Bioindicators of climate and trophic state in lowland and highland aquatic ecosystems of the Northern Neotropics.
Aquatic organisms that are sensitive to changes in water chemical composition, pollution and trophic state, i.e. aquatic bioindicators such as diatoms, chironomids and microcrustaceans, are frequently used to track environmental change. Diatoms are generally a dominant group in the phytoplankton, whereas cladocerans, copepods and ostracodes are typically the main zooplankters in fresh waters (Dole-Olivier 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). Chironomids are non-biting midges (Insecta: Diptera) and are frequently the most abundant group of aquatic insects in fresh waters. Chironomids are true flies, but they spend most of their life cycle (egg, larva, pupa) in aquatic habitats (Armitage et al. 1995). They are ubiquitous inhabitants of Neotropical aquatic ecosystems. Nevertheless, there have been few studies in the region concerning their taxonomy and aut-ecology (Perez et al. 2010a). Microcrustaceans such as ostracodes, cladocerans and copepods are important organisms in limnological and paleolimnological studies. Ostracodes are typically <3mm long. The two valves that enclose the body are composed of low-Mg calcite (Meisch 2000). Similar to ostracodes, cladocerans are small (0.2-2.5mm). Limbs and a postabdomen extend from a ventral opening in the carapace, facilitating locomotion and feeding (Dole-Olivier 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, sacs with resting eggs of some copepod species are robust and well preserved in late Quaternary lake sediments (Bennike 1998). Microcrustaceans, diatoms and chironomids are the main food sources for many aquatic macroinvertebrates and for vertebrates such as fish. They are key components of the food web in lake ecosystems and therefore of great ecological and economic value (Cohen 2003, O'Sullivan & Reynolds 2004). Impacts on these communities from pollution, changes in lake trophic state or climate, can have dramatic consequences for fish populations (Moss et al. 2003). Microcrustaceans, diatoms and chironomids are widely distributed, can rapidly colonize new habitats (Cohen 2003, Hausmann & Pienitz 2007) and share characteristics that make them useful as bioindicators and paleo-indicators: (1) their well preserved remains in lake sediments can be identified to genus, and sometimes to species level, (2) they are often abundant, (3) they are highly sensitive to environmental changes, (4) they have short life cycles and communities thus respond quickly to environmental changes.
Consistent taxonomy, along with information on species autecology and the factors that affect species distributions and diversity, are indispensable to ensure that inferences from bioindicators, whether in modern or paleoenvironmental contexts, are valid. There have been few paleolimnological studies using bio-indicators in remote tropical areas, in large part because of the paucity of autecological data. Detailed bioindicator analysis, coupled with information on physical and chemical attributes of aquatic ecosystems, is required to fully exploit the utility of such bioindicator taxa. These taxonomic groups are highly sensitive to environmental changes, such as shifts in salinity, conductivity or ionic concentration (Fritz et al. 1991, Smith 1993, Perez 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 (Rosen et al. 2000), and changes in precipitation and trophic state (Massaferro et al. 2004, Perez et al. 2010a).
There has been little research on the aut-ecology of lacustrine organisms in the Northern Neotropics. Most studies have focused on taxonomy and biogeography. Studied groups include cladocerans (Elias-Gutierrez et al. 2006, 2008) and copepods (Suarez-Morales & Elias-Gutierrez 2000, Suarez-Morales & Reid 2003). Perez et al. (2010a,b,c, 2011b) recently conducted studies on the freshwater ostracode fauna of the Yucatan 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 climate on the Yucatan Peninsula, Guatemala and Belize. In this study, we (1) present an inventory of the main species that inhabit aquatic ecosystems of the Northern Neotropics, (2) display ecological information from the studied waterbodies, (3) evaluate relationships between bioindicator relative abundances and environmental variables, (4) identify areas with high species richness and diversity that could be of conservation interest in this zoogeographic province and (5) develop a basis for transfer functions that can be applied in paleolimnological studies to infer past environmental variables such as water chemical composition and lake level. Ultimately, these transfer functions will be applied to fossil assemblages in long sediment cores retrieved from Lago Peten Itza, Guatemala and other waterbodies in the Northern Neotropics to infer past environmental variables.
MATERIALS AND METHODS
Study site: The Yucatan 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 (Perez et al. 2011a). The Yucatan 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 (Perez et al. 2011a). A dry season (January-May) and a rainy season (June-October) characterize the Yucatan Peninsula and surrounding areas. Short-duration showers usually occur from November to December (Schmitter-Soto 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, Perez et al. 2011a).
Sampling and habitat characterization:
Two fieldtrips were carried out in the Yucatan Peninsula (Mexico), Guatemala and Belize (14[degrees]13'00"-21[degrees]25'00" N and 87[degrees]20'00"91[degrees]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 250[micro]m and 100[micro]m-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 the lake's deepest point (surface, mid-depth and bottom). Only surface waters near the shore were collected in smaller water bodies (ponds, rivers and wetlands). Water temperature, dissolved oxygen, pH and conductivity in surface waters were measured 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 [delta][sup.18]O and [delta][sup.13][C.sub.DIC] analysis. [delta][sup.18]O values were used as an indicator of the balance between evaporation and precipitation and [[delta].sub.13]C 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 fur Umweltgeologie, Technische Universitat 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 preparation device at the University of Florida, USA.
Bioindicator analysis: Surface sediments (~3g wet sediment) for chironomid analysis were (1) deflocculated in 10% KOH, (2) heated to 70[degrees]C for 10 minutes, (3) heated in water to 90[degrees]C for 20 minutes, and (4) sieved using 212Lim and 95Lim-mesh sieves. Chironomid head capsules were extracted from samples using a Bogorov sorting tray and fine forceps. Head capsules were slide-mounted in Euparal, identified, counted and photographed. Identification followed Perez et al. (2010a). We identified taxa to the morphospecies level because taxonomic data are generally lacking for the Northern Neotropics.
Sediment samples for diatom analysis were treated with hot concentrated HN[O.sub.3], then with 33% [H.sub.2][O.sub.2], 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[R] 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 followed Krammer & LangeBertalot (1986, 1988, 1991a, 1991b) revised by the nomenclature of E. Fourtanier & J.P. Kociolek (on-line version of the Catalog of Diatom Names: http://research.calacademy.org).
Surface sediments were initially analyzed for cladocerans using low magnification on a light microscope. Remains were isolated, identified, and counted and specimens were kept in small vials filled with 3-4% formaldehyde solution. Several drops of glycerin were added to all vials to prevent desiccation. Permanent preparations of peculiar species were prepared for detailed microscopic observation to facilitate identification. We used polyvinyl lactophenol or Hydro-Matrix[R] as mounting media. Species were identified using the works of Korovchinsky (1992), Smirnov (1992, 1996), Lieder (1996), Flossner (2000), Kotov & Stifler (2006), Elias-Gutierrez et al. (2008) and Van Damme et al. (2011). Calanoid copepods that live in open waters and littoral zones were sampled with a plankton net (100-Lm mesh), preserved with 10% formalin, and identified and counted under a dissecting microscope. Literature used for taxonomic identification included Bowman (1996), Gutierrez-Aguirre & Suarez-Morales (2000), Suarez-Morales & Elias-Gutierrez (2000, 2001), and Elias-Gutierrez et al. (2008). The details of the method used for ostracode analysis is in Perez et al. (2011b). At least 100 adult ostracode valves were extracted from 50mL of wet surface sediment. Samples were wet-sieved using stacked sieves (630-, 250-, 63Lm 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 Perez et al. (2010a, b, c, 2011 b). Samples are stored at the Institut fur 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 aut-ecology by relating species relative abundances to water variables. Prior to statistical analysis, 14 environmental variables (water depth, water temperature, conductivity, dissolved oxygen (DO), pH, [delta][sup.18]O, [delta][sup.13][C.sub.DIC], Ca, K, Mg, Na, Cl, HC[O.sub.3], [SO.sub.4]) 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 chironomid, 97 diatom, 32 cladoceran, 3 copepod and 17 ostra-code species were included in the statistical analysis. Correlations between environmental factors and the relative abundance of organisms were explored using Pearson correlation, which allowed up to seven environmental variables to be included in statistical analysis. Seven environmental variables were forward selected for statistical analysis of chironomids (DO, pH, temperature, conductivity, HC[O.sub.3], [delta][sup.13]C, water depth) and diatoms (DO, pH, temperature, conductivity, [[delta].sub.13]C, [[delta].sub.18]O, water depth), four for cladocera (DO, temperature, HC[O.sub.3], conductivity), and six for copepods (temperature, HC[O.sub.3], Na, Cl, [delta][sup.18]O, water depth) and ostracodes (temperature, pH, HCO3, Na, conductivity, water depth). Forward selection of the environmental variables followed Hausmann & Kienast (2006) and Mischke et al. (2007).
Detrended Correspondence Analysis (DCA) and Canonical 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 & Smilauer 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 (<3 SD), a linear model should be used, whereas with larger gradients (>4 SD), a unimodal model is recommended, because the approximation using the linear function is poor (Leps & Smilauer 2003).
We collected 66 chironomid species and morphospecies belonging to the subfamilies Chironominae, Orthocladiinae and Tanypodinae (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 anthracinus, 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 Amatitlan, Southern Guatemala. Chironomids inhabiting mainly the Peten 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 Yucatan 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 4 a, b show the most abundant diatom species ([greater than or equal to]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 distributed in lowland waterbodies on the Yucatan Peninsula. Widely distributed diatom species, i.e. those found in >20 waterbodies, include 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 Amatitlan were Cyclotella meneghiniana and Discostella aff. pseudostelligera. Fragilaria crotonensis is a 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 Atitlan (86.2% 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 seven families. Ostracodes were next, with 29 species distributed in 10 families. Calanoid copepods followed, with six species belonging to two families (Tables 4 a, b). Figures 5 a, b and figure 6 show the relative abundances of the most widespread cladoceran, copepod and ostracode species, i.e. those present in >2 aquatic environments.
