Bioaccumulation of microcystins in seston, zooplankton and fish: A case study in Lake Zumpango, Mexico

Accepted Manuscript Bioaccumulation of microcystins in seston, zooplankton and fish: a case study in Lake Zumpango, Mexico.

Cesar Alejandro Zamora Barrios, S. Nandini, S.S.S. Sarma PII:

S0269-7491(18)34520-2

DOI:

10.1016/j.envpol.2019.03.029

Reference:

ENPO 12301

To appear in:

Environmental Pollution

Received Date:

08 October 2018

Accepted Date:

10 March 2019

Please cite this article as: Cesar Alejandro Zamora Barrios, S. Nandini, S.S.S. Sarma, Bioaccumulation of microcystins in seston, zooplankton and fish: a case study in Lake Zumpango, Mexico., Environmental Pollution (2019), doi: 10.1016/j.envpol.2019.03.029

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Bioaccumulation of microcystins in seston, zooplankton and fish: a case study in Lake Zumpango, Mexico.

Cesar Alejandro Zamora Barriosa, S. Nandinib*, S.S.S. Sarmab

aPosgrado

en Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México; Av. Ciudad Universitaria 3000, C.P. 04510, Coyoacán, Ciudad de México, México.

bLaboratory

of Aquatic Zoology, Division of Research and Postgraduate Studies, National Autonomous University of Mexico, Campus Iztacala, Av. de Los Barrios No. 1, C.P. 54090, Los Reyes, Tlalnepantla, State of Mexico, Mexico.

E-mail addresses: [email protected] *(Nandini, S.) corresponding author

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Abstract:

45

Cyanotoxins from toxic blooms in lakes or eutrophic reservoirs are harmful to several

46

organisms including zooplankton, which often act as vectors of these secondary

47

metabolites, because they consume cyanobacteria, bioaccumulate the cyanotoxins and pass

48

them on along the food chain. Microcystins are among the most commonly found

49

cyanotoxins and often cause zooplankton mortality. Although cyanobacterial blooms are

50

common and persistent in Mexican water bodies, information on the bioaccumulation of

51

cyanotoxins is scarce. In this study we present data on the bioaccumulation of cyanotoxins

52

from Planktothrix agardhii, Microcystis sp., Cylindrospermopsis

53

Dolichospermum planctonicum blooms in the seston (suspended particulate matter more

54

than 1.2 µm) by zooplankton and fish (tilapia (Oreochromis niloticus) and mesa silverside

55

(Chirostoma jordani) samples from Lake Zumpango (Mexico City). The cyanotoxins were

56

extracted from the seston, zooplankton and fish tissue by disintegration using mechanical

57

homogenization and 75% methanol. After extraction, microcystins were measured using an

58

ELISA kit (Envirologix). Concentration of microcystins expressed as equivalents, reached a

59

maximum value of 117 µg g-1 on sestonic samples; in zooplankton they were in the range

60

of 0.0070 to 0.29 µg g-1. The dominant zooplankton taxa include Acanthocyclops

61

americanus copepodites, Daphnia laevis and Bosmina longirostris. Our results indicate

62

twice the permissible limits of microcystins (0.04 µg Kg-1 d-1) for consumption of

63

cyanobacterial products in whole fish tissue of Chirostoma jordani. The data have been

64

discussed with emphasis on the importance of regular monitoring of water bodies in

65

Mexico to test the ecotoxicological impacts of cyanobacterial blooms and the risk that

66

consumption of products with microcystins could promote.

raciborskii and

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Keywords:

71

Main findings: We found that microcystins do bioaccumulate in the tissue of fish collected

72

from Lake Zumpango, mostly in the liver and intestine. The levels are above the

73

permissible limits in Chirostoma jordani, which is consumed whole, than in Oreochromis

74

niloticus where only the muscular tissue is eaten.

Microcystins, Bioaccumulation, Chirostoma jordani, Oreochromis niloticus, Mexico.

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Graphical abstract:

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Highlights: 1. Cyanobacterial blooms result in high levels of microcystins in water, zooplankton and fish. 2. We observed bioaccumulation of microcystins in the primary and secondary consumers. 3. This is a risk to those who consume small species of fish such as Chirostoma whole and raw (dried). 4. Larger species, especially tilapia was not much affected and is probably a better dietary option. 5. Regular risk assessment of aquaculture produce, an important protein source, is recommended.

