An Index of Limnological Conditions for Urban Wetlands of Bogotã¡ City, Colombia

Home , Altiplano Cundiboyacense, El Burro, Jaboque, La Conejera, La Vaca, Techo (wetland)

Ecological Indicators 10 (2010) 848–856

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Ecological Indicators

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An index of limnological conditions for urban wetlands of Bogota´ city, Colombia

Gabriel Pinilla *

Biology Department, National University of Colombia, Colombia

ARTICLE INFO ABSTRACT

Article history: The urban wetlands of Bogota´ are ecosystems of great importance, yet they are deteriorating. The state of Received 20 September 2009 deterioration must be evaluated in order to develop new methods of ecosystem monitoring and Received in revised form 5 January 2010 conservation. Here we describe the development of an index to assess the ecological health of five urban Accepted 17 January 2010 wetlands and one rural wetland from limnological data. The field phase of this study took place in November 2007 (rainy season) and February 2008 (dry season). Physical and chemical variables of the Keywords: wetland ecosystems (temperature, dissolved oxygen, pH, conductivity, hardness, chlorides, ammonia, Urban wetlands nitrites, nitrates, orthophosphates, and biological oxygen demand) were measured and samples of Multi-metric index phytoplankton, periphyton, macroinvertebrates, and aquatic plants (macrophytes) were collected. The Limnological condition Colombia indices developed (biotic indices of communities: BI, and limnological conditions index: LICOI) allow classification of wetlands into three categories: those that have ‘‘acceptable limnological conditions’’ (Meridor, Jaboque and Guaimaral), those with ‘‘regular limnological conditions’’ (Santa Marıá del Lago, Juan Amarillo) and those with ‘‘poor limnological conditions’’ (Tibanica). None of the environments studied fit a potential fourth category of ‘‘best limnological conditions.’’ The LICOI is a management tool that can be used to assess changes in wetlands after positive actions (restoration, cleaning, hydraulic management), or negative impacts (depletion, alien species, pollution). It also could allow regular monitoring of wetland evolution and serve as a basis for the development of indices measuring the ecological status of other aquatic environments in Colombia. ß 2010 Elsevier Ltd. All rights reserved.

1. Introduction group (e.g., fish, Harris and Silveira, 1999; periphyton, Hill et al., 2003;macrophytes,Reiss, 2006; vascular plants, Miller et al., 2006; In the 1970s and 1980s, evaluation of global aquatic systems was diatoms, Lane and Brown, 2007; macroinvertebrates, Smith et al., based on individual information about each variable (e.g., physical, 2007). For the study of Colombian ecosystems, there is a chemical, or biological) measured in the body of water (Tolkamp and macroinvertebrate index, adapted from a European index (Roldań, Gardeniers, 1988). Later, in the 1990s, these variables were 2003), and some exercises to assign primary bioindication values for integrated, and indices of physicochemical quality (Kung et al., macroinvertebrate families (Riss et al., 2002a, 2002b). Riverine 1992; Dojlido et al., 1994; Van Helmond and Breukel, 1997)and diatoms were also used as bioindicators to assess the water quality biological integrity appeared (Jackon and Davis, 1994; Barbour et al., of Andean rivers (Dıáz and Rivera, 2004). However, there are no 1999; Barbour et al., 2000; Pinilla, 2000). More recently, develop- indices of limnological conditions for any aquatic ecosystems in ments of indices have included both abiotic and biological factors in Colombia that were developed integrating both physicochemical the same equation. To date, there are an appreciable number of such and biological indices. metrics. These indices vary from simple structures (e.g., indices of Most limnological indices that have been developed are ideal trophic classification and water-quality assessment, Vollenweider for use in temperate regions, and are not appropriate for assessing et al., 1998; Viaroli and Christian, 2003; Sańchez et al., 2007), to tropical ecosystems. Rivers are the best-studied ecosystems complex multi-metrics that take into account physical and internationally, and macroinvertebrates have the most metrics. biological factors (e.g., indices of lotic or lentic conditions, Schultz, There are few indices for wetlands and metrics for biological 2001; Hu et al., 2006; Brazner et al., 2007). Between these two groups such as bacteria, protozoa, and zooplankton have only extremes lie a variety of indices that focus on a particular biological recently been developed. The wetlands of Bogota´ are ecosystems of great importance, largely due to their myriad ecological and social functions. At * Corresponding author. Tel.: +57 1 3165000; fax: +57 1 3165310. present, there are eleven main wetlands in Bogota´ city: Capellanıá E-mail addresses: [email protected], [email protected]. (18 Ha), La Vaca (40 Ha), Techo (3 Ha), Tibanica (10 Ha), El Burro