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 found. Assemblages in the highlands were dominated by Bosmina huaronensis, Ceriodaphnia dubia, Daphnia mendotae, Daphnia pulicaria, Moinodaphnia minuta and Simocephalus congener. Daphnia pulicaria and Simocephalus congener are restricted to highland lakes. Daphnia mendotae was the only species collected in highly productive Lake Amatitlan. 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 Peten and Belize lowlands, and like Ceriodaphnia dubia, was absent in the Yucatan lowlands. The greatest numbers of cladoceran species were collected in the Mexican lowlands (n=41), followed by the Belizean lowlands (n=36), and the Guatemalan lowlands (n=25). Cladoceran communities in the lowlands were dominated by 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 (Loche), Dadaya macrops (Jamolun), Karualona karua (Cenote), Kurzia longirostris (Chacan-Bata) and Oxyurella ciliata (Cayucon).
Copepods: Only calanoid copepods were studied, and only six species belonging to the families Diaptomidae and Pseudodiaptomidae were identified (Table 4 b, Fig. 6). Copepod species found in highland lakes include Arctodiaptomus dorsalis, Leptodiaptomus siciloides and Prionodiaptomus colombiensis. Arctodiaptomus dorsalis was the only species collected in hypereutrophic Lake Amatitlan. Leptodiaptomus siciloides and P. colombiensis are rare species that live in the highlands and were collected in the oligotrophic Laguna de Ayarza and in Lake Guija. Arctodiaptomus dorsalis was widely distributed in the lowlands, but mostly dominated aquatic ecosystems in the Peten lowlands. Mastigodiaptomus nesus is restricted to the Belize and Yucatan lowlands, whereas Pseudodiaptomus marshi inhabits the Peten and Belize lowlands. Except for Mastigodiaptomus nesus, which was found in Cenote Juarez, no calanoid copepods were collected from "cenotes" and rivers.
Ostracodes: Partial results on ostracode distribution in the Yucatan Peninsula and surrounding areas were published by Perez et al. (2011b) and therefore only the most important results are presented here. Ostracoda was the group of microcrustaceans that displayed the highest number of families (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 ilosvayi, 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 denticulata inhabits aquatic ecosystems of the lowlands in Belize and Yucatan, whereas Physocypria globula is restricted to the Peten lowlands. Lowland rare species Cytherura sandbergi, Elpidium bromeliarum, Eucypris sp., and Physocypria xanabanica, were collected in Celestun, Rio 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 aquatic ecosystems: 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 as 33 species (cladocerans). Lowland waterbodies Crooked Tree Lagoon, Lake Peten Itza and Almond Hill Lagoon, followed by Lakes Yaxha, Macanche, San Jose Aguilar, Cayucon, San Francisco Mateos, Coba, Yalahau, Ocom, Nohbec, Milagros and Bacalar, yielded the highest overall species richness (up to S=77) on the Yucatan Peninsula and in surrounding areas.
Chironomids and ostracodes were present in all waterbody types (Fig. 7 a). Sampled rivers lacked diatoms and cladocerans. Copepods were scarce in rivers, "cenotes" and coastal waterbodies. The Jamolun wetland was dominated by chironomids and cladocerans. Cladocerans and ostracodes were present in all the highland lakes. Lakes Amatitlan, Gloria, Petexbatun, Celestun and Laguna Rosada displayed H values of 0 for chironomids, cladocerans and calanoid copepods. Ostracodes yielded H values >0, in TUM, a pond near Lake Oquevix, in the Subin river and in Laguna Rosada. Cenote San Ignacio Chochola displayed an H=0 for all 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 Yaxha and in the pond Belize 2, and 16 species were collected in Lakes Oquevix, Almond Hill Lagoon, Chacan-Bata, Bacalar and highland Guatemala Lake Atitlan (Fig. 7 a). Hypereutrophic Lake Amatitlan had a monospecific chironomid assemblage of Chironomus anthracinus. Dicrotendipes sp. was the only species collected in Lake Petexbatun, southern Peten. Highest diversity was reported in Lakes Oquevix (H=2.50) and Yaxha (H=2.54). Relatively low diversities (H [less than or equal to] 0.7) were determined in Cenotes Peten de Monos and Timul, Northern Yucatan Peninsula.
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 Peten Itza, Yaxha, Coba, Yalahau, Milagros, San Jose Aguilar, San Francisco Mateos, Cenote and Crooked Tree Lagoon. Among sampled ponds, only Belize 1 and 2 possessed diatoms. In oligotrophic Crater Lake Ayarza, no diatoms were found. High diatom diversities (H [greater than or equal to] 2.0) were determined in Lakes Yaxha, Macanche, Peten Itza, San Jose Aguilar, San Francisco Mateos, Coba, Yalahau, Milagros, Bacalar, Crooked Tree Lagoon, Cenote Xlacah and in coastal waterbody Celestun. In contrast, Lakes Atitlan, Rosario, Almond Hill Lagoon and Cenote Timul were characterized by low diversities (H<1.0).
Highest cladoceran species richness was found in Crooked Tree Lagoon (33), Almond Hill Lagoon (21), Lakes Peten Itza and Ocom, and in the Jamolun 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 ([less than or equal to] 10) were collected in Lakes Bacalar and Milagros in Eastern Yucatan and in Ixlu River, Northern Guatemala (Fig. 7 a). The largest and deepest lake, Peten Itza, possessed nine ostracode species. Only a few waterbodies on the Yucatan Peninsula lacked ostracodes: Chacan Lara, Sabanita and Silvituc. Ostracodes were abundant on the Yucatan Peninsula, especially in the lowlands of Peten (S [greater than or equal to] 5). Rivers were characterized by relatively high numbers of species (S=5-10). Ostracodes in "cenotes" and in the Jamolun wetland were not as abundant as in other aquatic ecosystems. Ostracodes were highly diverse in rivers, and lowland lakes (H [less than or equal to] 1.8). Ponds displayed low diversities (H [less than or equal to] 0.5) except for a pond near Lake Oquevix (TUM, H=1.0). Brackish waterbodies were characterized by diversity indices [less than or equal to] 1.29.
Copepods were less abundant and diverse than chironomids, diatoms, cladocerans and ostracodes. Few calanoid copepod species (S [less than or equal to] 2) were collected and were rarely found in rivers, "cenotes" or coastal waterbodies. Copepod diversity in the study area was [less than or equal to] 0.69. Highest diversities were reported in Lakes Bacalar and San Francisco Mateos, followed by Lakes Izabal (H=0.65), Crooked Tree Lagoon (H=0.60) and Almond Hill Lagoon (H=0.33).
Calibration of bioindicators on the Yucatan Peninsula: We assessed relationships between the various studied biological groups and environmental variables. Quantitative relations between chironomids, diatoms, cladocerans and ostracodes and environmental variables were assessed using a unimodal model with 14 explanatory variables, because gradient lengths were [greater than or equal to] 3 standard deviations (SDs). The first two axes in the DCA explained 17.7% of chironomid variability, 16.3% of diatom variability, 21.5% of cladoceran variability, and 27.8% of the ostracode species data. The sum of eigenvalues was 2.8 for chironomids, 4.3 for cladocerans, 6.1 for diatoms and 3.1 for ostracodes.
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. Forward-selected variables displayed low inflation factors (<5). Seven variables were related to chironomid (HC[O.sub.3], [delta][sup.13]C, pH, temperature, conductivity, dissolved oxygen, water depth) and diatom relative abundances (conductivity, [[delta]sup.18]O, dissolved oxygen, temperature, pH, [delta][sup.13]C, water depth), four to cladoceran (conductivity, HC[O.sub.3], temperature, dissolved oxygen) and six to ostracode abundances (conductivity, HC[O.sub.3], 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 (HC[O.sub.3], Cl, Na, temperature, water depth, [delta][sup.18]O) were included in the final RDA. In the final CCAs and RDA, HC[O.sub.3] was the main factor controlling chironomid and copepod assemblages on the Yucatan Peninsula (Fig. 8). Diatom, cladoceran and ostracode communities are more influenced by conductivity. [delta][sup.13][C.sub.DIC], a lake productivity proxy, and lakewater [delta][sup.18]O, 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 chi-ronomids explained 4.8% ([lambda]1=0.14, [lambda]2=0.11), 6.8% for diatoms ([lambda]1=0.42, [lambda]2=0.33), 6.4% for cladocerans ([lambda]1=0.27, [lambda]2=0.15), 9.9% for ostracodes ([lambda]1=0.31, [lambda]2=0.13) of the variability in species data, and the final RDA for copepods explained 24.9% ([lambda]1=0.25, [lambda]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 Yucatan Peninsula, Belize, and the central and Eastern areas of the Peten 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 Atitlan. 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 biplot was mainly collected in "cenotes," Lake Oquevix, Rio Dulce and Loche pond. Chironomus anthracinus, located in the lower right quadrant, was the only species present in hypereutrophic Lake Amatitlan. Labrundina sp., Beardius sp. and Paratanytarsus sp.1 were widely distributed in the lowlands of the Yucatan 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 cladocerans indicates that water conductivity influences species distribution on the Yucatan Peninsula (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 000LiS/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[degrees]C) with lower conductivities (<350[micro]S/cm) such as Oquevix, Crooked Tree Lagoon and Cayucon. The dominant cladocerans in highland Lakes Atitlan, Amatitlan, Ayarza and Guija 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 Jamolun wetland. Daphnia mendotae was the only species identified in surface sediments from Lake Amatitlan.
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, and was absent in "cenotes" and coastal waterbodies. Mastigodiaptomus nesus, in the lower right quadrant, is typical of HCO3rich waters (125-710mg/L), such as San Jose Aguilar, Loche, Juarez, Coba, 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 Lagoons Progreso and Almond Hill, Belize. This species was also collected in waterbodies displaying slightly higher conductivities, such as Bacalar and Lagoons Progreso and Almond Hill.