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1. Introduction

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The pioneering studies of Carson (1962) led to a surge in investigation on the adverse

94

effects of bioaccumulation and the biotransfer of toxicants along the food chain or web. As

95

a result of this process, concentrations of chemical substances in the tissues of organisms

96

exceed the levels in the medium, due to uptake by all exposure routes (Ibelings and Chorus,

97

2007). Several studies indicate that heavy metals, pharmaceutical products and organic

98

compounds easily bioaccumulate in the tissues of fish (Van der Oost et al., 2003; Tanoue et

99

al., 2014). This is a risk to humans since fish is an important source of protein and part of

100

the staple diet in several countries. Fish, especially omnivorous taxa, accumulate

101

microcystins (MCs) in their tissues through the consumption of cyanobacteria. Contact of

102

epithelial cells (skin and gills) with diluted cyanotoxins in the environment may also result

103

in bioaccumulation although this route is less important since mixis in the lake, adsorption

104

by clay, photolysis and bacterial degradation could reduce the availability of diluted toxins

105

(Ibelings and Chorus, 2007). Another route is via zooplankton, one of the most important

106

links between the primary producers and secondary or tertiary consumers. Thus,

107

zooplankton could be an important vector of cyanotoxins towards higher trophic levels,

108

including humans (Ferrão-Filho et al., 2002; Berry et al., 2011).

109

Microcystins (MCs) are among the most abundant cyanotoxins in freshwater and

110

brackish water environments, with more than 240 reported congeners (Spoof and Catherine,

111

2017). The genus Microcystis is the main producer; however, MCs are produced by several

112

planktonic and benthic biofilm-forming genera such as Anabaena, Phormidium,

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Planktothrix,

114

Cylindrospermopsis, Fischerella, Hapalosiphon, Lyngbya, Oscillatoria, Rivularia,

115

Synechocystis, and Synechococcus (Codd et al., 2005). Despite the limited knowledge on

Nostoc,

Limnothrix,

Anabaenopsis,

Aphanocapsa,

Aphanizomenon,

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their ecophysiological role, there are environmental factors such as cell growth rate,

117

competition, predation, temperature, salinity, light, water flow and nutrient concentrations,

118

which trigger or stimulate the biosynthesis of these secondary metabolites (Merel et al.,

119

2013).

120

Once absorbed or consumed, MCs are accumulated in the tissues of aquatic

121

organisms, binding covalently to target molecules such as phosphatase proteins, glutathion

122

or cysteine (Zhang et al., 2010). The MCs have an inhibitory effect on the enzymes serine

123

and threonine, responsible for catalyzing phosphorylation, critical in homeostasis and

124

regulation of cytoskeleton organization in cells (Zanchett and Oliveira-Filho, 2013; Chen et

125

al., 2016). MCs are resistant to degradation, even at temperatures above 300°C

126

(Wannemacher, 1989). Cooking promotes the bioavailability of MCs in foods by

127

weakening these bonds, thus increasing the risk to human health (Morais et al., 2008;

128

Zhang et al., 2010). Different toxic secondary metabolites produced by cyanobacteria are

129

known to accumulate in the viscera and muscles of Oreochromis niloticus, the route to

130

human exposure to cyanotoxins (Guzmán-Guillén et al., 2017). In addition to toxic

131

compounds, fish which have been in contact with cyanobacteria have low nutritional

132

quality and do not taste good, because of the absorption of geosmin and 2-methylisoborneol

133

produced by cyanobacteria (Vallod et al., 2007; Liang et al., 2015). The main symptoms of

134

microcystin poisoning are gastroenteritis, skin irritations, liver diseases including liver

135

necrosis, cancer and eventually death (Fontanillo and Kohn, 2018).

136

The zooplankton community structure is influenced by several factors, important

137

among them are the quantity and quality of the available food source (Müller-Solger et al.,

138

2002). Bloom forming cyanobacteria are considered to be poor diets for filter feeders (Paes

139

et al., 2016), affecting the energy transfer from primary production towards higher levels.

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Cladocerans and rotifers compete for food; however, any environmental factor that alters

141

the cladoceran populations more than the rotifers will be reflected in shifts in favor of the

142

latter (Gilbert, 1990). Low densities of large grazers such as cladocerans and high densities

143

of rotifers are common during cyanobacterial blooms (Haney, 1987). There are three main

144

ways in which cyanobacteria affect zooplankton: (1) The production of toxic secondary

145

metabolites, causing lethal or sub-lethal effects when ingested by zooplankton (Tõnno et al.

146

2016). (2) Low nutritional quality, due to their deficiency in fatty acids such as EPA, DHA,

147

Omega 3, vital to regulate their cellular functions (Gulati and DeMott, 1997; Müller-

148

Navarra et al., 2000) and (3) Colonies or filament aggregates, turn cyanobacteria into

149

inedible particles due to their large size which promotes clogging of food collecting

150

appendages (Gliwicz and Lampert, 1990).

151

Mexico has an annual fish production of 1.7 million tons from the fishing and

152

aquaculture sectors; and the average of consumption per person is around 12 kg year-1

153

(CONAPESCA, 2016). Carps and Tilapia, the most commonly produced fish in

154

aquaculture practices globally, feed on phytoplankton including cyanobacteria and detritus

155

(Jhingran, 1995). The tropical omnivorous species Oreochromis niloticus, constitutes up to

156

80% of the total production (FAO, 2010). This species was introduced in Mexico in 1964

157

and currently, close to 128 thousand tons for human consumption (SAGARPA, 2016) are

158

produced annually. Oreochromis niloticus has the capacity to ingest and digest toxic

159

cyanobacteria (Semyalo et al., 2011). It has even been suggested for use in bioremediation

160

due to its capacity to reduce harmful algal populations (Lu et al., 2006). Nevertheless,

161

omnivorous fish can also promote cyanobacterial blooms by altering the trophic state of the

162

systems, removing sediments while searching for food and thus releasing nutrients in the

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water column through bioturbation (Cline et al., 1994; Adamek and Marsalek, 2013), or by

164

icthyoeutrophication through ingestion, digestion and excretion of macrophytes

165

(Opuszyński, 1980).