(31 Ha), Co´ rdoba (40 Ha), Jaboque (147 Ha) Guymaral-Torca where n is the number of chemical variables, N is the number of (73 Ha), La Conejera (60 Ha), Juan Amarillo or Tibabuyes (40 Ha), stations, and i represents the stations where the taxon was and Santa Maria del Lago (4 Ha) (Moreno et al., 2005). The first five collected. The biotic index (BI) of a given community is calculated of these, which have suffered the greatest deterioration, exist as: within the dry zone of the city (Herrera et al., 2004). In total, the Xn wetland area within the urban district is approximately 500 Ha. As ðTPVÞ mentioned, these aquatic environments are worsening (Van der BI ¼ i¼1 (3) Hammen et al., 2008) and improved methods for assessing their n ongoing deterioration are needed for purposes of monitoring and conservation. In this paper, an index of limnological conditions where n is the number of species or taxa in a community and TPV is (LICOI) is proposed for assessing the urban wetlands of Bogota´,to the pollution value of each taxon, i. serve as a tool for characterization and management of these The LICOI is calculated as the weighted sum of the BI of the ecosystems. various communities. The weighting factor was established based on the regressions obtained in the correlation coefficients. Thus, 2. Materials and methods the BIs of phytoplankton (BIP), periphytic diatoms (BID), and macrophytes (BIM) were each multiplied by 0.3 (because all of 2.1. Location of wetlands and sampling these BI obtained the highest correlation coefficients), and the BI of macroinvertebrates (BII, which has lower correlation coefficient) The wetlands studied belong to the Bogota´ River Basin. Based on was multiplied by 0.1 (the sum of the weights is 1). The BI values secondary information and preliminary assessment, five of these were converted to percentages (100% is the highest possible BI for wetlands with diverse degrees of preservation and deterioration each community) and subtracted from 100 to obtain estimates were selected for study (Guaimaral, Jaboque, Tibanica, Santa Marıá directly proportional to the degree of conservation and the LICOI. del Lago, Juan Amarillo). A small rural wetland (Meridor 9.6 Ha, Thus, the LICOI is high for limnological systems in good condition municipality of Tenjo) was also included as a reference system due (well-preserved ecological functions) and low for limnological its low degree of human intervention. These wetlands are environments in poor condition (impaired ecological functions). The equation for calculating the LICOI is as follows: relatively close, with a difference of altitude not exceeding 125 m (2451–2576 masl). Each wetland was sampled twice, once LICOI ¼ 100 %BIP 0:3 þ 100 %BID 0:3 during the November 2007 rainy season and once during the February 2008 dry season. For each sample period, three sites in each wetland were selected to measure the following physical and þ 100 %BII 0:1 þ 100 %BIM 0:3 (4) chemical variables: Secchi transparency, temperature, dissolved oxygen, pH, conductivity, hardness, chlorides, ammonia, nitrites, where %BIP is the biotic index of phytoplankton, %BID is the biotic nitrates, orthophosphates, and biological oxygen demand (BOD5). index of periphytic diatoms, %BII is the biotic index of aquatic Communities of phytoplankton, periphytic diatoms, macroinver- macroinvertebrates, and %BIM is the biotic index of aquatic tebrates, and aquatic plants (macrophytes) were collected from the macrophytes, all expressed in percentages. same three sites for each wetland and assessed. In all cases, Four categories for the wetlands of Bogota´, based on %BI and standard methods proposed by APHA (1995), Wetzel and Likens LICOI values, were established using quartiles. In order to confirm (1991), and Rueda (2002) were followed. the significance of index calculations, correlations were identified between the environmental conditions, expressed as PI values, and 2.2. Development of Indices the BI and LICOI values. Similarly, regression graphs between indices and PI values were drawn, using the logarithmic equation, The pollution index (PI) was computed, integrating all Y = a log (X)+b. physicochemical variables, using the methodology proposed by Jiang and Shen (2005) and Jiang (2006). The variables described are 3. Results those for which Colombian law has established allowable limits for drinking water, and which have a direct relationship with the 3.1. Physical and chemical environment ecology of aquatic systems (conductivity, total dissolved solids, dissolved oxygen, pH, chloride, carbonate hardness, ammonia, Table 1 summarizes the information on physical and chemical nitrites, nitrates, phosphates, and biological oxygen demand). The variables in selected wetlands. In general, each wetland exhibits PI allowed determination of taxon-pollution values (TPV), which some unique characteristics. Jaboque has high oxygen content and were used to calculate the biotic indices (BI) for each community alkaline pH, likely due to high phytoplankton photosynthesis. collected. The following are the equations for calculating the PI, the Tibanica and Meridor have high conductivity and dissolved solids, TPV, and the BI: which is consistent with the high chloride concentrations found in these ecosystems. Santa Marıá del Lago has few suspended solids Xn C and moderate oxygen concentration. Juan Amarillo was the richest PI ¼ (1) LC i¼1 in nutrients (ammonium and orthophosphates), indicating a greater degree of eutrophication. Meridor was the most transpar- where PI is the pollution index of a sample or site, C is the ent wetland, with a high degree of water hardness (indicating high concentration of the variable, LC is the variable concentration limit carbonate levels) but low biological oxygen demand (BOD5), which for human consumption according to Colombian Decree 1594 of suggests that this system has the least organic load. 1984, and n is the number of parameters. The pollution value of a With regard to climatic changes between sample periods, it was specific taxon (TPV) is calculated as: observed that the highest conductivity and dissolved solids occurred during the dry period, probably as a result of increased Xn 10PI i evaporation and concentration of ions dissolved in water. During ðLn n Þ the dry season, a BOD reduction was also seen, perhaps due to less TPV ¼ i¼1 (2) 5 N organic matter reaching wetlands via runoff. Transparency also 850 G. Pinilla / Ecological Indicators 10 (2010) 848–856

