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Diatoms as bioindicators of pollution in the Mantaro River, Central Andes,

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DOI: 10.1504/IJENVH.2008.018674

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82 Int. J. Environment and Health, Vol. 2, No. 1, 2008

Diatoms as bioindicators of pollution in the Mantaro

River, Central Andes, Peru

Pedro M. Tapia
Universidad Peruana Cayetano Heredia,
Biological Sciences Department – LID,
Lab. Palynology and Paleobotany
Av. Honorio Delgado 430, Lima 31, Peru
E-mail: [email protected]

Instituto del Mar del Perú (IMARPE),

Marine Geology Lab.,
Av. Gamarra and Gral. Valle, s/n,
Chucuito, Callao, Peru

Abstract: Semi-quantitative analysis of two algal samples from the

Mantaro River taken few kilometres downstream from La Oroya city at
Junin, Peru, contained both organic-pollution tolerant and morphologically
abnormal diatom associations. The organic pollution is inferred by elevated
percentages of Nitzschia palea, Gomphonema parvulum and the Achnanthidium
minutissimum complex; the total assemblage indicates an oligosaprobic to
α-mesosaprobic status. A distinctive subset of diatom valves shows abnormal
outline morphology and ornamentation deformities in several individuals
of the species Achnanthidium macrocephalum, Cymbella hustedtii, Diatoma
moniliformis, Encyonema silesiacum, Surirella minuta, Synedra acus, Synedra
rumpens, Synedra ulna and Synedra vaucheriae. Abnormal diatom
ornamentation and morphology is usually associated to elevated concentration
of heavy metals (Cr, Cd, Cu, Zn, Sr) in aquatic ecosystems. Therefore, the
Mantaro River at this site contained a low water quality based on diatom
bioindicators of organic and heavy metal pollution.

Keywords: deformed morphology; diatoms; bioindicator; heavy metal; organic

pollution; water quality; Mantaro River; La Oroya; Central Andes; Peru.

Reference to this paper should be made as follows: Tapia, P.M. (2008)

‘Diatoms as bioindicators of pollution in the Mantaro River, Central Andes,
Peru’, Int. J. Environment and Health, Vol. 2, No. 1, pp.82–91.

Biographical notes: Pedro Tapia holds his PhD in Geosciences from the
University of Nebraska at Lincoln, USA, and has studied modern and fossil
diatoms from the Peruvian coast and Central Andes for the past 15 years. He
is also interested in diatom applications to assess aquatic ecosystem health
and the use of diatoms in paleoclimate reconstructions from both marine and
lacustrine environments.

Copyright © 2008 Inderscience Enterprises Ltd.

 Diatoms as bioindicators of pollution in Mantaro River 83

1 Introduction

Freshwater ecosystems respond to external factors such as climate, geological disasters

and human disturbances by adapting their basin geometry, morphology and biota to new
conditions. Water running along an altitudinal gradient permits a natural purification
of the stream allowing adequate oxygenation, consumption of dissolved nutrients, and
the sustainability and protection of a rich aquatic biota. Thus, any drastic change to the
aquatic ecosystem will threat the river health affecting both the aquatic organisms that
depend upon its water quality and all the ecological services which provides to man
(food, wood and water). Human-induced changes affect rivers and streams in the form of
dam constructions, canalisation, shoreline erosion, riparian clearing, agricultural runoff,
eutrophication, sewage discharge, and high loads of suspended sediments, heavy metals,
hydrocarbons and pesticides. When anthropogenic changes occur over long periods of
times, the result is a constant degradation of rivers and streams which overcomes the
ecosystem resilience against external changes.
Land occupation and cultural activities have a long history in the Central Peruvian
Andes. The town of La Oroya was created in 1681 under the name of San Jerónimo de
Callapampa but its local population gathered in this area for several millennia before
(Chuquimantari, 1985). La Oroya embodies the oldest polymetallic smelter in this region
whose operation began in 1922 and now mainly process Cu, Pb, Zn, Cd, Ag and Au.
Currently, airborne pollutants in La Oroya are PM10, Pb, SO2, Cd, As, Bi, Sb and Tl
(CONAM, 2007). The fate of this town, local residents, farmers and ranchers has been
swinging according to policies that sustained an economy based in metal concentration
but severely impaired environmental controls. Many years of continuous degradation on
terrestrial and aquatic ecosystems have left a strong imprint around the city over the hills,
soils, pastures, and riverine flora and fauna. Environmental degradation affected not only
native vegetation and animals but also has had a high toll in the 33,000 inhabitants
of La Oroya people (La Oroya, 2007). Many respiratory, dermal, allergic, cancer and
mental diseases have been observed in the local population from several years. Lead
concentration levels, three times higher than the maximum recommended by the World
Health Organization (WHO), were found in La Oroya children’s blood (DIGESA, 1999;
CDC, 2005), and now the town is considered one of the ten most polluted places on earth
(Blacksmith Institute, 2006).
Several environmental assessments applied diverse techniques to reveal the health
and degree of perturbation in soils and waters. One of the most reliable techniques to
assess water quality in river and stream is through the use of bioindicators, which are
sensible to ecological stressors. Diatoms (Bacillariophyta, single-cell aquatic siliceous
algae) are perhaps one of the most used bioindicators to assess water quality because (1)
their assemblages changes with different base-line environmental conditions; (2) they
integrate the whole suite of water pollutants; (3) they reproduce rapidly which indicates
ecological conditions from days to weeks; (4) the siliceous valve is resistant to organic
decay; and (5) with experience it is easy to identify them under the transmitted light
microscope (McCormick and Cairns, 1994).
This paper presents the results of a diatom-based rapid environmental assessment in
order to shed light on the water quality from Site 1 in the Mantaro River nearby the town
of La Oroya, Junin, Peru.
84 P.M. Tapia