166

Chirostoma, commonly known as the silverside, is found mainly Central Mexico.

167

This genus has about 25 endemic species (Navarrete-Salgado, 2017). Chirostoma jordani

168

has been widely consumed since pre-Hispanic times, and due to its high protein content

169

(74% g / 100 g), minerals, lipids and carbohydrates, it is considered as a high nutritional

170

value food (Melo-Ruiz et al., 2014). Chirostoma adults (>5 cm) are marketed dried or

171

fresh. The maximum production of silverside or “charal” was reached in 2016 (>12

172

thousand tons) (Navarrete-Salgado, 2017). This was from capture from lakes with high

173

densities of cyanobacteria (Dzul-Caamal et al., 2014). Chirostoma is also common in Lake

174

Zumpango and forms an important part of the diet of local communities around the lake.

175

Lake Zumpango in the State of Mexico, our study site, provides water for irrigation

176

and fish, mostly Tilapia and Chirostoma, production. The aim of this work was to evaluate

177

the seasonal changes in microcystin production over a year, and accumulation in two

178

trophic levels, the primary and secondary consumers in Lake Zumpango. Chronic exposure

179

to microcystins which are known to bioaccumulate in aquatic produce and cultivated crops

180

is a health concern. We also present information about how changes in microcystin

181

concentrations affect abundances of the dominant zooplankton taxa and shifts in

182

zooplankton community structure.

183 184

2. Materials and methods

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2.1. Study area

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The shallow lake (1.2 to 3.8 m) of Zumpango is located between the municipalities

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Zumpango de Ocampo and Teoloyucan, both in the State of Mexico at 19° 48’ N and 99°

188

06’ W (Fig. 1). It is a high altitude reservoir (2250 m above sea level), with a water storage

189

capacity of 100 x106 m3 and an area of 20 km2. Together with Xochimilco, Texcoco,

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Chalco and Xaltocán, Zumpango once formed part of the ancient lacustrine system in

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Mexico City. Ever since 1976, this lake is being refilled with partially treated waste water

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from the Santo Tomás Canal and Cuautitlán River. Nowadays, water from this lake is used

193

for irrigation, fishing (Oreochromis niloticus and Chirostoma jordani) and for recreation. A

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persistent cyanobacterial bloom exists throughout the year, dominated mainly by

195

Planktrothrix. Vasconcelos et al. (2010) report that 97% of the phytoplankton is

196

represented by high densities of cyanobacteria (1.4 x 106 cells ml-1) with genes involved in

197

microcystin production (mcyA, mcyB, mcyE and mcyE/ndaf), with microcystin

198

concentrations > 60 μg L-1 in the cells). We present here information on bioaccumulation

199

in samples of fish collected from site 1 (Fig. 1) where an aquaculture farm is being planned

200

by the government for the local population. In all, we had 63 samples over a period of one

201

year (12 water samples, 12 seston samples, 9 individuals of tilapia and 30 individuals of the

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mesa silverside).

203

The following physical and chemical variables were measured: dissolved oxygen

204

using an YSI 55 oxygen meter, water temperature, pH and conductivity using a

205

Conductronic meter, bicarbonates, hardness and chlorophyll a following standard

206

techniques (Clesceri et al., 1988) and nitrogen and phosphorus using a YSI 9000 kit.

207 208

2.2. Estimation of the concentration of microcystins in the seston and water

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To analyze diluted and particulate microcystin concentrations in the seston and water, we

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collected one liter of surface water every month (April 2016- March 2017) from Lake

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Zumpango. The samples were stored in dark bottles to prevent cyanotoxin degradation and

212

a subsample was immediately preserved in 3% formalin to identify and quantify the

213

cyanobacteria. Samples (revised to remove large particles such as zooplankton) were

214

filtered through pre-weighed and dried GF/C filters (pore opening 1.2 μm). Microcystins

215

from particulate samples were extracted from the filters (dried for 24 h at 45°C) using 75%

216

methanol after which they were mechanically homogenized and sonicated for 10 min at 20

217

kHz (Model: CP 130PB-1, Cole-Palmer Instruments). The organic solvent was then

218

eliminated by evaporation (Rotary evaporator) and the extract was suspended in distilled

219

water, centrifuged and filtered. Both, microcystins in water and that extracted from the cells

220

were measured by immunochemical ELISA kits with a detection range from 0.16 to 2.5 ppb

221

following Fastner et al. (1998) with modifications. Microcystin contained in cells are

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reported as μg g-1 (Ferrão-Filho et al., 2002):