The CCA biplot for ostracodes suggests that conductivity, followed by HC[O.sub.3], are the main factors controlling species distribution (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 (750[micro]S/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 Amatitlan include Candona sp., Cypridopsis vidua and Darwinula stevensoni. Ostracodes displaying high abundances in highland and lowland lakes included Cypridopsis okeechobei, Cytheridella ilosvayi and Darwinula stevensoni. Potamocypris sp., in the upper left quadrant, was collected in Lakes Rosario, Yalahau, Loche pond and Cenote Timul, suggesting its preference for warm waters (up to 32[degrees]C) and waters with HC[O.sub.3] concentrations as high as 707mg/L.
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 in each lake, and quantitative ecological information. CCA ordination biplots, relating bioindicator species and forward selected variables, distinguish between taxa typical of highland vs. lowland lakes, brackish vs. fresh waters, alkaline vs. acidic waters, and lakes of different trophic states. Most bioindicator species live at low elevations (<450m.a.s.l.), with fewer species and individuals in highland lakes. In general, diatom, cladoceran and ostracode communities are most affected by conductivity, reflecting lake water chemical composition, marine influence (Perry et al. 1995) and the N-S precipitation gradient in the Yucatan Peninsula. Species of these taxonomic groups presented characteristic faunas of fresh and brackish waters. Bicarbonate controls chironomid and copepod distribution in the study area. Concentration of bicarbonate in lake waters is an important variable in the study area because most of the studied lakes lie in karst terrain. Another related factor could be the greater abundance of edible algae in hard water lakes (Ghadouani et al. 1998). The second determinant variable for chironomid distribution was [delta][sup.13][C.sub.DIC], 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 Yucatan Peninsula are highly sensitive to changes in water column conductivity, alkalinity and trophic state.
Sanchez et al. (2002) identified 75 diatom species in "cenotes" and anchialine caves on the Eastern Yucatan Peninsula. Similar to our findings, they reported that pennate diatoms were the dominant group. Few diatoms were of marine origin. Similar results were also found in aquatic ecosystems of Costa Rica (Haberyan 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 and Bacillariaceae were hydrochemically tolerant and displayed wide distributions: Brachysira procera, Encyonema densistriata, Mastogloia smithii, Denticula kuetzingii, Cyclotella meneghiniana and Nitzschia amphibia. Nitzschia amphibia tolerates broad trophic state and conductivity ranges. Cyclotella meneghiniana and Discostella aff. pseudostelligera dominated the hypereutrophic waters of Lake Amatitlan, 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. Highland and lowland lakes differ in their bioindicator communities, as some species are highly sensitive and restricted to specific areas. 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 Atitlan, a lake that experienced extensive cyanobacteria (Lyngbya hieronymusii/birgei/robusta) blooms in October 2009 (Rejmankova et al. 2011). When we visited Lake Atitlan 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) reported 84 chironomid taxa, mainly morphospecies, from 18 lakes on the Yucatan Peninsula. In their study, the dominant chironomid species were 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 & MacDonald 2003), which characterize many lowland and some highland lakes in the study area. For instance, C. anthracinus was the only dipteran species collected in hypereutrophic Lake Amatitlan, Guatemala. For decades, this highly productive lake has received wastewater, delivered by its main inflow river, the Rio Villalobos. This species was also collected in Cenote Timul, which displayed high [delta][sup.13][C.sub.DIC] values of +13.6%o (Perez 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). Cladocerans and copepods are the two taxonomic groups most studied on the Yucatan Peninsula and in surrounding areas (Elias-Gutierrez et al. 2008). Mexico has been actively involved in studying the systematics of Cladocera (Elias-Gutierrez et al. 2006). Therefore, identification of collected cladocerans and copepods to species level was possible. Elias-Gutierrez (2006) reported a total of 162 cladoceran species for two regions of Mexico (Morelos and southeast Mexico), four being endemic species of Southeast Mexico. Some of the cladoceran species we collected are widely distributed in the Northern Neotropics and South America. These include Diaphanosoma brevireme, Pseudosida ramosa, Macrothrix spinosa, M. elegans, Chydorus nitidilus, Ephemeroporus tridentatus, Alona ossiani, Oxyurella ciliata and O. longicaudis (Elias-Gutierrez 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 Loche, 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 Atitlan still display oligo-mesotrophic conditions. Macrophytes, the typical habitat of cladocerans, are scarce in these lakes. In contrast, Lake Amatitlan is hypereutrophic, and only a single cladoceran species, 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, Illyova & Nemethova 2005, Marrone et al. 2005). For instance, D. pulicaria seems to prefer cool waters, typical of highland Lake Atitlan ([less than or equal to] 21.8[degrees]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 (Elias-Gutierrez 2006). Mainly cladoceran carapaces were collected in "cenotes" and rivers, but there were few live specimens. Most "cenotes" we sampled lacked aquatic vegetation, the main habitat of most cladoceran species. Distribution of zooplankton in rivers is very heterogenous (Vadadi-Fulop 2009) and we might simply have collected samples from sites where densities were low. Scarcity of cladocerans in rivers, however, is common because they are not as well adapted to lotic aquatic environments as ostracodes and chironomid larvae. Another explanation for the low species richness and numbers could be that adults of some species are more typical of the rainy season, and we collected surface sediments in the dry season. Future sampling should be conducted across the seasons.
Only six calanoid copepod species were collected from the sampled waterbodies. Recent studies in Mexico (Elias-Gutierrez et al. 2008, Brandorff 2012) report up to 100 freshwater copepod species, of which 20 species belong to the order Calanoida. SuarezMorales & Reid (2003) suggest that the fauna of the Yucatan Peninsula has affinities with Cuba and the insular Caribbean, and differs from that of Central Mexico, which is closer to the fauna of upper Central America. 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 (Elias-Gutierrez et al. 2008). 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 Amatitlan in the highlands, and meso-oligotrophic, karst Lake Peten Itza in the lowlands. According to Suarez-Morales (2003), this nearctic species is the most widespread diaptomid in the Yucatan 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 Yucatan Peninsula during past marine regressions, during times of emergence of areas on the peninsula. This could explain why this species is now highly tolerant and widely distributed.
Of the six copepod species found, M. reidae is endemic to Campeche (Elias-Gutierrez et al. 2008, Suarez-Morales & Elias-Gutierrez 2000) and Northern Guatemala (this study). All species belonging to the genus Mastigodiaptomus found in the Yucatan Peninsula are neotropical. Suarez-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 Chicana pond, near the Biosphere Reserve of Calakmul, Yucatan Peninsula, and probably speciated for ecological reasons. Our results indicate that M. nesus inhabits waterbodies in Belize, Campeche, Quintana Roo and Yucatan, as reported by Elias-Gutierrez et al. (2008). The present distribution of this taxon could be a remnant of the original Mastigodiaptomus fauna in the Yucatan Peninsula and may reflect recent, post-Pliocene dispersal and Holocene climatic fluctuations (Suarez-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 Yucatan (Bacalar). Pseudodiaptomid copepods mainly inhabit marine and brackish water environments, although recent studies (Suarez-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 this copepod species in freshwater Lake Izabal supports the idea that is starting to colonize freshwater environments. Lake Izabal is connected with the Caribbean Sea via the Rio Dulce and El Golfete. Similar to cladocerans, few copepods were found in rivers, probably because they are not well adapted to inhabit running waters, avoiding such environments and preferring the littoral zones of lakes (Casanova & Henry 2004).
Effects of altitude and related variables precipitation and trophic state, on ostracode 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 Perez et al. (2010b, 2010c, 2011b), Darwinula stevensoni has a worldwide distribution and Cytheridella ilosvayi is abundant throughout the entire continental Neotropics. Cypridopsis okeechobei displays a narrower distribution, extending from the United States to the Peten Lake District, Northern Guatemala. Pseudocandona sp. was also abundant and we suggest this species is endemic to the Yucatan Peninsula, but further taxonomic and molecular analysis is needed to test this assertion. We were unable to identify some ostracodes collected in the highlands to species level. They may be endemic to the region or be distributed throughout higher-elevation areas of Central America and Mexico that have not been studied yet. These species include Candona sp., Limnocythere sp. and Trajancypris sp. A conductivity gradient is well marked on the Yucatan 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, Macanche, and a pond near Lake Oquevix in Peten, Guatemala and in San Jose Aguilar, Mexico.
A broad trophic state gradient characterizes the study area, ranging from hypereutrophic Lake Amatitlan to oligotrophic Laguna Ayarza. Hypereutrophic Lake Amatitlan 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 Yucatan Peninsula and surrounding areas (Guatemala and Belize) are rich in aquatic ecosystems, therefore it will be important to collect samples from additional sites to expand our training set. Aquatic bio-indicators should also be collected at different seasons to provide information on species life cycles. Despite the utility of the collected data, additional sampling campaigns in aquatic ecosystems throughout Mexico, Guatemala, Belize and Central America are required. We also recommend return visits to previously studied ecosystems to capture seasonal variability. Central Mexico is rich in aquatic ecosystems and there have been few studies on bioindicators in that region. We are developing a calibration dataset for central Mexico that will provide new autecological information for bioindicators that will expand our original Yucatan training set.
Importance of species richness and diversity of bioindicators in neotropical aquatic ecosystems: 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 Yucatan 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[less than or equal to]2.4, diatoms). The lagoon is protected and recognized as a wetland of international importance under the Ramsar Convention of Wetlands (http://www.ramsar.wetlands.org). Lakes Bacalar and Chichancanab, on the Yucatan Peninsula, were declared protected areas in April 2011 (SIPSE 2011). Most aquatic ecosystems in the study area, however, lack such environmental protection. Government agencies, universities and NGOs should collaborate to guarantee that aquatic ecosystems in the region are protected. Highland lakes, despite their lower diversities, deserve special attention because they often possess rare or unidentified taxa and may be home to new or endemic species. Chironomids and ostracodes were highly diverse (H[less than or equal to]2.54) in sampled aquatic ecosystems. Lakes Chacan Lara, Sabanita and Silvituc were small waterbodies that lacked ostracodes, probably due to low lake water conductivities ([less than or equal to]183LiS/cm). Diatoms, cladocerans and copepods were scarce or lacking in rivers, "cenotes" and coastal waterbodies. Further sampling campaigns are needed to corroborate these observations and improve on methods for collection of bioindicators that were present in low abundances. Rivers deserve special attention because they frequently receive domestic and industrial waste, affecting species distributions and diversity.