2 Materials and methods

A brief environmental reconnaissance along the Mantaro River at about 10 km

downstream (Site 1) of the city of La Oroya, Junin, Peru (Figure 1), gives us the
opportunity to collect two algal samples to broadly estimate the river health at this
particular point. The water at this site had a brown colour, moderate discharge, turbulent
flow and carried out a fair amount of suspended particles. The boulders along the river
bank were black-stained and the stony flood bed contained scarce vegetation.

Figure 1 Site 1 in the Mantaro River, downstream from the city of La Oroya, Junin, Peru
(for colours see online version)

The collected algal samples were brought to the laboratory with no preserving elements.
Initial algal analysis was performed in a Zeiss, Axiostar Plus, Transmitted Light
Microscope with a CP-Achromat objective of 40× (NA = 0.65), for a total magnification
of 400×. A sub-sample was taken for diatom preparation; the frustules were treated with
HCl 10% and H2O2 30% to eliminate carbonates and the organic matter, respectively.
Permanent strewn slides were made with the clean material using Zrax® as a mounting
medium (RI = 1.73). Diatom analysis was performed with an oil CP-Achromat objective
of 100× (NA = 1.25) for a final magnification of 1000×. Semi-quantitative analyses were
performed identified a minimum of 500 valves per slide and then reported in percentage
of the total diatom community. Cosmopolitan, regional and local algal and diatom
floras were used to identify the taxa (Hustedt, 1930; Hustedt, 1930–1966; Manguin,
1964; Patrick and Reimer, 1966–1975; Germain, 1981; Servant-Vildary, 1986; Krammer
and Lange-Bertalot, 1991–2000; Lange-Bertalot et al., 1996; Rumrich et al., 2000). The
remaining raw samples were, then, fixed with formalin 4% for long-term storage.
Pollution-tolerant indicators were pooled following the concepts of Lange-Bertalot
(1979) and Kobayashi and Mayama (1989), whereas the saprobiological terms were
followed after Sládeček (1973). Separately, the total number of deformed diatom valves
from both samples were counted and reported as percentage of total counts.
 Diatoms as bioindicators of pollution in Mantaro River 85

3 Results

Environmental parameters at the studied site indicate cold, alkaline waters with moderate
amounts of electrolytes (Table 1). The initial assessment of the organisms present at both
river samples showed a low diversity of benthic flora and fauna indicated by the small
aquatic taxa richness (Table 2).