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Content in seston µg g-1 = (MCs extracted µg L-1) / (Weight of seston g L-1)

224

2.3. Bioaccumulation in Zooplankton

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Microcystins were extracted from zooplankton samples collected monthly from April 2016

226

to March 2017. Lake surface water (600 L) (50 cm of the water column) was filtered

227

through a plankton net of 50 μm mesh size, a subsample was concentrated to 50 ml and

228

fixed in 4% formalin for identification and quantification. To avoid contamination or

229

overestimation of microcystin concentrations due to the presence of phytoplankton, the

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collected zooplankton was filtered and washed repeatedly with distilled water using a 250

231

μm mesh and observed under a stereoscopic microscope (Nikon SMZ 645) until the sample

232

was free of any cyanobacteria. Finally, zooplankton was placed in EPA medium

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(Environmental Protection Agency moderately hard water) and maintained for 1.5 hour to

234

allow cyanobacteria excretion from gut. The zooplankton biomass was passed onto a pre-

235

weighed glass fiber filter (GF/C) and kept in an oven for 24 h at 45°C to dry. Microcystin

236

extraction from the tissues in the filters were carried out adding 20 ml of 75% methanol,

237

mechanically homogenizing using a homogenizer (IKA, Ultra-Turrax) for 10 minutes and

238

then centrifuged at 3000 rpm to eliminate debris (El Ghazali et al., 2010). To remove the

239

solvent, the supernatant was placed into rotary evaporator at 50°C (the process was

240

repeated three times), the extract was re-suspended in distilled water and the microcystin

241

concentrations were quantified using ELISA kits (Envirologix).

242

2.4. Density and identification of zooplankton

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For identification of zooplankton we used specialized keys (Korovochinsky and Smirnov,

244

1998; Dussart and Defaye, 2001). Quantitative analysis of the zooplankton was carried out

245

using a counting cell chamber of clear glass, transected with 20 ml of capacity. Three

246

aliquots of 5 mL for each sample were analyzed using a stereoscopic microscope at 40×

247

magnification.

248

2.5. Bioaccumulation in fish

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Common Tilapia (Oreochromis niloticus) and mesa silverside (Chirostoma jordani) fish

250

(species consumed locally in small markets around the lake) were captured with a cast net

251

and kept at 4 ± 1°C) until transported to the laboratory, where the size and weight of the

252

organisms were recorded. Microcystins accumulated in tissues of Tilapia were extracted

253

from the pre-weighed livers, kidneys, intestines and muscles of nine fish captured in April,

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October and February (three per month), and 30 mesa silverside caught in April, June,

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August, October, December and February (five per month). This was done using 75%

256

methanol for extraction and mechanical homogenization for 30 min. Tissues were

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centrifuged at 3000 rpm for 15 min, and the resulting supernatant was passed through GF/C

258

filters. The filtrate was placed into a rotary evaporator set at 45°C (repeated 3 times,

259

decanting each time in the same flask). The extract was suspended in distilled water,

260

centrifuged and filtered for a second time to completely eliminate the particulate matter.

261

Microcystin concentrations were quantified using the ELISA immunological kit (EL

262

Ghazali et al., 2010). Accumulated microcystin in zooplankton and fish were reported as μg

263

g-1 and μg Kg-1.

264

Content in tissue in ng/g =

(MCs extracted ng/ml ) X (Extracted volumen ml) (Weight of tissue g)

265

2.6. Statistical analyses

266

Sigma Plot 11. Were used to analyze statistically Pearson´s correlation to detect relations

267

among measured variables.

268

3. Results

269

3.1. Physico-chemical characteristics and species abundances

270

The physical and chemical variables during the study period were as follows: the dissolved

271

oxygen concentrations ranged from 3.5 to 11.7 mg L-1; for 9 of the 12 months the water

272

was well saturated with concentrations above 8 mg L-1. Water temperature ranged from 16

273

to 24 °C with a mean of 20.3 °C. The pH was alkaline during the entire period (8.5-9.8).

274

Range of conductivity was from 415 to 631 µS cm-1 with a single peak of 810 µS cm-1 in

275

January. Bicarbonates ranged between 70 to 197 mg L-1 and hardness between 88 to 160

276

mg L-1, except in October and November. Lake Zumpango is hypertrophic with total

277

dissolved phosphate levels from 0.85 to 3 mg L-1 and nitrate concentrations between 9-28

278

mg L-1; the latter was less than 5 mg L-1 only in April, August and October. In accordance

279

with the high levels of nutrients (TN/TP = 0.53-15.88 with a mean of 4.77), the primary

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production was also very high; chlorophyll a was between 48 and 537 µg L-1 with an

281

exceptionally high value of 1462 µg L-1 with a Microcystis bloom in October. The Secchi

282

depth value was about 25 cm during the study period which is 10% of the total depth (~ 200

283

cm).