This study on the waterbodies on and around the Yucatan 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 chironomids, diatoms, ostracodes, cladocerans and copepods in the region and is a pre-requisite for future quantitative paleolimnological reconstruction of late Quaternary environments in the Northern Neotropics. Our results highlight the exceptional potential of the studied taxonomic groups as bioindicators of climate and trophic state.
Analysis of the distribution and ecological preferences of the five studied groups (diatoms, chironomids, cladocerans, copepods and ostracodes) generated new information that is required to make better use of these aquatic bioindicators in the neotropical region. Clear differences emerged in the chemistry and biology of highland versus lowland water bodies. Volcanic highland lakes display origin and water chemical composition different from those of karst lowland lakes. Biodiversity in the highlands is lower than in the lowlands. The highland aquatic fauna is dominated by chironomids Apsectrotanypus sp., Cricotopus spp., Tanytarsini C, Stenochironomus sp., diatoms Ulnaria acus, cladocerans Ceriodaphnia dubia and Bosmina 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 species inhabiting highly productive waters and tolerating extreme conditions include 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 Yucatan 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 utility of the collected data, additional sampling campaigns in aquatic ecosystems throughout Mexico, Guatemala, Belize and other parts of Central America are required. We also recommend return visits to previously studied ecosystems to capture seasonal variability.
We are grateful to the agencies and people who helped us with field and laboratory work, including the University of Belize, Forestry and Fisheries Departments (Belize), Universidad del Valle de Guatemala, CONAP, AMSCLAE, AMPI, FINABECE, Trifinio (Guatemala), SRE, CONAPESCA, ECOSUR-Chetumal (Mexico),
Institut fur Geosysteme und Bioindikation (Germany), TU-Braunschweig (Germany), Dietmar Keyser, Dustin Grzesik, Jason Curtis, David Klassen, Jose Harders, Carmen Herold, Bessie Oliva, Roberto Moreno, Eleonor de Tott, Margaret Dix, Margarita Palmieri, Alma Quilo, Gabriela Alfaro, Jacobo Blijdenstein, Melisa Orozco, Silja Ramirez, Wolfgang Riss, Evgenia Vinogradova, Luis Toruno, Mario Cruz, Rita Bugja, Luciana Mitsue, Susanne Krueger, Javier Perez y Perez, and Carolina Alvarado de Perez. Special thanks to anonymous reviewers for detailed suggestions and comments. We 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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Liseth Perez * (1,2), Julia Lorenschat (1), Julieta Massaferro (3), Christine Pailles (4), Florence Sylvestre (4), Werner Hollwedel (5), Gerd-Oltmann Brandorff (6), Mark Brenner (7), Gerald Islebe (8), Maria del Socorro Lozano (2), Burkhard Scharf (1) & Antje Schwalb (1)
(1.) Institut fur Geosysteme und Bioindikation, Technische Universitat Braunschweig, Langer Kamp 19c, 38106 Braunschweig, Germany; firstname.lastname@example.org, email@example.com, firstname.lastname@example.org, email@example.com
(2.) Instituto de Geologia, Universidad Nacional Autonoma de Mexico (UNAM), Ciudad Universitaria, 04510, Distrito Federal, Mexico; firstname.lastname@example.org, email@example.com
(3.) CENAC-APN, CONICET, San Martin 24, 8400, Bariloche, Argentina; firstname.lastname@example.org
(4.) CEREGE, Universite Aix-Marseille, CNRS, IRD, Europole mediterraneen de l'Arbois, BP 80, 13545 Aix-enProvence cedex 4, France; email@example.com, firstname.lastname@example.org
(5.) Oldenburger Strasse 16A, 26316, Varel, Germany; email@example.com
(6.) Georg-Groning-Str. 29A, 28209, Bremen, Germany; firstname.lastname@example.org
(7.) Department of Geological Sciences & Land Use and Environmental Change Institute, University of Florida, Gainesville, 32611, Florida, USA; email@example.com
(8.) Herbario, El Colegio de la Frontera Sur (ECOSUR), Unidad Chetumal, Av. del Centenario 424, 77000, Chetumal, Quintana Roo, Mexico; firstname.lastname@example.org
* Corresponding author
Received 29-V-2012. Corrected 02-IX-2012. Accepted 04-X-2012.
TABLE 1A Location, morphometry and selected limnological variables of surface waters (single measurements) for sampled waterbodies on the Yucatan Peninsula (modified from Perez et al. 2011b). ID indicates the abbreviations used for the studied waterbodies in figures 3-7. ID-Nr. indicates the location of all sampled aquatic ecosystems across a NW-S precipitation gradient in figure 1 Area ID ID- Name of Nr. aquatic ecosystem Guatemalan AMA 19 Amatitlan Highlands ATI 20 Atitlan AYA 23 Ayarza GUI 21 Guija ATE 22 Atescatempa Guatemalan IZA 1 Izabal Eastern Lowlands Peten OQU 25 Oquevix Lowlands SAL 26 Salpeten MAC 4 Macanche YAX 5 Yaxha ITZ 2 Peten Itza SAC 28 Sacpuy PER 3 Perdida GLO 29 La Gloria DIE 30 San Diego POZ 32 Las Pozas PET 33 Petexbatun ROS 34 El Rosario Yucatan MIL 12 Milagros Lowlands BAC 13 Bacalar NOH 14 Nohbec OCO 15 Ocom CHI 16 Chichancanab PUN 17 Punta Laguna JOS 36 San Jose Aguilar SAB 37 Sabanita BAT 38 Chacan-Bata LAR 39 Chacan-Lara JOB 41 Jobal FRA 42 San Francisco Mateos MIS 43 La Misteriosa CAY 45 Cayucon YAL 18 Yalahau COBA 61 Coba Belizean ALM 8 Almond Hill Lowlands Lagoon CRO 9 Crooked Tree Lagoon HON 10 Honey Camp Lagoon Area Coordinates Altitude NW [m.a.s.l] Guatemalan 14[degrees]26'03.7" 90[degrees]32'58.6" 1200 Highlands 14[degrees]42'34.8" 90[degrees]15'59.4" 1560 14[degrees]25'39.3" 90[degrees]08'11.6" 1414 14[degrees]15'43.7" 89[degrees]32'11.3" 433 14[degrees]13'01.1" 89[degrees]41'39.2" 587 Guatemalan 15[degrees]29'24.5" 89[degrees] 8'32.7" 4 Eastern Lowlands Peten 16[degrees]39'14.2" 89[degrees]44'26.1" 148 Lowlands 16[degrees]58'38.2" 89[degrees]40'30.9" 114 16[degrees]57'60.0" 89[degrees]38'06.5" 165 17[degrees]03'48.9" 89[degrees]24'27.1" 219 17[degrees]00'02.0" 89[degrees]51'16.4" 115 16[degrees]58'46.4" 90[degrees]00'52.2" 122 17[degrees]04'00.7" 90[degrees]12'41.7" 75 16[degrees]57'07.5" 90[degrees]22'36.1" 132 16[degrees]55'59.5" 90[degrees]24'54.5" 134 16[degrees]21'02.4" 90[degrees]10'28.9" 146 16[degrees]26'11.8" 90[degrees]11'46.0" 115 16[degrees]31'31.4" 90[degrees]09'36.2" 117 Yucatan 18[degrees]30'41.5" 88[degrees]25'35.8" 1 Lowlands 18[degrees]39'54.0" 88[degrees]23'27.0" 1 19[degrees]08'8.54" 88[degrees]10'46.6" 1 19[degrees]28'28.6" 88[degrees]03'17.9" 1 19[degrees]52'43.2" 88[degrees]46'06.5" 2 20[degrees]39'00.6" 87[degrees]38'28.2" 3 18[degrees]22'04.5" 89[degrees]00'41.2" 107 18[degrees]24'03.2" 88[degrees]34'20.6" 38 18[degrees]28'42.1" 89[degrees]05'13.9" 91 19[degrees]11'21.8" 88[degrees]10'17.0" 90 18[degrees]41'40.7" 90[degrees]06'45.4" 74 17[degrees]53'55.9" 90[degrees]39'22.8" 52 18[degrees]02'40.3" 90[degrees]29'14.0" 57 18[degrees]02'34.3" 90[degrees]58'33.0" 69 20[degrees]39'25.9" 89[degrees]13'02.0" 2 20[degrees]29'40.2" 87[degrees]44'19.2" 7 Belizean 17[degrees]27'49.0" 88[degrees]18'31.6" 1 Lowlands 17[degrees]46'42.8" 88[degrees]31'37.4" 2 18[degrees]02'44.5" 88[degrees]26'20.5" 1 Area Depth * Surface Temp. Diss. pH [m] area [[degrees]C] oxygen [[km.sup.2]] [mg/L] Guatemalan 23 15.2 22.8 18.7 9.3 Highlands 