Table 1 Basic environmental parameters (single measurements) in site 1 of Mantaro River

near La Oroya, Junin, Peru

Parameter Values and units

Electrical conductivity 650 µS/cm
pH 8.2
Surface water temperature 8ºC
Latitude 11º38’49.1” S
Longitude 75º48’25.2” W, precision 10 m
Elevation 3606 m

Table 2 Generic-level, rapid hydrobiological assessment of the benthic algae and

microzoobenthos in the samples from the Mantaro River, Peru. Relative abundance
estimation: R = Rare, F = Few, C = Common, A = Abundant

Taxon group Surface sediment Epilithic

23.VI.07-1 23.VI.07-2
Bacillariophyta
Achnanthidium R R
Cymbella R –
Denticula R R
Fragilaria F R
Gomphonema R C
Naviculoids A C
Nitzschia F-C A
Synedra F F
Chlorophyta
Chlamydomonas R R
Cladophora F R
Scenedesmus R R
Cyanobacteria
Oscillatoria R R
Unidentified cyanophyte – R
Protozoa
Ciliate F R
Amoeba – R
Others
Nematoda R –
Rotifera R –
Taxa richness 15 14
86 P.M. Tapia

The surface sediment sample 23.VI.07-1 was taken from the edge of the river and
contained the filamentous green algae Cladophora. A microscopic observation showed
grain-sizes composed of fine quartz sand and clayey-silt embedded with organic matter.
Among the aquatic organisms, diatoms were the most abundant.
The epilithic sample 23.VI.07-2 was taken from pebble- and cobble-size rocks laid
over the river edge and scrubbed off over a plastic container. The sample contained mats
of slit, clay and organic matter; again the diatoms were the most diverse group among the
benthic taxa (Table 2).
As diatoms were the most conspicuous group in both samples, a special treatment was
performed and arranged accordingly to the tolerance of the organic pollution status and
the aberrant morphology they might present. Therefore, the diatom flora was segregated
in three groups: (a) saprobic (organic pollution tolerant), (b) morphologically aberrant
and (c) indifferent species (Figure 2, Table 3). This clearly shows that both saprobic
(46.5–64%) and abnormal (4.5–5.5%) forms are unusually high in the diatom assemblage
from both samples.

Figure 2 Percentage of abnormal, saprobic and indifferent diatom associations in surface

sediment and epilithic samples (n = 2) from Mantaro River near La Oroya, Junin, Peru

Table 3 Composition and relative abundance of diatoms from River Mantaro near La Oroya,
Junin, Peru

Surface
Diatoms – normal morphology sediment Epilithic Limnosaprobity
23.VI.07-1 23.VI.07-2
Achnanthidium macrocephalum (Hustedt) ND
Round and Bukhtiyarova (*) 10.5 2.1
Achnanthidium minutissimum (Kützing) o-β
Czarnecki (*) 4.7 9.1
Achnanthidium saprophilum (Kobayashi and o-β
Mayama) Round and Bukhtiyarova (*) 8.4 4.0
Caloneis sublinearis (Grunow) Krammer 25.3 2.3 ND
Cymbella hustedtii Krasske – 0.2 ND
 Diatoms as bioindicators of pollution in Mantaro River 87

Table 3 Composition and relative abundance of diatoms from River Mantaro near La Oroya,
Junin, Peru (continued)
Surface
Diatoms – normal morphology sediment Epilithic Limnosaprobity
23.VI.07-1 23.VI.07-2
Diatoma moniliformis Kützing 1.8 0.9 ND
Encyonema silesiacum (Bleisch) Mann 0.2 – ND
Encyonopsis falaisensis (Grunow) Krammer 0.4 – ND
Encyonopsis microcephala (Grunow) ND
Krammer – 0.4
Fistulifera saprophila (Lange-Bertalot and ND
Bonik) Lange-Bertalot (*) 0.2 0.4
Fragilaria capucina Dezmazières – 0.2 o-β
Fragilaria capucina var. capitellata o-β
(Grunow) Lange-Bertalot – 0.4
Gomphonema parvulum (Kützing) β
Kützing (*) 2.7 11.3
Navicula cari Ehrenberg 0.2 – ND
Navicula cryptocephala Kützing – 0.2 α
Nitzschia palea (Kützing) W. Smith (*) 20.0 37.2 α
Pinnularia kuetzingii Krammer 8.4 0.2 ND
Staurosira sp. 0.6 – ND
Surirella minuta Brébisson ex Kützing 1.2 0.4 ND
Synedra acus Kützing 1.6 0.6 β
Synedra goulardi Brébisson – 0.2 ND
Synedra rumpens Kützing 3.7 9.8 ND
Synedra tenera W.Smith – 1.5 ND
Synedra ulna (Nitzsch) Ehrenberg (*) 1.8 0.6 β
Synedra vaucheriae (Kützing) Kützing 2.9 13.8 β
Synedra sp. 0.2 – ND
Sub-total 1 94.6 95.5
Teratologic forms
Achnanthidium macrocephalum (Hustedt) ND
Round and Bukhtiyarova 1.4 0.6
Cymbella hustedtii Krasske 0.6 – ND
Diatoma moniliformis Kützing 0.2 – ND
Encyonema silesiacum (Bleisch) Mann – 0.2 ND
Surirella minuta Brébisson ex Kützing 0.2 – ND
Synedra acus Kützing 0.2 0.2 β
Synedra rumpens Kützing 2.3 3.0 ND
Synedra ulna (Nitzsch) Ehrenberg 0.6 – β
Synedra vaucheriae (Kützing) Kützing – 0.6 β
Sub-total 2 5.4 4.5
Total (%) 100 100
Note: Asterisks denote organic-tolerant diatom taxa. Saprobic terminology after
Sládecek (1973): o = oligosaprobity, β = beta-mesosaprobity, α = alpha-
mesosaprobity, ND = No data.
88 P.M. Tapia