284

The phytoplankton was dominated by Planktothrix agardhii, Microcystis sp.,

285

Cylindrospermopsis raciborskii and Dolichospermum planctonicum (Table 1). and the

286

zooplankton by Acanthocyclops americanus copepodites, Daphnia laevis and Bosmina

287

longirostris (Table 1). The lake had more than 20 species of rotifers, five of cladocerans

288

and two copepods. The highest zooplankton density of Daphnia laevis (>560 Ind L-1) was

289

observed in May.

290

During the study period the dominant zooplankton taxa were copepods and

291

cladocerans; D. laevis and Acanthocyclops were present throughout the year (Fig. 2). Adult

292

Acanthocyclops densities were between 2 to 5 Ind L-1 during most months; on the other

293

hand, the density of the calanoid, Mastigodiaptomus peaked in October but was less than 1

294

Ind L-1 during the rest of the year. Moina macrocopa densities were between 2 to 5 Ind L-

295

1during

296

1)

297

Daphnia also reached very high densities (100 to 600 Ind L-1) in May and then from

298

October to March.

most of the year whereas Ceriodaphnia dubia reached its highest density (15 Ind L-

in November and December but was less than 1 Ind L-1 during the rest of the period.

299

With regard to the total abundances, Acanthocyclops americanus copepodites

300

dominated the system, followed by Daphnia laevis and Bosmina longirostris. The highest

301

abundance of zooplankton (968 Ind L-1) was found in May. In August there was a drastic

302

decrease of organisms in the lake, below 1 Ind L-1. High densities of Acanthocyclops

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americanus copepodites were observed in May (307) and March (450 Ind L-1); Bosmina

304

longirostris was most abundant in October (250 Ind L-1).

305

3.2. Concentration of microcystins

306

Concentrations of microcystin equivalents were recorded in all samples (n= 63). In spite of

307

the high concentrations of cyanotoxins, we found a decrease in the concentration at higher

308

trophic levels (seston> zooplankton>fish) (Fig. 3).

309

The concentrations of microcystin equivalents in Lake Zumpango, over the year,

310

ranged from 0.10 to 1.4 μg L-1. The concentrations of these secondary metabolites were

311

highest in the end of raining season in October (1.48 μg L-1), and the lowest concentration

312

of these toxic compounds (0.10 μg L-1) was observed in June. On an average, the annual

313

concentration was 0.33 μg L-1. The highest level of microcystin in the seston was found in

314

October and December (34.13 and 27.13 μg L-1, respectively). During the rest of the study

315

period the concentrations were < 20 μg L-1. From February to September there was a lower

316

production of cyanotoxins (average 3.15 μg L-1) than from October to January (Fig. 3).

317

The highest concentration of microcystins accumulated by the zooplankton was

318

associated with the lowest total abundance and vice-versa, although the correlation was not

319

statistically significant (P= -0.435) (Fig. 4). The accumulation of cyanotoxins was lowest in

320

May (0.070 μg g-1), the month with the highest zooplankton abundance (968 Ind L-1).

321

Highest accumulation in the zooplankton was in October and December (0.29 and 0.28 μg

322

g-1), but the total zooplankton abundance was < 300 and 105 Ind L-1, respectively. There

323

was an annual average accumulation of 0.15 μg g-1 in the zooplankton, which could move

324

to the next trophic level. There was a positive correlation between microcystin accumulated

325

in the seston with the content in zooplankton both tending to increase together (P= 0.01).

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We found an accumulation of cyanotoxins in the different organs and tissues of

327

Oreochromis niloticus. The highest microcystin concentrations were detected in the liver

328

(9.6 μg Kg-1) followed by the intestine of the fish (6.0 μg Kg-1) (Fig. 5).

329

In Chirostoma jordani, microcystin concentrations in the whole body ranged from

330

5.05 to 24.02 μg Kg-1 dry weight (DW) or 1.5 to 7.27 μg Kg-1 wet weight (WW). The

331

concentration of these secondary metabolites was highest in October and December with an

332

average of 6.65 and 7.22 μg Kg-1 DW or 0.076 and 0.059 μg Kg-1 WW, respectively (Fig.

333

6). From April to August there was a decrease in the accumulated cyanotoxin

334

concentrations which ranged from 2.53 to 3.72 DW. All the fish analyzed had

335

concentrations above the maximum permissible limit. For example, when orally

336

administered, microcystin at dose of 5 mg Kg-1 causes 50% mortality to rodents (Falconer,

337

2005). On the other hand, daily intake of microcystin at 0.04 μg Kg-1 is tolerable to humans

338

as set by the World Health Organization.

339

4. Discussion

340

The concentrations of microcystins in the lake water ranged from 0.1 to 1.4 μg L-1; except

341

in October when the values did not exceed the 1 μg L-1 limit established by WHO for

342

drinking water, and were in the range observed in other Mexican water bodies such as Lake

343

Texcoco (0.20 to 2.4 μg L-1) (Barrios et al., 2017), Valle de Bravo Reservoir (0.5 to 5.56 μg

344

L-1) (Alillo-Sánchez et al., 2014) and Lake Pátzcuaro (0.16 to 0.19 μg L-1) (Berry et al.,

345

2011). Lethal doses for small mammals, reported by Falconer (2005), are higher than lethal

346

concentrations. We have used lethal concentrations here, since we are not sure of the actual

347

intake of toxins by aquatic organisms.