340 126 21.8 7.3 8.4 250 14 21.6 7.2 8.4 21.5 45 26.2 7.7 8.4 2 1.1 27.3 6.7 8.0 Guatemalan 14.8 645 26.4 7.6 8.3 Eastern Lowlands Peten 10 1.6 31.4 6.9 7.7 Lowlands 38 2.9 29.7 8.4 8.2 80 2.5 26.8 5.0 8.0 22 7 29.0 7.3 8.7 165 100 27.6 8.9 8.5 6 3.5 28.8 8.0 8.4 4 11 28.8 9.8 8.8 65 3.6 29.2 8.8 8.6 8.1 3.8 28.6 8.2 8.6 35 2.0 29.8 9.0 8.4 40 5.6 30.9 9.7 8.0 3 0.02 28.3 7.6 7.1 Yucatan 4 3.1 27.9 12.4 8.1 Lowlands 16 51 27.0 7.9 7.8 0.6 8.5 29.2 9.4 8.5 10 0.25 27.9 7.2 8.0 14 5.1 28.5 7.7 8.0 20 0.9 26.8 7.2 8.0 3 2.0 - 4.8 8.0 2.5 0.02 27.5 8.1 8.0 -- 2.9 26.3 2.2 7.0 3 1.2 28.1 6.0 7.5 3 31.7 10.9 8.3 5 0.1 24.8 0.9 7.3 5.8 5.0 26.7 7.7 8.0 8 2.0 25.3 3.3 7.4 11 0.25 28.8 8.7 8.9 -- 0.35 28.9 8.7 8.5 Belizean 1.9 1.5 27.5 6.4 7.1 Lowlands 3.3 23 28.5 6.9 7.8 8 3.9 25.9 9.1 8.5 Area Cond. Secchi [[micro] [m] S/cm] Guatemalan 630 0.1-0.8 Highlands 465 6.6 1772 11.4 206 1.4 283 0.1 Guatemalan 215 -- Eastern Lowlands Peten 238 0.4 Lowlands 4310 0.8 850 -- 232 1.8 533 7.5 285 0.5 232 0.7 187 0.6 179 0.6 292 1.8 568 0.6 1019 -- Yucatan 2720 1.0 Lowlands 1221 10.3 1231 0.6 774 5.5 2060 2.8 754 4.7 488 0.6 139 0.5 146 -- 174 0.7 241 -- 474 -- 1411 2.1 127 ? 2350 1.1 1213 0.9 Belizean 1715 1.7 Lowlands 330 2.0 1481 1.8 * Maximum sampled water depth and/or maximum lake depth. TABLE 1B Location, morphometry and selected limnological variables of surface waters (single measurements) for sampled "cenotes" (sinkholes), coastal waterbodies, rivers, wetlands and ponds on the Yucatan Peninsula (modified from Perez et al. 2011b). ID indicates the abbreviations used for the studied waterbodies in figures 3-7. ID-Nr. indicates the location of all sampled aquatic ecosystems across a NW-S precipitation gradient in figure 1 Type of ID ID-Nr. Name aquatic ecosystem Cenotes XLA 50 Xlacah MON 52 Peten de Monos IGN 55 San Ignacio Chochola CHE 56 Chenha TIM 57 Timul YOK 58 Yokdzonot JUA 60 Juarez YAA 63 Ya'ax'ex KAN 54 San Francisco Kana TEK 62 Tekom Coastal PRO 35 Progreso water bodies CEN 11 Cenote Little Belize ROSA 49 Rosada CEL 51 Celestun Rivers SUB 31 Subin IXL 27 Ixlu DUL 24 Rio Dulce CUB 44 Cuba CAN 46 Candelaria GUE 47 Guerrero Wetland JAM 48 Jamolun Ponds TUM 53 Near Oquevix LOC 59 Loche SIL 40 Silvituc BZ1 6 Belize 1 BZ2 7 Belize 2 Type of Coordinates Altitude aquatic N W [m.a.s.l] ecosystem Cenotes 21[degrees]05'27.6" 89[degrees]35'53.3" 6 20[degrees]50'59.6" 90[degrees]19'13.8" 25 20[degrees]45'00.9" 89[degrees]50'03.2" 7 20[degrees]41'23.0" 89[degrees]52'34.5" 3 20[degrees]35'38.8" 89[degrees]21'23.7" 9 20[degrees]42'24.6" 88[degrees]43'52.0" 13 20[degrees]48'09.6" 87[degrees]20'23.8" 14 20[degrees]37'15.4" 88[degrees]24'56.0" 27 20[degrees]51'22.2" 90[degrees]07'04.5" 3 20[degrees]36'08.1" 88[degrees]15'52.5" 18 Coastal 18[degrees]13'05.2" 88[degrees]24'35.2" 5 water bodies 18[degrees]13'36.9" 88[degrees]22'55.57" 7 21[degrees]20'11.3" 89[degrees]18'01.9" 4 20[degrees]51'20.8" 90[degrees]22'39.2" 14 Rivers 16[degrees]38'11.6" 90[degrees]11'00.3" 141 16[degrees]58'27.3" 89[degrees]53'27.8" 110 15[degrees]40'25.3" 88[degrees]57'49.3'' 4 17[degrees]56'55.4" 90[degrees]28'39.1" 80 18[degrees]11'02.4" 91[degrees]02'59.6" 44 19[degrees]12'41.6" 90[degrees]43'47.6" 5 Wetland 19[degrees]27'58.3" 89[degrees]29'45.1" 115 Ponds 16[degrees]40'31.7" 89[degrees]44'18.1" 179 21[degrees]25'04.3" 88[degrees]08'30.8" 20 18[degrees]38'23.2" 90[degrees]17'35.2" 59 17[degrees]14'33.5" 88[degrees]58'19.7" 77 17[degrees]18'17.9" 88[degrees]29'18.9" 33 Type of Depth * Surface Temp. Diss. oxygen aquatic [m] area [[degrees]C] [mg/L] ecosystem [[km.sup.2]] Cenotes 45 <0.01 27.9 4.0 1.5 <0.01 26.6 1.4 4 <0.01 27.4 2.7 2 <0.01 28.3 10.4 - 0.03 30.4 11.4 45 <0.01 25.2 5.3 25 0.03 27.9 8.7 47 <0.01 26.4 10.6 - 0.01 30.7 9.7 1.5 <0.01 25.5 6.7 Coastal 3.2 7.2 26.4 7.0 water bodies 11.1 0.06 25.8 8.3 0.5 2.3 28.1 10.5 1.5 28 24.9 5.2 Rivers 1 -- 26.2 4.2 1 -- 25.9 6.7 7 -- 27.6 6.5 0.5 -- 24.9 7.3 1.5 -- 26.9 1.9 1 -- 26.2 3.6 Wetland 1.5 -- 25.7 2.9 Ponds 1 <0.01 25.9 9.4 1 <0.01 32.0 14.4 2.5 <0.01 30.2 7.7 1.5 <0.01 28.2 5.8 1 <0.01 27.4 7.5 Type of pH Cond. Secchi aquatic [mS/cm] [m] ecosystem Cenotes 7.0 1452 5 6.9 3670 1.5 6.9 2110 4 7.6 2520 3.5 9.1 1465 0.2 7.4 949 7 8.1 643 1.6 8.0 793 0.8 8.2 1751 0.3 7.3 958 1.5 Coastal 8.2 2040 1.3 water bodies 8.2 5960 5.5 8.7 55300 0.5 7.8 38200 0.5 Rivers 7.4 720 0.5 7.5 1025 1 7.6 192 0.5 7.8 2040 0.5 7.7 1564 1.0 7.7 2700 0.5 Wetland 7.3 2520 0.5 Ponds 9.3 168 -- 9.4 4340 0.2 8.2 183.2 -- 7.3 192 -- 8.0 244 -- * Maximum sampled water depth and/or maximum lake depth. TABLE 2 Chironomids (family Chironomidae; n=66) found in aquatic ecosystems in the Northern Neotropics. Species are ordered alphabetically within subfamilies and tribes. Species codes in bold (n=38) were taxa included in multivariate analysis. Code indicates the species abbreviations used in Figures 3a,b,c and 8. A number or letter was designated along with the genus to identify different morphospecies. For the ecosystem studies see tables 1A, B Taxa Code Subfamily Chironominae Tribe Chironomini Apedilum sp. APED Axarus sp. AXAR Beardius sp. BEAR Brundinella sp. BRUN Chironomus anthracinus Zetterstedt 1860 CHAN Chironomus plumosus Linnaeus 1758 CHPL Cladopelma sp. CLAD Corynocera ambigua Zetterstedt 1838 CORC Corynocera olivieri type CORO Cryptochironomus sp. CRYP Dicrotendipes sp. DICR Einfeldia sp. EINF Endochironomus sp. ENDO Endotribelos sp. ENTR Glyptotendipes sp.1 GLEN Glyptotendipes sp.2 GLYP Goeldochironomus sp. GOEL Harrisius sp. HARR Kiefferulus sp. KIEF Lauternborniella sp. LAUT Paracladopelma sp. PCLA Paratendipes sp. PART Parachironomus sp. PCHI Phaenopsectra sp. PHAE Polypedilum sp. POLY Polypedilum sp.2 PO16 Sergentia sp. SERG Stempellina sp. STEM Saetheria sp. SAET Stenochironomus sp. STEN Sublettea sp. SUBL Xenochironomus sp. XENO Tribe Tanytarsini Cladotanytarsus sp.1 CLA1 Cladotanytarsus sp.2 CLA2 Micropsectra sp. MICR Tanytarsini A TANA Tanytarsini C TANC Tanytarsini D TAND Tanytarsini F TANF Tanytarsini J TANJ Tanytarsini K TANK Paratanytarsus sp.1 PAR1 Paratanytarsus sp.2 PAR2 Tribe Pseudochironomini Pseudochironomus sp. PSEU Subfamily Orthocladiinae Corynoneura sp. CORY Cricotopus spp. CRIC Eukiefferiella sp. EUKI Limnophies sp. LIMN Mesosmittia sp. MESS Parakiefferiella fennica Tuiskunen 1986 PAFE Parapsectrocladius sp. PAPS Pseudosmittia sp. PSSM Psectrocladius sp. PSEC Subfamily Tanypodinae Ablabesmya sp. ABLA Alotanypus sp. ALOT Apsectrotanypus sp. APSE Coelotanypus/Clinotanypus COEL Djalmabatista sp. DJAL Fittkauimyia sp. FITT Labrundina sp. LABR Larsia sp. LARS Macropelopia/Apsectrotanypus MACR Monopelopia sp. MONO Procladius sp. PROC Tanypodinae indet. TAID Zavrelymia sp. ZAVR TABLE 3 Diatom species (n=282) found in aquatic ecosystems in the Northern Neotropics. Species are ordered alphabetically within classes, orders, suborders and families. Species codes in bold (n=97) were included in multivariate analysis Code indicates the species abbreviations used in figures 4a,b and 8. A number was designated along with the genus to identify different morphospecies. For the ecosystem studies see tables 1a,b Taxa Code Class Bacillariophyceae Order Centrales Sub-Order Coscinodiscineae Hemidiscaceae Actinocyclus