Table 1 Physical and chemical variables measured in the Bogota´ wetlands in the rainy (November 2007) and in the dry (February 2008) seasons. In Guaimaral, transparency was impossible to measure (IM) in the absence of a water mirror; pH in Jaboque and chlorides in Juan Amarillo were not measured (NM) in the ﬁrst sampling.

Variable Guaimaral Jaboque Tibanica Sta. Marı´a Juan Amarillo Meridor

Rainy Dry Rainy Dry Rainy Dry Rainy Dry Rainy Dry Rainy Dry

Water temperature (8C) 16.5 15.7 20.8 22.5 17.1 19.1 17.9 18.6 20.3 16.5 18.95 20.1 Total dissolved solids (mg/L) 200 375 81.00 117.8 709 819 106 138 127 408 438.5 117.8 Conductivity (mS) 352 485 153.2 168.8 1210 1840 186.9 211.3 214 585 855.5 1339 Dissolved oxygen (mg/L) 2.65 3.19 14.40 8.57 0.2 1.05 4.2 5.1 0.15 1.3 2.4 3.5 pH 6.8 7.3 NM 8.82 6.8 6.8 6.8 7 7.71 7.06 7 7.74 Chlorine (free + total) (mg/L) <0.1 0 <0.1 <0.1 <0.1 0.2 0.1 0.1 0.1 <0.1 0.1 0.1 Chloride (mg/L) 26.5 70 22 16 108 74 NM 15 20 50 368 369

Hardness (mg/L CaCO3) 114 176 80 62 91 179 100.7 98 69 136 295 262 Secchi transparency (m) IM IM 0.92 0.74 1.27 1.35 1.02 1.28 0.63 0.29 2.27 1.8 Suspended solids (mg/L) 47.26 796.75 47.27 45.56 9.16 11.34 0 2.45 20.66 52.38 42.25 19.65 Nitrates (mg/L) 0.01 0 0.1 0.3 0.01 0 0.02 0 0.03 0.3 0.04 0.2 Nitrites (mg/L) 0.002 0 0.006 0.3 0.003 0 0.003 1 0.024 7 0.002 0 Ammonium (mg/L) 0.95 1 0.7 0.6 1.2 0.6 0.4 0.7 10 14 0.01 0 Orthophosphates (mg/mL) 0.25 0.3 1.4 0.5 0.12 1.4 1.6 0 1.1 9.9 1.55 0.2