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The concentrations of microcystins in the seston and dissolved in the water in this

349

study are positively related, both increased together. This was also found by Romo et al.

350

(2012), where in this relationship, the seston had up to a ten-fold higher microcystin

351

concentration than the water. With the exception of Cylindrospermopsis raciborskii, which

352

has the capability to exude secondary metabolites (Figueredo et al., 2007), this is due to the

353

fact, that cyanotoxins are endotoxins and are only released when the cell membrane is

354

ruptured. However, even during the exponential growth phase, lysis has been documented

355

due to decomposition (Watanabe et al., 1992). Chemical contaminants also promote the

356

release of cyanotoxins from cells (Dai et al., 2016).

357

Particulate fractions were found in the range of 0.94 to 34.13 μg L-1, with an

358

accumulation in seston ranging from 2.51 to 117.68 μg g-1 DW. These concentrations are

359

lower compared to those reported by Ferrão-Filho et al. (2002), in two stations of

360

Jacarepagua Lagoon, where they found concentrations ranging from undetectable to >120

361

μg L-1 with accumulation values from undetectable to 0.0058 μg g-1. Microcystins detected

362

in seston from Mexican water bodies range from 4.9 to 78 μg L-1 (Vasconcelos et al.,

363

2010). In the seston of Lake Zumpango the concentration was 62.4 μg L-1, 46% more than

364

the highest concentration detected during their study in Lake Zumpango by Vasconcelos et

365

al. (2010).

366

Zooplankton often act as vectors since during blooms they are forced to consume

367

toxic cyanobacteria, encapsulating the cyanotoxins which then reach higher trophic levels

368

(Sotton et al., 2014). Zooplankton often have the highest concentrations of cyanotoxins in

369

relation to their biomass (> 1300 μg g-1) (Ibelings et al., 2005) and the only group where

370

biomagnification has been clearly demonstrated (Kozlowsky-Suzuki et al., 2012). The

371

microcystin concentrations contained in the zooplankton from Zumpango (0.007 to ~ 0.3

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372

μg g-1) were orders of magnitude lower than the average value of 383 μg g-1 reported by

373

Ferrão-Filho and Kozlowsky-Suzuki (2011) and Pham and Utsumi (2018). This is probably

374

due to the fact that the aforementioned studies included large (> 3.5 mm), generalist, filter

375

feeders such as Daphnia while in Lake Zumpango, the average body size of the cladocerans

376

is < 1 mm and these species do not feed well on cyanobacteria (Tõnno et al., 2016).

377

The main zooplankton contributing to the total abundance were Acanthocyclops

378

americanus copepodites, Daphnia laevis and Bosmina longirostris. The first two taxa have

379

a high production of antioxidant enzymes such as glutathione-s-transferase and catalases,

380

increasing their detoxification capacity of cyanotoxins (Kozlowsky-Suzuki et al., 2009,

381

Ferrão-Filho et al., 2017). Further studies are needed to explain the sensitivities of different

382

zooplankton species to cyanotoxins; Simocephalus sp., Moina macrocopa and ostracods

383

often tolerate these metabolites better (Nandini and Rao, 1998; Fernandez et al., 2016) than

384

several other species. Agrawal et al. (2001) have shown that the sensitivity of Moina

385

macrocopa to microcystins is due to an inhibition of proteases; it is likely that differences

386

in the sensitivity of cladocerans is directly related to the effect of microcystins on

387

enzymatic activities in cladocerans. Daphnia laevis, as shown in field observations and

388

laboratory experiments, is capable of coexisting with Microcystis sp., although the poor

389

nutritional quality of this diet results in poor reproduction and fluctuating populations

390

(Nandini et al., 2000; Pinto-Coehlo et al., 2003). It has been suggested that the ability of

391

Bosmina to withstand cyanobacteria is due to their ability to feed selectively and thus

392

eliminate toxic cyanobacteria from their diet (DeMott, 1986).

393

In general, the bioaccumulation pattern in fish depends on their mode of feeding as

394

follows zooplanktivores
395

et al., 2012). Here too we observed similar trends, in that the omnivorous Oreochromis had

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396

lower levels of microcystins than the zooplanktivorous Chirostoma. Most studies show that

397

bioaccumulation is more in the viscera and liver as compared with the muscle (Romo et al.,

398

2012) while others indicate the opposite trends (Hauser-Davis et al., 2015). Here we found

399

that the concentration of microcystins was lowest in the muscle; the liver had around 12.5%

400

(μg Kg-1) more and the intestines, 6.5% (μg Kg-1) in Oreochromis. Palikova et al. (2011)

401

show that Oreocrhomis niloticus accumulated up to 350 μg Kg-1 of microcystins in the

402

hepatopancreas and unlike the carps which can eliminate all the cyanotoxins after 2 weeks

403

(Adamovský et al., 2007), and thus they do not thereby increase the risk to consumers. The

404

concentrations detected in muscle in various studies are in a range of 0.065 μg Kg-1 (Prieto

405

et al., 2007) to 102 μg Kg-1 (Mohamed et al., 2003). In the fish we evaluated in February

406

and April, the concentrations in this edible tissue are 0.42 and 0.49 μg Kg-1, which could be

407

related to the low concentration of microcystins in the seston during this season.