sp. ACTI Melosiraceae Hyalodiscus scoticus (Kutzing) Grunow 1879 HYSC Paraliaceae Paralia sulcata (Ehrenberg) Cleve 1873 PARA Thalassiosiraceae Aulacoseira ambigua (Grunow) Simonsen 1979 MA Aulacoseira crenulata (Ehrenberg) Thwaites 1848 AUC Aulacoseira distans (Ehrenberg) Simonsen 1979 MD Aulacoseira granulata (Ehrenberg) Simonsen 1979 MG Aulacoseira granulata var. angustissima (Otto Muller) MGA Simonsen 1979 Aulacoseira granulata f. curvata (Hustedt) MGC Simonsen 1979 Cyclotella atomus Hustedt 1937 CYAT Cyclotella caspia Grunow 1878 CCAS Cyclotella comensis Grunow in Van Heurck 1882 CYCO Cyclotella cyclopuncta Hakansson & Carter 1990 CYCL Cyclotella meneghiniana Kutzing 1844 CYMG Cyclotella striata (Kutzing) Grunow in Cleve CYST & Grunow 1880 Cyclotella aff. petensis CYEN Cyclotella aff. striata CAST Cyclotella sp. CPS Cyclotella sp. 22 CP22 Discostella pseudostelligera (Hustedt) CCP Houk & Klee 2004 Discostella aff. pseudostelligera CYAP Discostella stelligera (Cleve et Grunow) CYCS Houk & Klee 2004 Stephanodiscus hantzschii Grunow in Cleve STHA & Grunow 1880 Stephanodiscus minutulus (Kutzing) Cleve STME & Moller 1882 Stephanodiscus medius H. Hakansson 1986 STNU Stephanodiscus parvus Stoermer & Hakansson 1984 STPA Thalassiosira sp. THAS Sub-Order Rhizosoleniineae Biddulphiaceae Terpsinoe musica Ehrenberg 1843 TERM Order Pennales Sub-Order Araphidineae Fragilariaceae Campylostylus normannianus (Greville) Gerloff, CAPS Natour & Rivera 1978 Cymatosira lorenziana Grunow 1862 CLOZ Fragilaria bidens Heiberg 1863 FRBI Fragilaria capucina Desmazieres emend Lange- FCA Bertalot 1980 Fragilaria capucina var. vaucheriae (Kutzing) Lange- FCAV Bertalot 1980 Fragilaria crotonensis Kitton 1869 FCR Fragilaria famelica (Kutzing) Lange-Bertalot 1980 FF Fragilaria tenera (W. Smith) Lange-Bertalot 1980 FT Fragilaria ulna var. goulardi (Brebisson) Lange- FRGO Bertalot 1980 Opephora marina (Gregory) Petit 1888 OMAR Pseudostaurosira brevistriata (Grunow in Van Heurck) FBR Williams & Round 1987 Staurosira construens Ehrenberg 1843 FRAC Staurosirella pinnata (Ehrenberg) FP Williams & Round 1987 Synedra hartii Cholnoky 1963 FHA Tabularia tabulata (C.A.Agradh) TABA Snoeijs 1992 Tabularia fasciculata (C.A.Agradh) TAFA Williams & Round 1986 Ulnaria acus (Kutzing) Aboal in Aboal, SYNA Alvarez-Cobelas, Cambra & Ector 2003 Ulnaria delicatissima var. angustissima FAAU (Grunow in Van Heurck) Aboal in Aboal, Alvarez Cobelas, Cambra & Ector 2003 Ulnaria delicatissima var. angustissima FARD (Grunow in Van Heurck) Aboal in Aboal, Alvarez-Cobelas, Cambra & Ector 2003 Ulnaria ulna (Nitzsch) Compere 2001 SYNU Sub-Order Raphidineae Eunotiaceae Eunotia camelus Ehrenberg 1841 EUCM Eunotia bilunaris (Ehrenberg) Mills 1933-1935 EUL Eunotia monodon Ehrenberg 1841(1843) EUMO Eunotia praerupta Ehrenberg 1841(1843) EUPR Eunotia sp. EUSP Peronia fibula (Brebisson in Kutzing) Ross 1956 PERF Achnanthaceae Achnanthes minutissima var. scotica (Carter) AMSC Lange-Bertalot in Lange-Bertalot & Krammer 1989 Achnanthidium brevipes (Agardh) Heiberg 1863 ABR Achnanthidium exiguum (Grunow) Czarnecki 1994 AEX Achnanthidium hungaricum Grunow 1863 AHU Achnanthidium minutissimum (Kutzing) AMI Czarnecki 1994 Cocconeis neodiminuta Krammer 1990 CD Cocconeis placentula Ehrenberg 1838 CP Karayevia submarina (Hustedt) Bukhtiyarova 2006 ASUB Psammothidium marginulatum (Grunow) AUM Bukhtiyarova et Round 1996 Naviculaceae Amphipleura pellucida (Kutzing) Kutzing 1844 APLL Amphora arenaria Donkin 1858 AMRE Amphora arenicola Grunow in Cleve 1895 AMER Amphora copulata (Kutzing) Schoeman AMPU & Archibald 1986 Amphora cymbifera Gregory 1857 AMCY Amphora graeffeana Hendey 1973 AMGR Amphora granulata Gregory 1857 APTA Amphora holsaticoides Nagumo & Kobayasi 1990 AMHS Amphora lybica Ehrenberg 1840 AY Amphora marina W. Smith 1857 AMAR Amphora pediculus (Kutzing) AMPE Grunow in Schmidt et al. 1875 Amphora proteus Gregory 1857 AMP Amphora securicula Peragallo & Peragallo 1899 AMSE Anomoeoneis sphaerophora Pfitzer 1871 ANS Anomoeoneis sphaerophora f. costata (Kutzing) ANSC A.-M. Schmid 1977 Anomoeoneis sphaerophora f. sculpta (Ehrenberg) ANSS Krammer in Krammer & Lange-Bertalot 1985 Anomoeoneis vitrea (Grunow) Ross in Patrick & ANV Reimer 1966 Brachysira australofollis H. Lange-Bertalot & BRAL G. Moser 1994 Brachysira hofmanniae H. Lange-Bertalot in BROF H. Lange-Bertalot & G. Moser 1994 Brachysira neoexilis H. Lange-Bertalot BREX in H. Lange-Bertalot & G. Moser 1994 Brachysira procera H. Lange-Bertalot BRPR & G. Moser 1994 Brachysira vitrea (Grunow) R. Ross in Hartley 1986 BRVI Brachysira sp. BRSP Caloneis alpestris (Grunow) Cleve 1894 CAL Caloneis bacillum (Grunow) Cleve 1894 CAB Caloneis fontinalis (Grunow) Lange-Bertalot & CAFO Reichardt in Lange-Bertalot & Metzeltin 1996 Capartogramma paradisiaca Novelo, CAPA Tavera & Ibarra 2007 Climaconeis colemaniae A.K.S.K. Prasad in Prasad, CLIM A.K.S.K., Riddle, K.A. & J.A. Nienow 2000 Craticula ambigua (Ehrenberg) Mann in Round, CRAA Crawford & Mann 1990 Craticula cuspidata (Kutzing) Mann in Round, NCU Crawford & Mann 1990 Craticula halophila (Grunow ex Van Heurck) NAHA Mann in Round, Crawford & Mann 1990 Craticula perrotettii Grunow 1867 CRPE Cymbella mexicana (Ehrenberg) Cleve 1984 CYMX Cymbella rhomboidea Boyer 1916 CYRH Cymbella sp. 25 CY25 Diadesmis confervacea Kutzing 1844 NACF Diadesmis contenta (Grunow ex Van Heurck) NCN Mann in Round, Crawford & Mann 1990 Encyonema densistriata Novelo, Tavera & Ibarra 2007 ENDE Encyonema gracile Rabenhorst 1853 CYL Encyonema mesianum (Cholnoky) Mann in Round, CYME Crawford & Mann 1990 Encyonema minutum (Hilse in Rabenhorst) Mann in CYMT Round, Crawford & Mann 1990 Encyonema muelleri (Hustedt) Mann in Round, CYMU Crawford & Mann 1990 Encyonema perpusillum (A. Cleve) Mann in Round, CYPE Crawford & Mann 1990 Encyonema silesiacum (Bleisch in Rabenhorst) Mann CYML in Round, Crawford & Mann 1990 Encyonema turgidum (Gregory) Grunow CYTI in Schmidt et al. 1875 Encyonopsis angusta Krammer et Lange-Bertalot CYAM in Krammer 1997 Encyonopsis cesatii (Rabenhorst) Krammer 1997 CYC Encyonopsis falaisensis (Grunow) Krammer 1997 CYF Encyonopsis microcephala (Grunow) Krammer 1997 CYMI Encyonopsis naviculacea (Grunow) Krammer 1997 CYNV Diploneis caffra (Giffen) A. Witkowski, DICA H. Lange-Bertalot & D. Metzeltin 2000 Diploneis fusca (Gregory) Cleve 1894 DFUS Diploneis litoralis (Donkin) Cleve 1894 DILI Diploneis oblongella (Naegeli in Kutzing) Cleve-Euler DOB in Cleve-Euler (& Osvald) 1922 Diploneis ovalis (Hilse in Rabenhorst) Cleve 1891 DO Entomoneis paludosa (W. Smith) Reimer in Patrick ENTO & Reimer 1975 Eolimna minima (Grunow in Van Heurck) NAI H. Lange-Bertalot in G. Moser, H. Lange-Bertalot & D. Metzeltin 1998 Eolimna submuralis (Hustedt) Lange-Bertalot NAS & Kulikovskiy in Kulikovskiy et al. 2010 Eolimna aff. submuralis (Hustedt) Lange-Bertalot & NUSI Kulikovskiy in Kulikovskiy et al. 2010 Fallacia pygmaea (Kutzing) Stickle & Mann in Round, NPYG Crawford & Mann 1990 Fistulifera pelliculosa (Brebisson) Lange-Bertalot 1997 NPE Gomphonema affine Kutzing 1844 GAFF Gomphonema amoenum Lange-Bertalot in Krammer GOE & Lange-Bertalot 1985 Gomphonema angustum Agardh 1831 GOIM Gomphonema clevei Fricke in Schmidt et al. 