and ]]>
Copepods were less abundant and diverse than chironomids, diatoms, cladocerans and ostracodes. Few calanoid copepod species (S≤2) were collected and were rarely found in rivers, “cenotes” or coastal waterbodies. Copepod diversity in the ]]>
Calibration of bioindicators on the Yucatán Peninsula: We assessed relationships between the various studied biological groups and environmental variables. Quantitative ]]>
]]>
To improve the performance of the CCA model, the number of environmental variables was reduced to include only those that best explain the bioindicator distributions. Forwardselected variables displayed low inflation factors (<5). Seven variables were related to chironomid (HCO3, 13C, pH, ]]>
18O, dissolved oxygen, temperature, pH, 13C, water depth), four to cladoceran (conductivity, HCO3, temperature, dissolved oxygen) and six to ostracode abundances (conductivity, HCO3, Na, water depth, temperature, pH) (Fig. 8). For copepods, a linear model was chosen because the gradient length was only 2.15 SD units. The first two axes in the DCA explained 72.9% of the variability in the copepod species data. The sum of eigenvalues was 1.6. Six forward-selected variables (HCO3, Cl, Na, ]]>
18O) were included in the final RDA. In the final CCAs and RDA, HCO3 was the main factor controlling chironomid and copepod assemblages on the Yucatán Peninsula (Fig. 8). Diatom, ]]>
13CDIC, a lake productivity proxy, and lakewater 18O, a proxy for changes in the balance between evaporation and precipitation and perhaps conductivity, were the second most important factors affecting chironomid and diatom distributions, respectively (Fig. 8). The final CCA for chironomids explained 4.8% (1=0.14, 2=0.11), 6.8% for diatoms (1=0.42, 2=0.33), 6.4% for cladocerans (1=0.27, 2=0.15), 9.9% for ostracodes (1=0.31, 2=0.13) of the variability in species data, and the final RDA for copepods explained 24.9% (1=0.25, 2=0.11) of the variability in species data (Table 5).
Chironomid species such as Stempellina sp., Goeldochironomus sp., Coelotanypus/Clinotanypus, ]]>
Paratanytarsus sp. 2, Tanytarsini A and Tanytarsini J were positioned in the lower left quadrant of the CCA ordination biplot Fig. 8 a). These species are typical of lowland waterbodies, especially those located on the Eastern part of the Yucatán Peninsula, Belize, and the central and Eastern areas of the Petén Lake District. Species located in the upper left quadrant inhabit mainly lowland aquatic ecosystems, except for Apedilum ]]>
sp. This species was collected at both high and low elevations, but was more abundant in highland Lake Atitlán. Apsectrotanypus sp., Cricotopus spp., Tanytarsini C and Stenochironomus sp. inhabit highland lakes and were positioned in the right upper quadrant of the biplot. The chironomid species Glyptotendipes sp. 2 in the upper part of the right quadrant of the ]]>
Chironomus anthracinus, located in the lower right quadrant, was the only species present in hypereutrophic LakeAmatitlán. Labrundina sp., Beardius sp. and Paratanytarsus sp.1 were widely distributed in the lowlands of the Yucatán Peninsula and surrounding areas. ]]>
Diatom species Halamphora coffeaeformis, Campylostylus normannianus, Nitzschia frustulum, Navicula palestinae, Tabularia fasciculata, Navicula salinarum,
Amphora securicula and Cocconeis placentula are located in the lower quadrant of the biplot (Fig. 8 b) and are characteristic of lakes with high conductivities, up to 38.2mS/cm. Species characteristic of lower conductivities and most diatom species typical of fresh waters are located near the central part of the biplot.
The CCA biplot for ]]>
Fig. 8 c). Simocephalus mixtus and Karualona muelleri were positioned in the upper right and left quadrant of the CCA biplot, respectively, because they dominated lakes with high conductivities (up to ~6 000μS/cm) such as Cenote, Almond Hill Lagoon, Chichancanab, Punta Laguna, Yalahau, among others.