408

Even a low concentration and accumulation of microcystins can have an adverse

409

effect on humans and animals. The main symptoms of microcystin poisoning are

410

gastroenteritis, irritations, liver diseases including liver necrosis, cancer and eventually

411

death (Fontanillo and Kohn, 2018). Avoiding the consumption of liver and other viscera of

412

fish does help but not cooking the fish muscle. MCs are stable molecules even at high

413

temperatures (above 300°C) (Wannemacher, 1989). In the case of Oreochromis niloticus it

414

has been shown that the cooked tissues reduce microcystin concetrations by 25% in

415

microwaves and 50% by boiling, for a period of 5 min. However, when fish tissues are

416

boiled, microcystins are transferred to the water (Guzman-Guillen et al., 2011) and there is

417

a weakening of the covalent bonds in the target molecules such as the phosphatase proteins,

418

Glutathion or Cysteine (Zhang et al., 2010), and an increased risk to human health (Morais

419

et al., 2008; Zhang et al., 2010). In addition to toxic compounds, fish which have been in

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420

contact with cyanobacteria have low nutritional quality and do not taste good as do fish in

421

contact with sediments, because of Geosmin and 2-Methylisoborneol production (Vallod et

422

al. 2007; Varga et al. 2013; Liang et al. 2015).

423

The aetherinid, Chirostoma is endemic to the central region of Mexico. It has a

424

great cultural importance in the diet of Mexicans. Chirostoma sp. from Lake Pátzcuaro,

425

accumulated MCs at concentrations <18 μg Kg-1 DW (Berry et al., 2011). This is the first

426

report on MCs in Chirostoma jordani, with the highest concentrations between 22 and 24

427

μg Kg-1 DW in October to December, after the rains and a decomposition of the

428

Microcystis blooms. It is evident that unlike certain other fish taxa, Chirostoma does not

429

have good detoxification capacity of MCs. Jia et al. (2014) show that small-sized fish tend

430

to accumulate greater concentration of microcystins in their kidney or heart, because

431

biotransformation and excretion is not as developed¸ compared to large fish.

432

In order to protect consumers, WHO (1998) has established a TDI value of 0.04 µg

433

Kg-1 d-1 for products exposed to microcystins-LR (Chorus and Bartram, 1999), according to

434

the regulations of the Environmental Protection Agency (EPA) the permissible limits are

435

more than an order of magnitude lower; chronic consumption (0.003 µg Kg-1 d-1) or

436

occasional consumption (0.006 µg Kg-1 d-1) (Catherine et al., 2017) (Fig. 7). Assuming that

437

a person (60 Kg), consumes about 200 g (DW) of Chirostoma daily especially from

438

October to December, the average daily consumption is 1.8 and 2.0 times higher than the

439

TDI value. However, considering the average weight of a child, between 2 to 5 years of age

440

(13.77 Kg WHO, 2018) and a consumption of 1/4 (50 g) of an adult, the risk is even

441

greater. At these permissible limits consuming Chirostoma jordani is a risk throughout the

442

year but Oreocrhomis niloticus only in winter when the concentrations are < 0.006 µg Kg-1

443

d-1.

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444

5. Conclusions

445

Our study clearly indicates that high densities of Microcystis, and perhaps other

446

cyanobacterial blooms result in high concentrations of microcystins in the lake ecosystem

447

and thereafter in the zooplankton and fish. This poses a risk to the local community which

448

consumes small species such as Chirostoma whole and raw (dried). Larger species,

449

especially tilapia is not much affected and is a better dietary option, although local

450

populations prefer Chirostoma. Since aquaculture products are an important source of

451

protein in Mexico and many waterbodies harbour high densities of cyanobacteria, we

452

would like to emphasize the urgency to conduct similar studies in other states in Mexico.

453 454

6. Acknowledgements: The first author thanks Posgrado en Ciencias del Mar y Limnología

455

(UNAM) and CONACyT (189194) for financial support. SN and SSSS thank PAPIIT

456

(UNAM) (219218) for a research grant and CONACyT (20520 and 18723) for financial

457

assistance. We thank three anonymous reviewers whose constructive criticism helped

458

improve the manuscript. Mónica Chico Avelino and Sarai M. Zamora Barrios helped

459

prepare the map of Zumpango Lake and the graphical abstract, respectively. We thank

460

Marcelo Silva-Briano for confirming the identification of Daphnia laevis.

461 462

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804

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805

Figure legends:

806

Fig. 1. Map of the study site, Lake Zumpango. Arrow points north.