BOD (mg/L O2) 13 2 24 16 29 8 70 10 84 25 11 8

tended to decline in the dry period, possibly due to a higher Guaimaral. These algae (euglenoids and cyanobacteria) are concentration of plankton algae that reduced light penetration. It is indicators of high levels of nutrients and organic matter (Reynolds, important to note that transparency in Guaimaral was not 2006), so their predominance in Tibanica, Juan Amarillo, and measured due to the lack of a visible water mirror. Guaimaral indicates that these wetlands have signiﬁcant organic The N: P ratio indicates that all systems (except Tibanica and matter loads. Moreover, the relatively greater presence of desmids Juan Amarillo in the rainy season) were limited by nitrogen. This in Santa Maria del Lago indicates that this system has fewer limitation was extreme in Meridor, Jaboque, and Santa Marı´a del minerals, since this group of algae prefers demineralized waters Lago. Only Guaimaral had balanced nutrients close to the ideal (Reynolds, 2006). ratio (N: P = 16). The lack of nitrogen limitation in Tibanica and Table 2 shows the percentages of major periphytic diatom taxa Juan Amarillo during the rainy season may indicate greater found in the studied wetlands. Species of Navicula were most ammoniation due to either low oxygen conditions in these abundant and common in all ecosystems during the rainy season, ecosystems, or increased inputs of residual waters high in followed by Gomphonema and Nitzchia. The genera Cyclotella and ammonium. Fragilaria were most abundant during the rainy season in Juan Amarillo and Guaimaral, respectively. During the dry season, 3.2. Biotic communities Navicula species diminished, while Gomphonema and Nitzschia became more abundant. In Meridor, Eunotia increased during the Diatoms, dinophytes, euglenoids, chlorophytes, and cyanobac- dry season, as did Stauroneis and Cyclotella in Tibanica, Fragilaria in teria were present in the phytoplankton of all wetlands (Fig. 1). Jaboque, and Achnanthes in Santa Maria del Lago. In general, there However, different groups dominated in each ecosystem. In was a large variability of diatom taxa represented, among the Meridor, the euglenophytes and dinophytes prevailed; dinophytes various wetlands as well as between seasons. Many of these genera were particularly dense in the dry period. In Tibanica, cyanobac- are indicators of meso to eutrophic states (Muscio, 2002; Lane and teria were predominant, whereas in Jaboque the large chlorophyte Brown, 2007), characteristics consistent with the general condi- community (Oocystis and Scenedesmus) may explain the high tions of the studied water bodies. oxygen concentration. Euglenoids and chlorophytes were domi- Fig. 2 clearly reveals differences in abundance and composition nant in Juan Amarillo, and euglenoids and cyanobacteria in of macroinvertebrate fauna in the evaluated wetlands. Most

Fig. 1. Abundance in percentage of phytoplankton divisions in the Bogota´ urban wetlands during the rainy (a) and dry (b) seasons. M: Meridor, T: Tibanica, J: Jaboque, SM: Santa Marı´a del Lago, JA: Juan Amarillo, G: Guaimaral. G. Pinilla / Ecological Indicators 10 (2010) 848–856 851

Table 2 Abundances in percentage of the periphytic diatoms in urban wetlands of Bogota´ in rainy (November 2007) and dry (February 2008) seasons.

Taxon Meridor Tibanica Jaboque SM del Lago Juan Amarillo Guaimaral

Rainy Dry Rainy Dry Rainy Dry Rainy Dry Rainy Dry Rainy Dry

Navicula spp. 35.9 26.6 33.4 16.5 11.3 32.6 26.7 2.6 36.9 4.9 Epithemia cf goeppertiana 0.5 4.3 0.9 5.0 Epithemia cf adnata 1.5 Epithemia other spp 4.8 1.2 Eunotia spp 7.5 28.0 0.7 3.0 1.9 27.2 3.8 Fragilaria spp 4.2 8.0 22.0 1.5 Fragilaria cf ulna 52.3 4.5 24.7 Gomphonema cf acuminatum 10.3 19.4 Gomphonema cf truncatum 7.7 3.6 1.8 3.9 Gomphonema cf parvulum 1.0 Gomphonema cf pseudoaugur 4.2 Gomphonema cf gracile 3.0 Gomphonema other spp 10.4 10.1 43.3 23.4 14.9 22.2 24.5 23.0 8.2 21.6 53.2 Nitzschia cf amphibia 0.2 0.4 Nitzschia cf umbonata 1.5 Nitzschia other spp 32.0 4.5 8.2 1.1 55.6 14.9 15.2 14.5 10.9 47.0 5.2 18.5 Stauroneis sp 1.3 23.55 8.34 6.2 0.81 1.5 Cocconeis placentula 5.0 5.2 Cocconeis sp 2.1 0.0 2.50 0.12 Cyclotella sp 0.5 11.6 2.0 2.1 2.70 54.4 0.65 Encyonema sp 0.5 Achnanthes cf exigua 1.2 12.0 12.41 Pinnularia spp 1.2 1.0 2.3 3.0 1.9 3.8 1.0 Aulacoseira sp 4.41 Sellaphora sp 0.29 cf Surirella 3.0 0.5 cf Rhopalodia 0.5 0.5 cf Staurosira 0.8 cf Ctenophora 2.6 1.3 cf Discostella cf Martyana 2.9 cf Encyonema 0.80 cf Aulacoseira 2.1 cf Kobayasiella 2.6