Kurzia polyspina was located in the upper right quadrant because it prefers waters with dissolved oxygen concentrations between 7.3 and 8.3mg/L. Streblocerus pygmaeus, located in the lower left quadrant of the CCA biplot, is a species typical of warm lake waters (>25°C) with lower conductivities (<350μS/cm) such as Oquevix, Crooked Tree Lagoon and Cayucón. The dominant cladocerans in highland Lakes Atitlán, Amatitlán, Ayarza and Güija were ]]>
Ceriodaphnia dubia and Bosmina huaronensis, located in the upper and lower right quadrants, respectively. Moina minuta was typical of Lake Atescatempa, Izabal, Chacan-Bata, pond Belize 1 and the Jamolún wetland. Daphnia mendotae was the only species identified in surface sediments from Lake Amatitlán. ]]>
Similar to the findings for chironomids, bicarbonate determined calanoid copepod distribution in the study area (Fig. 8 d). Few specimens were collected in the highlands of Southern Guatemala, thus all species on the biplot are typical of the lowlands. Arctodiaptomus dorsalis, in the lower left quadrant of the ordination diagram, dominated lakes with fresh waters, ]]>
Mastigodiaptomus nesus, in the lower right quadrant, is typical of HCO3- rich waters (125-710mg/L), such as San José Aguilar, Loché, Juárez, Cobá, Punta Laguna, Chichancanab and Yalahau. Pseudodiaptomus marshi, in the upper right quadrant, is typical of lakes at low altitudes (<5m.a.s.l.), such as Lake Izabal, Guatemala and ]]>
The CCA biplot for ostracodes suggests that conductivity, followed by HCO3, are the main factors controlling ]]>
Fig. 8 e). Perissocytheridea cribosa, Cyprideis sp. and Thalassocypria sp. are situated in the positive part of axis 1, indicating their preference for high-conductivity waters (750μS/cm-55.3mS/cm). Ostracode species that prefer freshwaters are situated in the center of the CCA biplot.
Cypridopsis vidua, in the upper right quadrant of the CCA biplot, was more abundant in highland Lake Ayarza, Guatemala. Species tolerating the hypereutrophic water of Lake Amatitlán include Candona sp., Cypridopsis vidua and Darwinula stevensoni. Ostracodes displaying high abundances in highland and ]]>
Cypridopsis okeechobei, Cytheridella ilosvayi and Darwinula stevensoni. Potamocypris sp., in the upper left quadrant, was collected in Lakes Rosario, Yalahau, Loché pond and Cenote Timul, suggesting its preference for warm waters (up to 32°C) and waters with HCO3 concentrations as high as 707mg/L. ]]>
Discussion
Neotropical aquatic bioindicators across broad trophic and climatic gradients: We have provided a first comprehensive list of modern diatom (282) and chironomid (66) species for the region, along with species distributions, relative abundances ]]>
et al. 1995) and the N-S ]]>
et al. 1998). The second determinant variable for chironomid distribution was 13CDIC, an indicator of lake water productivity (McKenzie 1985), indicating the potential of some chironomid species as indicators of lake trophic state. Our results demonstrate that aquatic bioindicators on the Yucatán Peninsula are highly sensitive to changes in water column conductivity, alkalinity and trophic state.
Sánchez et al. (2002) ]]>
et al. 1997), El Salvador (Rivas Flores et al. 2010) and Nicaragua (Swain 1966). All studies indicated that Naviculaceae is a dominant family in waterbodies of the Northern Neotropics. Six species belonging to Naviculaceae, Thalassiosiraceae ]]>
Brachysira procera, Encyonema densistriata, Mastogloia smithii, Denticula kuetzingii, Cyclotella meneghiniana and Nitzschia amphibia. Nitzschia amphibian tolerates broad trophic state and conductivity ranges. Cyclotella ]]>
and Discostella aff. pseudostelligera dominated the hypereutrophic waters of Lake Amatitlán, Guatemala. Velez et al. (2011) used diatoms and other variables to infer environmental and cultural changes in and around this highland lake. They suggested that C. meneghiniana is an indicator of low lake levels, whereas N. amphibia indicates eutrophic waters. ]]>
Fragilaria crotonensis is a species typical of the highlands and Eastern lowlands in Guatemala. Fragilaria species indicate oligotrophic to mesotrophic conditions (Castellanos & Dix 2009). This species dominated (86.2%) in Lake Atitlán, a lake that experienced extensive cyanobacteria (Lyngbya hieronymusii/birgei/robusta) blooms in ]]>
et al. 2011). When we visited Lake Atitlán in March 2008, the lake still displayed oligo- to mesotrophic conditions, indicated by the dominance of F. crotonensis, shortly before the first cyanobacteria bloom, which occurred in December 2008.