1902 GC Gomphonema gracile Ehrenberg 1854 GG Gomphonema hebridense Gregory 1854 GOH Gomphonema insigne Gregory 1856 GOIN Gomphonema parvulum (Kutzing) Kutzing 1849 GP Gomphonema pseudoaugur Lange-Bertalot 1979 GPA Gomphonema pseudotenellum Lange-Bertalot in GPST Krammer & Lange-Bertalot 1985 Gomphonema truncatum Ehrenberg 1832 GT Gomphonema vibrioides Reichardt & GOVI Lange-Bertalot 1991 Gomphonema aff. bozenae Lange-Bertalot et GOBE Reichardt in Lange-Bertalot & Metzeltin 1996 Gomphonema sp. GOSP Gyrosigma baltica (Ehrenberg) Rabenhorst 1853 GBAL Halamphora acutiuscula (Kutzing) Z. Levkov 2009 AMCU Halamphora coffeaeformis (Agardh) Z. Levkov 2009 AMCO Halamphora montana (Krasske) Z. Levkov 2009 AMMO Halamphora normanii (Rabenhorst) Z. Levkov 2009 AMNI Halamphora veneta (Kutzing) Z. Levkov 2009 AMVN Hippodonta capitata (Ehrenberg) Lange-Bertalot, NACA Metzeltin & Witkowski 1996 Hippodonta hungarica (Grunow) Lange-Bertalot, NCHU Metzeltin & Witkowski 1996 Luticola mutica (Kutzing) Mann in Round, Crawford NAMM & Mann 1990 Mastogloia asperuloides Hustedt 1933 MAAS Mastogloia braunii Grunow 1863 MABR Mastogloia constricta Cleve 1892 MACO Mastogloia cyclops Voigt 1942 MACY Mastogloia elliptica (Agardh) Cleve in MASE Schmidt et al. 1893 Mastogloia elliptica var. dansei (Thwaites) Cleve 1895 MDAN Mastogloia lanceolata Thwaites in W. Smith 1856 MLAN Mastogloia malayensis Hustedt 1942 MALY Mastogloia pseudoelegans Hustedt 1955 MELP Mastogloia pusilla Grunow 1878 MAPP Mastogloia recta Hustedt 1942 MREC Mastogloia smithii Thwaites in lit. ex W. Smith 1856 MASM Mastogloia smithii var. lacustris Grunow 1878 MASL Mastogloia aff. gracilis Hustedt 1933 MAAG Mastogloia aff. recta Hustedt 1942 MARC Mastogloia sp. MASP Navicula apta Hustedt 1955 NAPT Navicula concentrica Carter & Bailey-Watts 1981 NCCA Navicula cryptotenella Lange-Bertalot in Krammer & NRT Lange-Bertalot 1985 Navicula eidrigiana Carter 1979 NEDR Navicula flanatica Grunow 1860 NAFN Navicula gregaria Donkin 1861 NGG Navicula hasta Pantocsek 1892 NHAS Navicula leptostriata Jorgensen 1948 NLEP Navicula palestinae Gerloff, Natour & Rivera 1984 NPAE Navicula perminuta Grunow in Van Heurck 1880 NAPR Navicula phyllepta Kutzing 1844 NAPH Navicula pseudoarvensis Hustedt 1942 NPS Navicula pseudocrassirostris Hustedt 1961 NPCO Navicula radiosa Kutzing 1844 NRA Navicula salinarum Grunow 1880 NRUM Navicula salinicola Hustedt 1939 NASA Navicula schroeteri Meister 1932 NACH Navicula subrhynchocephala Hustedt 1935 NCHO Navicula subrostellata Hustedt 1955 NSRO Navicula subrotundata Hustedt 1945 NSO Navicula veneta Kutzing 1844 NAVE Navicula sp. NS Neidium ampliatum (Ehrenberg) Krammer in Krammer NEAP & Lange-Bertalot 1985 Neidium iridis (Ehrenberg) Cleve 1894 NEI Oestrupia powelli (Lewis) Heiden ex Hustedt 1935 NPOW Parlibellus panduriformis John 1991 PARP Parlibellus aff. crucicula (W. Smith) A. Witkowski, NCRU H. Lange-Bertalot & D. Metzeltin 2000 Parlibellus sp. PARL Petroneis sp. PETRO Pinnularia acrosphaeria Rabenhorst 1853 PA Pinnularia alpina Mereschkowsky 1906 PIAL Pinnularia appendiculata (Agardh) Cleve 1895 PIAP Pinnularia borealis Ehrenberg 1843 PIB Pinnularia braunii (Grunow in Van Heurck) PBR Cleve 1895 Pinnularia cuneatiformis Krammer et Metzeltin PICU in Metzeltin & Lange-Bertalot 1998 Pinnularia divergens W. Smith 1853 PIDI Pinnularia interrupta W. Smith 1853 PIIT Pinnularia major (maior) (Kutzing) Rabenhorst 1853 PIMA Pinnularia mesolepta (Ehrenberg) W. Smith 1853 PIME Pinnularia microstauron (Ehrenberg) Cleve 1891 PIMI Pinnularia subcapitata Gregory 1856 PISU Pinnularia tabellaria Ehrenberg 1843 PITB Pinnularia stomatophora (Grunow in Schmidt et al.) PITO Cleve 1895 Pinnularia streptoraphe Cleve 1891 PITR Placoneis clementioides (Hustedt) Cox 1987 PLCI Placoneis porifera (Hustedt) E.J. Cox 2003 NPOR Plagiotropis neovitrea Paddock 1988 PLVI Pleurosigma sp. PLSP Rhoicosphenia abbreviata (C. Agardh) GAB Lange-Bertalot 1980 Sellaphora densistriata (H. Lange-Bertalot & SEDE D. Metzeltin) H. Lange-Bertalot & D. Metzeltin in D. Metzeltin & H. Lange-Bertalot 2002 Sellaphora laevissima (Kutzing) D.G. Mann 1989 NAV Sellaphora pupula (Kutzing) Mereschkowsky 1902 NAPP Sellaphora seminulum (Grunow) D.G. Mann 1989 NSM Sellaphora stroemii (Hustedt) H. Kobayasi in Mayama, NSTR S., Idei, M., Osada, K. & T. Nagumo 2002 Seminavis strigosa (Hustedt) D.G. Mann & AMST A. Economou-Amilii in D.B. Danielidis & D.G. Mann 2003 Seminavis robusta Danielidis & D.G. Mann 2002 SEMI Seminavis pusilla (Grunow) E.J. Cox & G. Reid 2004 CYMP Stauroneis anceps Ehrenberg 1843 SA Stauroneis nana Hustedt 1957 STNA Stauroneis phoenicenteron (Nitzsch) Ehrenberg 1843 SPH Stauroneis schimanskii Krammer in Krammer STSH & Lange-Bertalot 1985 Stauroneis aff.schimanskii Krammer in Krammer STAH & Lange-Bertalot 1985 Epithemiaceae Epithemia adnata (Kutzing) Brebisson 1838 EZ Epithemia turgida (Ehrenberg) Kutzing 1844 ET Epithemia sp. EPSP Rhopalodia acuminata Krammer in Lange-Bertalot RHAC & Krammer 1987 Rhopalodia gibba (C.G. Ehrenberg 1830) RG O. Muller 1895 Bacillariaceae Bacillaria paxillifera (O. F. Muller) Hendey 1951 BACX Denticula elegans Kutzing 1844 DE Denticula kuetzingii Grunow 1862 DKU Denticula neritica Holmes & Croll 1984 DNER Denticula subtilis Grunow 1862 DSB Hantzschia amphioxys (Ehrenberg) Grunow in Cleve HA & Grunow 1880 Hantzschia virgata (Roper) Grunow in Cleve & HAVR Grunow 1880 Nitzschia acidoclinata Lange-Bertalot 1976 NIAC Nitzschia amphibia Grunow 1862 NIAM Nitzschia amphibia f. frauenfeldii (Grunow) NIFE Lange-Bertalot in Lange-Bertalot & Krammer 1987 Nitzschia amphibioides Hustedt 1942 ND Nitzschia bacillum Hustedt 1922 NIBU Nitzschia commutata Grunow in Cleve & Grunow 1880 NTCM Nitzschia constricta (Kutzing) Ralfs in Pritchard 1861 NICO Nitzschia distans Gregory 1857 NDIN Nitzschia frustulum (Kutzing) Grunow in Cleve NFRU & Grunow 1880 Nitzschia frustulum var. bulnheimiana (Rabenhorst; NBUL Rabenhorst) Grunow in Van Heurck 1881 Nitzschia gessneri Hustedt 1953 NGSS Nitzschia gracilis Hantzsch 1860 NTGR Nitzschia granulata Grunow 1880 NGRA Nitzschia grossestriata Hustedt 1955 NIGR Nitzschia hantzschiana Rabenhorst 1860 NIH Nitzschia homburgiensis Lange-Bertalot 1978 NIHO Nitzschia inconspicua Grunow 1862 NI Nitzschia lacuum Lange-Bertalot 1980 NILA Nitzschia liebethruthii Rabenhorst 1864 NILI Nitzschia linearis (Agardh) W. Smith 1853 NILN Nitzschia littorea Grunow in Van Heurck 1881 NIL Nitzschia microcephala Grunow 1880 NIMI Nitzschia miserabilis Cholnoky 1963 NBIS Nitzschia nana Grunow in Van Heurck 1881 NINA Nitzschia palea (Kutzing) W. Smith 1856 NPA Nitzschia pararostrata (Lange-Bertalot) NIPR Lange-Bertalot 1996 Nitzschia perminuta (Grunow in Van Heurck) NIPE M. Peragallo 1903 Nitzschia pseudofonticola Hustedt 1942 NIPF Nitzschia sigma (Kutzing) W. Smith 1853 NSIG Nitzschia sp. 1 NISP1 Nitzschia subacicularis Hustedt in Schmidt et al. 1922 NISU Nitzschia thermaloides Hustedt 1955 NTOI Nitzschia vitrea Norman 1861 NIVT Tryblionella acuminata W. Smith 1853 NICU Tryblionella hungarica (Grunow) Mann in Round, NIHU Crawford & Mann 1990 Tryblionella levidensis W. Smith 1856 NILE Tryblionella panduriformis (Gregory) Pelletan 1889 NPAN Tryblionella scalaris (Ehrenberg) P. Siver