Fig. 2. Abundance in organisms per square meter of macroinvertebrates in the Bogota´ urban wetlands during the rainy (a) and dry (b) seasons. M: Meridor, T: Tibanica, J: Jaboque, SM: Santa Marı´a del Lago, JA: Juan Amarillo, G: Guaimaral.

notable is the large number of organisms in Meridor, nearly four (Pennak, 1978; Timm et al., 2006). In more contaminated wetlands times that seen in the other wetlands. Meridor also had a higher (e.g., Juan Amarillo), the planarians (flatworms) were most richness of taxa. This is likely due to the good conditions and lower abundant. In general, all macroinvertebrate taxa found are typical pollution levels in this rural wetland, confirming that it is a cleaner of environments with high organic matter and nutrients. However, system. The most abundant groups in all wetlands were dipterans the most polluted wetland (Juan Amarillo) had more indicators of (chironomids and culicids), followed by annelids (leeches and contamination by organic matter (Oligochaeta and dipterans) and tubificids). Meridor also has bivalves (clams), gordioids (horsehair a lack of organisms indicating clean waters (plecopterans, aquatic worms), acari (mites), and hemipterans (aquatic bugs); some of mites, hydras, and bivalves). In Tibanica, Jaboque, and Santa Marıá these (mites and bivalves) grow best in waters with less pollution del Lago, macroinvertebrate numbers were lower, possibly due to 852 G. Pinilla / Ecological Indicators 10 (2010) 848–856

Table 3 Frequency of occurrence of macrophyte species in urban wetlands of Bogota´. Data are the average of two samples (wet season and dry season).

Vernacular name Scientiﬁc name Meridor Tibanica Jaboque SM del Lago Juan Amarillo Guaimaral

Smooth beggarticks Bidens laevis 0.2 72.625 57.25 67 5.375 Least duckweed Lemna minuta 5.625 5.95 44.935 5.375 Duckweed Spirodela intermedia 51.625 24.55 44.375 89.25 3.625 Common duckweed Lemna minor 38.75 46.685 10.125 Gibbous duckweed Lemna gibba 36.2 8.19 2.5 Water fern Azolla filiculoides 53.25 4.8 24.5 36.625 Floating primrose-willow Ludwigia peploides 27.25 12.63 Floating marshpennywort Hydrocotyle ranunculoides 64.75 6.8 77.875 16.315 97.625 87 American black nightshade Solanum americanum 4.5 1.8 5.125 0.94 6.625 21.375 West Indian spongeplant Limnobium laevigatum 4.1875 Swamp smartweed Polygonum hydropiperoides 17 7.4 1.5 1.8125 4.875 27.375 Clustered dock Rumex conglomeratus 2.25 7.7 12 0.625 61.375 Baccharis Baccharis latifolia 0.8 0.625 Flatsedge Cyperus rufus 7.875 7.5 1.25 55.875 Flatsedge Cyperus sp. 5.375 Kikuyugrass Pennisetum clandestinum 22.5 60.25 1.5 34.5 22.75 Common velvetgrass Holcus lanatus 9.25 3.315 10.75 Streambank rabbitsfoot grass Polypogon elongatus 3.9 Madagascar ragwort Senecio madagascariensis 4.875 1.5 4.5 11 Broadleaf cattail Typha latifolia 6.75 50 50 0.625 California bulrush Schoenoplectus californicus 50 60.2 1.5 3.83 15.625 Common rush Juncus effusus 6 25.625 Spikerush Eleocharis sp. 27.375 Water hyacinth Eichornia crassipes 41.125 68.375 51.875 Spotflower Acmella sp. 5.875 Onerow yellowcress Nasturtium officinale 4.375 13.75 1.25 6.625 Common sowthistle Sonchus oleraceus 1.5 American everlasting Gnaphalium americanum 4.375 0.625 Red clover Trifolium pratense 1.5 Dandelion Taraxacum sp. 2.25 6.75 Bryophyte Marchantia sp. 0.75 Cress Rorippa pinnata 5.875 Umbeliferae 3.75 Asteraceae 2 0.625