Vinogradova & Riss (2007) ]]>
Cladopelma lateralis and species belonging to the genus Tanytarsus. Our dataset included a larger number of aquatic ecosystems (n=63), however results from both studies are similar. Few chironomid taxa are restricted to specific areas. Rather, the dipterans seem to tolerate a broad range of environmental conditions.
Chironomus anthracinus displayed high relative abundance in most sampled waterbodies and the larvae have been to shown to be among the dominant food items of fish (Armitage et al. 1995). This species was very abundant in many of our surface sediment samples. It tolerates eutrophic waters (Porinchu & Mac- Donald 2003), which characterize many lowland and some highland lakes in the study area. For instance, C. ]]>
was the only dipteran species collected in hypereutrophic Lake Amatitlán, Guatemala. For decades, this highly productive lake has received wastewater, delivered by its main inflow river, the Río Villalobos. This species was also collected in Cenote Timul, which displayed high 13CDIC values of +13.6‰ (Pérez et al. 2011a). These results illustrate that ]]>
C. anthracinus can be used as an indicator of highly productive waters in the Northern Neotropics. A larger number of species (n=51) inhabit the lowlands. Fewer species were identified in the highlands (n=15), suggesting that chironomids are very abundant in low-elevation neotropical regions, similar to findings in Africa (Eggermont et al. 2010), where 81 chironomid taxa were collected across an altitude gradient (489-4 575m.a.s.l.) and in Brazil (de Oliveira Roque & Trivinho-Strixino 2007), where 191 morphospecies were collected. ]]>
Cladocerans dominated the microcrustacean communities in the study area. Fifty-one species were collected in the waterbodies and the greatest number of species belonged to the family Chydoridae. Many species of Chydoridae have great value as water-quality indicators because they are highly sensitive to changes in lake trophic state (de Eyto et al. 2002). ]]>
et al. 2008). Mexico has been actively involved in studying the systematics of Cladocera (Elías-Gutiérrez et al. 2006). Therefore, identification of collected cladocerans and copepods to species level was possible. Elías-Gutiérrez (2006) reported a total of 162 cladoceran species for two regions of Mexico (Morelos and southeast Mexico), four ]]>
Diaphanosoma brevireme, Pseudosida ramosa, Macrothrix spinosa, M. elegans, Chydorus nitidilus, Ephemeroporus tridentatus, Alona ossiani, Oxyurella ciliata and
O. longicaudis (Elías-Gutiérrez 2006). One interesting finding of our study was the presence of Anthalona brandorffi, described as Alona brandorffi (Sinev & Hollwedel 2002) in the waterbodies Crooked Tree Lagoon, Silvituc Lagoon and Loché, because this species was found for the first time in Boa Vista, Brazil, and its distribution in the Northern Neotropics was unknown. Cladocerans were not as abundant in highland lakes of Guatemala. Laguna de Ayarza and Lake Atitlán still display oligo-mesotrophic ]]>
Daphnia mendotae, was collected in such extreme conditions. Species restricted to the highlands include D. pulicaria and S. congener, even though they apparently have wide distributions (Cerny & Hebert 1993, Illyová & Némethová 2005, Marrone et ]]>
. 2005). For instance, D. pulicaria seems to prefer cool waters, typical of highland Lake Atitlán (≤21.8°C). Occupying cooler, deep waters may be a strategy to reduce risk of predation (Stich & Maier 2007). Species restricted to aquatic ecosystems of Guatemala and Belize include: Dunhevedia odontoplax and Ceriodaphnia dubia. Dunhevedia odontoplax has been collected in Morelos, Veracruz (Elías-Gutiérrez 2006). Mainly cladoceran carapaces were collected in “cenotes” and ]]>