807

Fig. 2. Population densities of selected zooplankton taxa during the study period.

808

Fig. 3. Microcystin concentrations, diluted in water (solid line and triangles) and seston

809

(dotted line and circles) from Lake Zumpango, over a one year.

810

Fig. 4. Annual concentrations of accumulated microcystins by zooplankton against total

811

abundances.

812

Fig. 5 Microcystin concentrations in tissue (muscle) and organs (liver, intestine and gills) of

813

Oreochromis niloticus, in April, October and February months.

814

Fig. 6 Concentrations of microcystins accumulated in whole body in Chirostoma jordani

815

from Lake Zumpango.

816

Fig. 7 Permitted consumption of microcystins in relation to concentrations in fish,

817

Chirostoma (Chr) and Oreochromis (Ore).

818

ACCEPTED MANUSCRIPT

819 820

Table 1. Cyanobacterial abundance (ind. ml-1) in Lake Zumpango over one year (April 2016 to March 2017). * Single cells.

821 Species

Apr

May

Jun

Jul

Aug

Sep

Oct

Nov

Dec

Jan

Feb

Mar

Planktothrix sp.

32,355

36,735

33,975

26,280

15,236

18,135

17,910

24,045

18,135

24,720

25,035

16,365

Microcystis sp.

165

162

225

195

540

195

26,940

2,445

2,610

2,115

120

105

255

75

255

1,035

975

18.83 X 106* Aphanizomenon sp.

30

2,295

1,995

1,7580

7,095

2,910

Cylindrospermopsis sp.

302

390

16,650

32,040

521

75

60

150.3

2,220

330

75

45

63

285

15

63

555

Raphidiopsis sp.

330

360

49.5

30

Anabaenopsis elenkinii

54

Pseudoanabaena mucicola Dolichospermum planctonicum Dolichospermum sp.

Merismopedia sp.

822 823

1005

330

1,380

30

105

32

30

60 33 90.6

14

195

ACCEPTED MANUSCRIPT

824 825 826 827 828

Fig. 1

ACCEPTED MANUSCRIPT

600

Daphnia sp.

500

500

400

400

400

300

300

300

200

200

200

100

100

100

0

0

0

Asplancha sieboldii

50

M. albuquerquensis Copepodites

50

40

40

40

30

30

30

20

20

20

10

10

10

0

0

0

20

Moina micrura

20

M. albuquerquensis Male

20

15

15

15

10

10

10

5

5

5

0

0

0

10

A. americanus Female

10

A. americanus Male

829

Fig. 2

10 8

6

6

6

4

4

4

2

2

2

0

0

0

Apr May Jun Jul Aug Sep Oct Nov Dec Jan Feb Mar

8

Apr May Jun Jul Aug Sep Oct Nov Dec Jan Feb Mar

8

Time (moths)

830

600

500

50

Densities (Ind L-1)

A. americanus Copepodites

B. longirostris

C. dubia

M. albuquerquensis Female

Nauplii

Apr May Jun Jul Aug Sep Oct Nov Dec Jan Feb Mar

600

ACCEPTED MANUSCRIPT

Water Seston

3

30

2

20

1

10

0

0

Microcystins (µg g-1)

140

Accumulated

120 100 80 60 40 20

832

Ju l Au g Se p Oc t No v De c Ja n Fe b M ar

Ap r M ay Ju n

0 Time (months)

831

Fig. 3.

40 Microcystins (µg L-1)

Microcystins (µg L-1)

4

ACCEPTED MANUSCRIPT

Microcystin concentrations in zooplankton

0.30

833 834

Fig. 4

1200 1000

0.25

800

0.20

600

0.15

400

0.10 0.05

200

0.00

0

Total abundances (Ind L-1)

Accumulation Abundances

Ap r M ay Ju n Ju l Au g Se p Oc t No v De c Ja n Fe b M ar

Microcystins (µg g-1)

0.35

ACCEPTED MANUSCRIPT

Oreochromis niloticus 16

October

14 12 10 8 6 4 2

Microcystins (µg Kg-1)

0

Liver Intestine

Gills

Muscle

April

16 14 12 10 8 6 4 2 0

16

Liver Intestine

Gills

Muscle

February

14 12 10 8 6 4 2 0

835 836

Fig. 5

Liver Intestine

Gills

Muscle

ACCEPTED MANUSCRIPT

Microcystin concentrations in Chirostoma jordani

Microcystins (µg K-1)

35 Wet weight Dry weight

30 25 20 15 10 5

837 838 839

Fig. 6

Fe b

De c

Oc t

Au g

Ju n

Ap r

0

ACCEPTED MANUSCRIPT

0.10

0.08

0.06

0.04

(WHO)

0.02 (EPA ACUTE) (EPA CHRONIC)

0.00 Ap rC hr Ju nC Au hr gC hr O ct -C hr D ec -C hr Fe bC h Ap r rO re O ct -O Fe re bO re

Daily consumption (µg Kg-1 bw d-1)

840

Fish date

841 842 843 844 845

Fig. 7