Total number of taxa 24 15 14 14 17 17

an excess of organic matter in sediment, which increases oxygen wetlands would be ordered from lowest biological status to demand (BOD5) and worsens benthic environment conditions for highest biological status as follows: Tibanica, Santa Marıá del Lago, these organisms. Juan Amarillo, Jaboque, Meridor, and Guaimaral. As shown in Table 3, several species of aquatic plants are Almost all correlations between biotic indices (expressed as common to most of the studied wetlands, such as duckweeds, percentages) and LICOI with the IP of physicochemical variables smooth beggarticks, floating marshpennywort, American black were statistically significant. There is good correlation and nightshade, swamp smartweed, clustered dock, kikuyugrass, explanation seen for the %BI of phytoplankton (p < 0.0001, broadleaf cattail, and California bulrush. Other species have more r = 0.914), diatoms (p = 0.0001, r = 0.823), and macrophytes restricted distribution that could indicate a preference for more or (p = 0.006, r = 0.764). In the case of the macroinvertebrate %BI, less contaminated water. Smooth beggarticks, common rush, and the correlation is less significant (p > 0.05, r = 0.447) and the water hyacinth seem to thrive best in wetlands with higher organic degree of explanation is low (20%). The LICOI-IP relationship load, while species such as water fern, floating primrose-willow, demonstrates a good adjustment (p < 0.0001, r = 0.891). Similar- and West Indian spongeplant are more abundant in less ly, the regression analysis between %BIs and IP (Fig. 4) indicates contaminated systems. Some species in Table 3 can live in satured good adjustment for %BI of phytoplankton and %BI of the diatoms. soils, or in dry environments. These plants (American black The graphic of the macroinvertebrate %BI confirms the minor fit, nightshade, Baccharis, Madagascar ragwort, common sowthistle, while that of the macrophytes shows a moderate fit. The American everlasting, red clover, dandelions, and grasses in correlation plot between LICOI and IP (Fig. 5) also shows a good fit. general) are located mainly in the supralittoral zone of the Table 4 shows the proposed scales for %BI and LICOI (LICOI wetlands. computed as a weighted sum of BI, shown as a percentage). Once the biotic indices are transformed into percentages, they directly 3.3. Biotic indices and limnological status measure ecological status (i.e., high percentages represent high ecological conservation and low percentages indicate poor Fig. 3 shows the BIs of communities expressed in percentages. conservation). Table 4 also includes an interpretation of each In general, we saw agreement across indices regarding a particular established category. wetland’s pollution status. Tibanica, for example, had the lowest As indicated by the calculated %BIs and LICOI values, Guaimaral, %BI for phytoplankton, diatoms, as well as macrophytes. The LICOI Meridor, and Jaboque are the most conserved ecosystems (LICOI shows a result similar to that described by the various %BI; the higher than 17.5%, as illustrated in Fig. 3 and Table 5), while the LICOI is low in wetlands with low %BIs and high in wetlands with most deteriorated ecosystem is Tibanica (LICOI lower than 4%). high %BIs. Therefore, the LICOI can be used to summarize the Juan Amarillo and Santa Marıá del Lago are in intermediate states pollution status of a particular wetland. Using this index, the of deterioration based on limnological conditions. The %BI of G. Pinilla / Ecological Indicators 10 (2010) 848–856 853

Fig. 3. Biotic Indices (BI) of different communities and limnological condition index (LICOI) expressed in percentage, for Bogota´ urban wetlands. D: dry season (November 2007), R: rainy season (February 2008).