Only six calanoid copepod species were collected from the sampled waterbodies. Recent studies in Mexico (Elías-Gutiérrez et al. 2008, Brandorff 2012) report up to 100 freshwater copepod species, of which 20 species belong to the order Calanoida. Suárez- Morales & Reid (2003) suggest that ]]>
Prionodiaptomus colombiensis mainly inhabits altitudes from 10 to 100m.a.s.l and it has been previously reported in Tabasco, Mexico while Leptodiaptomus siciloides is widely distributed in Mexico (Elías-Gutiérrez et al. ]]>
Arctodiaptomus dorsalis tolerates a broad range of environmental conditions and was collected in waterbodies with different origins and trophic states. For instance, it inhabits hypereutrophic volcanic Lake Amatitlán in the highlands, and meso-oligotrophic, karst Lake Petén Itzá in the lowlands. According to Suárez-Morales (2003), this nearctic species is the most widespread diaptomid in the Yucatán Peninsula and has also been collected in Southeastern USA, central and Eastern Mexico, Central America and the Caribbean islands. Dispersal of this species is relatively recent (post-Pliocene) and it colonized the ]]>
Of the six copepod species found, M. reidae is endemic to Campeche (Elías-Gutiérrez et al. ]]>
Mastigodiaptomus found in the Yucatán Peninsula are neotropical. Suárez-Morales (2003) report another endemic species for the area, Mastigodiaptomus maya. Unfortunately, we did not collect this species, but it seems to coexist with M. reidae in Chicaná pond, near the Biosphere Reserve of Calakmul, Yucatán Peninsula, and ]]>
M. nesus inhabits waterbodies in Belize, Campeche, Quintana Roo and Yucatán, as reported by Elías-Gutiérrez et al. (2008). The present distribution of this taxon could be a remnant of the original Mastigodiaptomus fauna in the Yucatán Peninsula and may reflect recent, post-Pliocene dispersal and Holocene climatic fluctuations (Suárez-Morales 2003). We identified
P. marshi in aquatic ecosystems in the lowlands of Belize (Lagoons Progreso and Almond Hill) in the Eastern lowlands of Guatemala (Lake Izabal) and Southern Yucatán (Bacalar). Pseudodiaptomid copepods mainly inhabit marine and brackish water environments, although recent studies (Suárez-Morales 2003) suggest that P. marshi is a species that is starting to colonize freshwater environments. Canonical Correspondence Analysis indicated that the ions sodium and chloride affect the distribution of this species. But the fact that we collected ]]>
Effects of altitude ]]>
species distribution and assemblage composition in the study area are clear. The taxonomy, ecology and distribution of non-marine ostracodes from the Northern Neotropics (Mexico, Guatemala and Belize) was investigated by Pérez et al. (2010b, 2010c, 2011b), Darwinula stevensoni has a worldwide ]]>
Cytheridella ilosvayi is abundant throughout the entire continental Neotropics. Cypridopsis okeechobei displays a narrower distribution, extending from the United States to the Petén Lake District, Northern Guatemala. Pseudocandona sp. was also abundant and we suggest this species is endemic to the Yucatán Peninsula, but further taxonomic and molecular analysis is needed to test this assertion. We were unable to identify some ]]>
Candona sp., Limnocythere sp. and Trajancypris sp. A conductivity gradient is well marked on the Yucatán Peninsula. Ostracodes were mainly typical of freshwaters, but some, like Cyprideis sp., Loxoconcha sp.,
Paracytheroma stephensoni, Perissocytheridea cribosa and Thalassocypria sp. were typical of waterbodies with high conductivities, up to 55.3mS/cm. Cypretta brevisaepta had been reported only from Southern Florida and the West Indies, but we found it in Lakes Oquevix, Macanché, and a pond near Lake Oquevix in Petén, Guatemala and in San José ]]>
A broad trophic state gradient characterizes the study area, ranging from hypereutrophic Lake Amatitlán to oligotrophic Laguna Ayarza. Hypereutrophic Lake Amatitlán displayed species characteristic of highly productive waters, including Chironomus anthracinus, Discostella aff. pseudostelligera,