NSCI & P.B. Hamilton 2005 Surirellaceae Campylodiscus echeneis Ehrenberg ex Kutzing 1844 CAEC Campylodiscus clypeus (Ehrenberg) Kutzing 1844 CAMPY Stenopterobia delicatissima (Lewis) Van Heurck 1896 SUE Surirella (Suriraya) elegans Ehrenberg 1843 SUEL Surirella ovalis Brebisson 1838 SUO Surirella sp. SUR Surirella striatula Turpin 1816-1829 SUTR TABLE 4 Microcrustaceans found in aquatic ecosystems in the Northern Neotropics. Species are ordered alphabetically within orders and families. Species codes in bold (cladocerans= 32; copepods= 3; ostracodes=17) were included in multivariate analysis. Code indicates the species abbreviations used in figures 6 and 8. For the ecosystem studies see tables 1a,b Taxa Code Cladocerans (n=51) Order Ctenopoda Family Sididae Diaphanosoma brevireme Sars 1901 DBR Latonopsis australis group LAU Pseudosida ramosa Daday 1904 PRA Order Anomopoda Family Daphniidae Ceriodaphnia dubia Richard 1894 CDU Ceriodaphnia cf. rigaudi Richard 1894 CRI Daphnia mendotae Birge 1918 DME Daphnia pulicaria Forbes 1893 DPU Scapholeberis armata freyi Dumont & Pensaert 1983 SAR Simocephalus congener (Koch 1841) SCO Simocephalus mixtus Sars 1903 SMI Simocephalus serrulatus (Koch 1841) SSE Family Moinidae Moina minuta Hansen 1899 MMI Moinodaphnia macleayi (King 1953) MMA Family Bosminidae Bosmina huaronensis Delachaux 1918 BHU Bosmina tubicen Brehm 1953 BTU Bosminopsis deitersi Richard 1895 BDE Family Ilyocryptidae Ilyocryptus spinifer Herrick 1882 ISP Family Macrothricidae Macrothrix elegans Sars 1901 MEL Macrothrix paulensis (Sars 1900) MPA Macrothrix cf. spinosa King 1853 MSP Streblocerus pygmaeus Sars 1901 SPY Family Chydoridae Alona dentifera (Sars 1901) ADE Alona guttata group AGU Alona ossiani Sinev 1998 AOS Alonella cf. excisa (Fischer, 1854) AEX Anthalona brandorffi (Sinev & Hollwedel 2002) ABR Anthalona verrucosa (Sars 1901) AVE Camptocercus dadayi Stingelin 1900 CDA Chydorus brevilabris Frey 1980 CHB Chydorus eurynotus Sars 1901 CHE Chydorus nitidulus Sars 1901 CHN Coronatella circumfimbriata (Megard 1967) CCI Coronatella monacantha (Sars 1901) CMO Dadaya macrops (Daday 1888) DMA Dunhevedia odontoplax Sars 1901 DOD Ephemeroporus barroisi (Richard 1894) EBA Ephemeroporus hybridus (Daday 1905) EHY Ephemeroporus tridentatus (Bergamin 1939) ETR Euryalona orientalis (Daday 1898) EOR Graptoleberis testudinaria (Fischer 1848) GTE Karualona muelleri (Richard 1897) KMU Kurzia longirostris Daday 1888 KLO Kurzia polyspina Hudec 2000 KPO Leberis davidi (Richard 1895) LDA Leydigia striata Biraben 1939 LST Notoalona globulosa (Daday 1898) NGL Oxyurella ciliata Bergamin 1939 OCI Oxyuella longicaudis Birge 1910 OLO Pleuroxus quasidenticulatus Smirnov 1996 PQU Pseudochydorus globosus (Baird 1843) PSG Copepods (n=6) Class Maxillopoda Subclass Copepoda Order Calanoida Family Diaptomidae Arctodiaptomus dorsalis (Marsh 1907) ADO Leptodiaptomus siciloides (Lilljeborg 1889) LSI Mastigodiaptomus nesus Bowman 1986 MNE Mastigodiaptomus reidae Suarez-Morales MRE & Elias- Gutierrez 2000 Prionodiaptomus colombiensis (Thiebaud 1912) PCO Family Pseudodiaptomidae Pseudodiaptomus marshi Wright 1936 PMA Ostracodes (n=29) * Class Ostracoda Order Podocopida Family Darwinulidae Darwinula stevensoni (Brady & Robertson 1870) DST Family Candonidae Candona sp. CAN Physocypria cf. denticulata (Daday 1905) PDE Physocypria globula Furtos 1933 PGL Physocypria xanabanica (Furtos 1936) PXA Pseudocandona sp. PSE Thalassocypria sp. THA Family Cyprididae Candonocypris cf. serratomarginata (Furtos 1936) CSE Chlamydotheca colombiensis Roessler 1985 CCO Cypretta cf. brevisaepta Furtos 1934 CBR Cypridopsis okeechobei Furtos 1936 COK Cypridopsis vidua (Muller 1776) CVI Eucypris sp. EUC Heterocypris punctata Keyser 1975 HPU Potamocypris sp. POT Stenocypris major (Baird 1859) SMA Strandesia intrepida Furtos 1936 SIN Trajancypris sp. TRA Family Cytheridae Perissocytheridea cribosa (Klie 1933) PCR Family Cytherideidae Cyprideis sp. CIS Family Cytheromatidae Paracytheroma stephensoni Puri 1954 PST Family Cytheruridae Cytherura sandbergi Morales 1966 CSA Family Ilyocyprididae Ilyocypris cf. gibba Ramdohr 1808 IGI Family Limnocytheridae Cytheridella ilosvayi Daday 1905 CIL Elpidium bromeliarum Muller 1880 EBR Limnocythere floridensis Keyser 1976 LFL Limnocythere opesta Brehm 1939 LOP Limnocythere sp. LIM Family Loxoconchidae Loxoconcha sp. LOX * Perez et al. (2011a). TABLE 5 Results of the Canonical Correspondence Analysis (CCA) and Redundancy Analysis (RDA) using chironomid, diatom, cladoceran, ostracode and copepod species data and forward selected variables (FSV) CCA Axes 1 2 3 4 Chironomids; FSV=7 Eigenvalues 0.141 0.110 0.087 0.080 Species-environment correlations 0.792 0.781 0.864 0.738 Cumulative percentage variance of species data 4.8 8.6 11.6 14.4 of species-environment relation 24.8 44.3 59.6 73.6 Sum of all canonical eigenvalues Diatoms; FSV=7 Eigenvalues 0.416 0.329 0.260 0.184 Species-environment correlations 0.890 0.947 0.834 0.831 Cumulative percentage variance of species data 6.8 12.2 16.4 19.4 of species-environment relation 26.9 48.2 65.0 76.9 Sum of all canonical eigenvalues Cladocerans, FSV=4 Eigenvalues 0.273 0.147 0.085 0.069 Species-environment correlations 0.771 0.677 0.635 0.611 Cumulative percentage variance of species data 6.4 9.9 11.9 13.5 of species-environment relation 47.5 73.1 87.9 100.0 Sum of all canonical eigenvalues Ostracodes; FSV=6 Eigenvalues 0.312 0.133 0.103 0.047 Species-environment correlations 0.792 0.611 0.561 0.398 Cumulative percentage variance of species data 9.9 14.2 17.4 18.9 of species-environment relation 49.7 70.9 87.3 94.8 Sum of all canonical eigenvalues RDA Calanoid copepodes, FSV=4 Eigenvalues 0.249 0.106 0.039 0.382 Species-environment correlations 0.637 0.670 0.510 0.000 Cumulative percentage variance of species data 24.9 35.5 39.4 77.6 of species-environment relation 63.1 90.1 100.00 0.0 Sum of all canonical eigenvalues CCA Axes Total inertia Chironomids; FSV=7 Eigenvalues 2.909 Species-environment correlations Cumulative percentage variance of species data of species-environment relation Sum of all canonical eigenvalues 0.567 Diatoms; FSV=7 Eigenvalues 6.111 Species-environment correlations Cumulative percentage variance of species data of species-environment relation Sum of all canonical eigenvalues 1.545 Cladocerans, FSV=4 Eigenvalues 4.247 Species-environment correlations Cumulative percentage variance of species data of species-environment relation Sum of all canonical eigenvalues 0.574 Ostracodes; FSV=6 Eigenvalues 3.140 Species-environment correlations Cumulative percentage variance of species data of species-environment relation Sum of all canonical eigenvalues 0.627 RDA Calanoid copepodes, FSV=4 Eigenvalues 1.000 Species-environment correlations Cumulative percentage variance of species data of species-environment relation Sum of all canonical eigenvalues 0.394
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|Title Annotation:||articulo en ingles|
|Author:||Perez, Liseth; Lorenschat, Julia; Massaferro, Julieta; Pailles, Christine; Sylvestre, Florence; Holl|
|Publication:||Revista de Biologia Tropical|
|Date:||Jun 1, 2013|
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