Fig. 4. Regression analysis between %BI of each community and PI of physicochemical variables in Bogota´ urban wetlands. (a) Phytoplankton, (b) Periphytic diatoms, (c) Macroinvertebrates, (d) Macrophytes. phytoplankton and the LICOI are the best indices for comparison 4. Discussion across wetlands and between seasons. It is notable that in all cases (except for Santa Marı´a del Lago), limnological status improves in 4.1. The limnological condition index the second sampling (dry season), possibly due to a reduction in the supply of nutrients and organic matter, which decrease Many of the organisms identiﬁed in the present study have because runoff and sewage connections are lower in this season. been described as indicators of eutrophic or saprobic conditions, 854 G. Pinilla / Ecological Indicators 10 (2010) 848–856

Table 5 Limnological conditions of the Bogota´ urban wetlands based on LICOI. D: dry season (November 2007), R: rainy season (February 2008).

Wetland Limnological status

Meridor-D Acceptable limnological conditions Meridor-R Acceptable limnological conditions Tibanica-D Bad limnological conditions Tibanica-R Bad limnological conditions Jaboque-D Acceptable limnological conditions Jaboque-R Acceptable limnological conditions Santa Marı´a-D Regular limnological conditions Santa Marı´a-R Regular limnological conditions Juan Amarillo-D Regular limnological conditions Juan Amarillo-R Regular limnological conditions Guaimaral-D Acceptable limnological conditions Guaimaral-R Acceptable limnological conditions

Fig. 5. Regression analysis between LICOI and PI of physicochemical variables in Bogota´ urban wetlands. example, a sub-index based on phytoplankton and periphyton might reflect short-time changes, while a sub-index based on such as the phytoplanktonic euglenophytes and cyanobacteria macrophytes and invertebrates could reflect changes on an (Reynolds, 2006), the pennate diatoms of periphyton (Muscio, intermediate time frame. A third sub-index could be created for 2002; Lane and Brown, 2007), the dipterans, annelids, and long-term changes, based on birds, reptiles, and mammals. This flatworms of macroinvertebrates (Roldań, 2003), and the Smooth strategy could be tested in future studies. beggarticks, common rush, and water hyacinth of the macrophytes The PI was calculated using physicochemical criteria of water fit (Cronk and Fennessy, 2001). Thus, the LICOI is consistent with the for human consumption, because these criteria are more bioindication obtained from these organisms. However, not all demanding than those required for the preservation of flora and communities respond similarly to environmental changes. Some fauna in Colombian legislation. Colombia’s legal parameters for populations are more sensitive to physicochemical changes (e.g., biota preservation are involved primarily with heavy metals and phytoplankton and periphyton) and can vary in size rapidly over pesticides and less with physicochemical conditions determining time, making them good indicators of short-term changes. Other the ecological status of wetlands. Simo˜es et al. (2008) used a communities are more permanent (e.g., macroinvertebrates and similar approach of employing physicochemical variables most macrophytes) making them better indicators of medium-term related to the ecological functioning of aquatic systems. fluctuations. The LICOI takes into account both of these sensitivi- The TPV was based on the presence or absence of taxa. In ties, although the weighting strategy gives them varied impor- principle, the abundances of taxa have no influence on the TPV. tance. For instance, the macroinvertebrate community was Therefore, a site with only a few specimens of a given taxon would weighted lower in the LICOI than other communities, because have the same weight in the TPV as a site dominated by this taxon. the explanation and the contribution of these organisms in This could affect the power of the LICOI. However, although the assessing the ecological status of wetlands were low. This is abundance in not taken into account, the frequency of occurrence reasonable because variations in water chemistry impact aquatic in the samples is considered. Thus, the most common taxa are invertebrates less directly, with the exception of pH and dissolved more important in the index. Data regarding the presence or oxygen (Thorp and Covich, 2001). Other communities measured, absence of species have been used successfully in many biotic such as algae and macrophytes, are impacted greatly by indices (e.g., Griffith et al., 2005; Jiang and Shen, 2005) and have physicochemical variables, and changes in water quality can affect been shown to be adequate and sufficient. Moreover, using this invertebrates indirectly through these communities, as they type of qualitative information in determining biotic indices is less provide both food and habitat. Although the %BI of macroinverte- costly in terms of both time and resources. brates was not strongly associated with the IP, it was an aspect of the LICOI equation given the important role of these organisms as 4.2. Limnological conditions of Bogota´ wetlands indicators (Alba-Tercedor, 1996). It is quite possible that a larger sampling, both in space and time, would better identify the Overall, Bogota´ wetland ecosystems are enriched with ions, potential association of %BI of this community with the IP. nutrients, and organic matter in greater or lesser degrees as shown Another approach for evaluating wetland ecological conditions by water chemical data (Table 1), and, in that respect, are much like could be developed based on two or three sub-indices. For wetlands in other regions. This is not surprising, since, in general,

Table 4 Scales proposed for interpretation of the BI of the biological communities and the LICOI (as percentage) for the wetlands of Bogota´.