Daphnia mendotae, Candona sp., Cypridopsis vidua and Darwinula stevensoni. Our results demonstrate that few zooplankton and zoobenthos species inhabit higher elevations (>450m.a.s.l.) in Guatemala. Cladocerans, copepods and ostracodes were more diverse and abundant in lowland aquatic ecosystems, suggesting that environmental conditions in those waterbodies are optimal for zooplankton and zoobenthos development and reproduction. The Yucatán Peninsula ]]>
Importance of species richness and diversity of bioindicators in neotropical aquatic ]]>
Diversity and species richness data from waterbodies provide information on modern environmental conditions, e.g., trophic state, anthropogenic impact and urban development and the degree of degradation. Our findings provide information for identifying conservation hotspots on the Yucatán Peninsula, Guatemala and Belize. Highest species diversities were reported at lower elevations (<450m.a.s.l.). The highest number of species and diversities per waterbody were usually reported for lowland lakes, where precipitation is high, up to 3 050mm/y. Crooked Tree Lagoon, Belize displayed the highest diversity (H≤2.4, diatoms). The ]]>
This study on the waterbodies on and around the Yucatán Peninsula found that microcrustacea, insect larvae and diatoms in neotropical lakes are abundant, diverse and highly sensitive to environmental variables. Such organisms therefore have great potential as modern and late Quaternary bioindicators. This investigation generated the first training sets for ]]>
Analysis of the distribution and ecological preferences of the five studied groups (diatoms, ]]>
Apsectrotanypus sp., Cricotopus spp., Tanytarsini C, Stenochironomus sp., diatoms Ulnaria acus, cladocerans ]]>
huaronensis, ostracodes Candona sp., Chlamydotheca colombiensis, Cypridopsis vidua, Cytheridella ilosvayi, Darwinula stevensoni, Limnocythere sp., Physocypria globula, Stenocypris major and Trajancypris sp,
cladocerans D. pulicaria and S. congener and the copepods Leptodiaptomus siciloides and Prionodiaptomus colombiensis.
This study covered a wide range of trophic state, which allowed us to differentiate between species that are tolerant and intolerant of highly eutrophic waters. Bioindicator ]]>
Chironomus anthracinus, Cyclotella meneghiniana, Discostella aff. pseudostelligera, Daphnia mendotae, Arctodiaptomus dorsalis, Candona sp., Cypridopsis vidua and
Darwinula stevensoni. A broad conductivity gradient also characterizes the Yucatán Peninsula and surrounding areas. Most collected species inhabit freshwaters, but a few tolerate high conductivities, making them potential indicators of such conditions. They include diatoms such as Halamphora coffeaeformis, Campylostylus normannianus, Nitzschia frustulum, Navicula palestinae, Tabularia fasciculata,
Navicula salinarum, Amphora securicula, and Cocconeis placentula, cladocerans Simocephalus mixtus and Karualona muelleri, the copepod species P. marshi, as well as ostracodes Cyprideis sp., Perissocytheridea cribosa and
Thalassocypria sp. Good indicators of alkaline waters are Paratanytarsus sp.1, Djalmabatista sp., Endotribelos sp., and Mastigodiaptomus nesus, whereas waters with HCO3<275mg/L were dominated by Stempellina sp., Tanytarsini J, K, Apedilum sp and
Arctodiaptomus dorsalis.
Transfer functions that express quantitative relations between bioindicator species and environmental variables will ultimately be developed using results from this study. These transfer functions will be used to make quantitative paleoenvironmental inferences, by applying them to fossil assemblages in sediment cores retrieved from lakes in the region. Despite the ]]>
Acknowledgments
We are grateful to ]]>
are grateful for financial support provided by the Deutsche Forschungsgemeinschaft (DFG, grant Schw 671/3) and start-up money to A.S. provided by the TU Braunschweig.
]]>
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*Correspondencia: Liseth Pérez: Institut für Geosysteme und Bioindikation, Technische Universität Braunschweig, Langer Kamp 19c, 38106 Braunschweig, Germany/ Instituto de Geología, Universidad Nacional Autónoma de México (UNAM), Ciudad Universitaria, 04510, Distrito Federal, México. l.perez@tu-bs.de; lcpereza@geologia.unam.mx Julia Lorenschat: Institut für Geosysteme und Bioindikation, Technische Universität Braunschweig, Langer Kamp 19c, 38106 Braunschweig, Germany. j.lorenschat@tu-bs.de Julieta Massaferro: CENAC-APN, CONICET, San Martin 24, 8400, Bariloche, Argentina; julimassaferro@hotmail.com Christine Pailles: CEREGE, Université Aix-Marseille, CNRS, IRD, Europôle méditerranéen de l’Arbois, BP 80, 13545 Aix-en-Provence cedex 4, France. pailles@cerege.fr Florence Sylvestre: CEREGE, Université Aix-Marseille, CNRS, IRD, Europôle méditerranéen de l’Arbois, BP 80, 13545 Aix-en-Provence cedex 4, France. sylvestre@cerege.fr Werner Hollwedel: Oldenburger Strasse 16A, 26316, Varel, Germany. whollwedel@freenet.de Gerd-Oltmann Brandorff: Georg-Gröning-Str. 29A, 28209, Bremen, Germany. gobrandorf@aol.com Mark Brenner: Department of Geological Sciences & Land Use and Environmental Change Institute, University of Florida, Gainesville, 32611, Florida, USA. brenner@ufl.edu Gerald Islebe: Herbario, El Colegio de la Frontera Sur (ECOSUR), Unidad Chetumal, Av. del Centenario 424, 77000, Chetumal, Quintana Roo, México; gislebe@ecosur.mx ]]>
María del Socorro Lozano: Instituto de Geología, Universidad Nacional Autónoma de México (UNAM), Ciudad Universitaria, 04510, Distrito Federal, México. mslozano@unam.mx Burkhard Scharf: Institut für Geosysteme und Bioindikation, Technische Universität Braunschweig, Langer Kamp 19c, 38106 Braunschweig, Germany. burkhard.w.scharf@t-online.de Antje Schwalb: Institut für Geosysteme und Bioindikation, Technische Universität Braunschweig, Langer Kamp 19c, 38106 Braunschweig, Germany. antje.schwalb@tu-bs.de 1. Institut für Geosysteme und Bioindikation, Technische Universität Braunschweig, Langer Kamp 19c, 38106 Braunschweig, Germany; l.perez@tu-bs.de, j.lorenschat@tu-bs.de, burkhard.w.scharf@t-online.de, antje.schwalb@tu-bs.de 2. Instituto de Geología, Universidad Nacional Autónoma de México (UNAM), Ciudad Universitaria, 04510, Distrito Federal, México; lcpereza@geologia.unam.mx, mslozano@unam.mx 3. CENAC-APN, CONICET, San Martin 24, 8400, Bariloche, Argentina; julimassaferro@hotmail.com 4. CEREGE, Université Aix-Marseille, CNRS, IRD, Europôle méditerranéen de l’Arbois, BP 80, 13545 Aix-en-Provence cedex 4, France; pailles@cerege.fr, sylvestre@cerege.fr 5. Oldenburger Strasse 16A, 26316, Varel, Germany; whollwedel@freenet.de 6. Georg-Gröning-Str. 29A, 28209, Bremen, Germany; gobrandorf@aol.com 7. Department of Geological Sciences & Land Use and Environmental Change Institute, University of Florida, Gainesville, 32611, Florida, USA; brenner@ufl.edu 8. Herbario, El Colegio de la Frontera Sur (ECOSUR), Unidad Chetumal, Av. del Centenario 424, 77000, Chetumal, Quintana Roo, México; gislebe@ecosur.mx
Received 29-V-2012. Corrected 02-IX-2012. Accepted 04-X-2012.
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18O ]]>
13CDIC analysis. 
2=0.11), 6.8% for diatoms (1=0.42,