BI-phytoplankton (%) BI-diatoms (%) BI-macroinvertebrates (%) BI-macrophytes (%) LICOI (%) Interpretation and implications

>50 >30 >15 >20 >35 Wetland slightly contaminated, excellent or good limnological condition, ecological functions are being satisfactorily implemented 30–50 15–30 10–15 10–20 17.5–35 Wetland moderately polluted, acceptable limnological conditions, ecological functions occur within tolerable limits 5–30 5–15 3–10 3–10 4–17.5 Wetland heavily contaminated, regular limnological conditions, ecological functions are abnormal or incomplete <5 <5 <3 <3 <4 Wetland severely contaminated, bad or poor limnological conditions, ecological functions are not fully satisfied or have been lost G. Pinilla / Ecological Indicators 10 (2010) 848–856 855 wetlands are eutrophic and saprobic systems (Horner et al., 2000). ecological health of wetlands and could be extended to other But there is little doubt that urban activity has exacerbated these aquatic environments. The proposed indices are a tool for medium- conditions. Information on the physicochemical characteristics of and long-term management of these ecosystems. However, Bogota´ wetlands is scarce, making comparisons with earlier data optimizing and refining the equations utilized will require more difficult. In the case of Santa Marıá del Lago wetland, conditions detailed taxonomic identification of the organisms evaluated, and described in a previous 2001 study (A´ lvarez, 2009) are similar to the incorporation of additional wetlands (both urban and rural). what was seen in this study. For the other wetlands, the partial Thus, further studies are needed to validate the proposed data available (Va´squez et al., 2006; Van der Hammen et al., 2008) methodology. Despite these limitations, the LICOI allows for the suggest little change in recent years. construction of an index that includes both physicochemical and A comparison of the biotic composition of the wetlands studied biological variables. is difficult, as there is not sufficient published information on the In summary, the results suggest that the new LICOI index could subject. However, the taxa composition and abundance observed be an effective tool for management, prioritization, and monitoring are typical of this type of environment, and similar to what has (restoration assessment) of Bogota´ wetlands and also nearby rural been found in other urban wetlands of Bogota´ (Van der Hammen wetlands. Similarly, use of LICOI in other aquatic environments, et al., 2008). Of course, variations are seen according to the degree such as swamps, reservoirs, and rivers, should be explored with of contamination of each individual wetland. Wetlands with the necessary adjustments to methodology. greatest deterioration mainly supported taxa that are more resistant to pollution, whereas the best-preserved wetlands have Acknowledgments greater species diversity. The low score of Santa Marıá del Lago is remarkable in that it The Research Division of Bogota´ Office (DIB) of the Academic had been established a priori as one of the best-preserved Vice-Rectory, National University of Colombia, funded this work wetlands, due to the positive interventions that have occurred (DIB Code: 6048). I thank biologists Manuela Venegas, Sandra there, including sewage removal and periodic cleaning of large Rojas, Denisse Castro, Andre´s Malago´ n, and Oscar Jimenez, who masses of macrophytes to maintain a sufficiently large water participated directly in this project, both in the field and in the mirror (Van der Hammen et al., 2008). However, this wetland is laboratory. I express my gratitude to the Department of Biology at more ‘‘urban’’ in the sense that it is located within the city, so its the National University of Colombia for the time and resources aquatic communities have been isolated from more natural areas. assigned, which allowed the successful conclusion of this study. I Studies of Pinilla and Guillot (1996) and Ramos-Jiliberto et al. must also make a very special thanks to the anonymous reviewers, (2009) indicate that the isolation of the water body is one of the whose contributions improved the paper substantially. most decisive factors in the composition of phytoplankton. This isolation could partly explain the low LICOI of this wetland. Also, References the pollution levels in this wetland have led to accumulation of many nutrients and organic matter that have not been processed or Alba-Tercedor, J., 1996. Macroinvertebrados acua´ticos y calidad de las aguas de los assimilated due to its total isolation within the city. 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