We found two types of deformities in the diatom valves. One group has a deformed cell
outline (Achnanthidium minutissimum and allies, Cymbella hustedtii, Surirella minuta,
Synedra rumpens, S. ulna, S. vaucheriae), the other presents altered striation patterns
(Synedra goulardi, S. ulna) (Figure 3).

Figure 3 Diverse degree of deformed diatoms from Mantaro River near La Oroya, Junin, Peru.
1–3, 12 Synedra vaucheriae; 4, 10, 11 Synedra rumpens; 5 Surirella minuta; 6, 7
Synedra goulardi; 8, 9 Achnanthidium macrocephalum; 13 Cymbella hustedtii; 14
Synedra ulna. Not to a scale (for colours see online version)

In terms of their limnosaprobity (Sládeček, 1973), the taxa range from oligosaprobic to
(β, α)-mesosaprobic, in other terms, from moderate to highly polluted waters.

4 Discussion and conclusion

Morphological abnormalities in diatoms are rarely found in natural communities,

although these have been found associated to altered environments in polluted sites that
contained heavy metals (Morin et al., 2008).
The effect of heavy metals in diatoms has long been studied in marine sediments
(Absil and van Scheppingen, 1996; Dickman, 1998), lakes (Yang and Duthie, 1993;
 Diatoms as bioindicators of pollution in Mantaro River 89

Ruggiu et al., 1998), rivers (Nakanishi et al., 2004) and streams (Medley and Clements,
1998; Gómez and Licursi, 2003).
Copper, cadmium and mercury toxicity experiments show drastic reduction of diatom
biomass with exposure to higher heavy metal concentrations because these elements
affect its physiology (Masahito and Hashizume, 1972; Berland et al., 1977; Pistocchi et
al., 1997; Morin et al., 2008).
At the studied site, a small (up to 5.5%) but significant amount of morphologically
altered diatom valves might indicate that latent heavy metals in sediments and over
stones interact to diatom flora. Although there is not unequivocal proof of the later
statement yet, the close proximity of La Oroya smelter led us to hypothesise in that
direction.
Metal pollution is not the only cause for ecological degradation that affects algae in
continental ecosystems. Acid rain produced by air-borne sulphur dioxide from La Oroya
smelter affects both terrestrial and aquatic ecosystem alike. While is evident the loss of
farming soil and biodiversity of aquatic and terrestrial flora and fauna, the human
population is also affected by the long-term exposure of contaminants. Heavy metals as
Pb were found in household dust with concentration exceeding the international standards
(Cornejo and Gottesfeld, 2005). It is also disturbing that high contamination levels have
been reached in the La Oroya children, several of them over the WHO’s maximum
recommended level in blood samples (DIGESA, 1999; CDC, 2005). Other heavy metals
from the metallurgic operation could play an important role in the La Oroya people’s
health, although no public-health research has been conducted for other pollutants
than Pb. So, it is much indeed of required investigation in public health over aquatic and
terrestrial ecosystems to assess and remediate years of environmental deterioration and
negligence.
The low diversity in the algal samples contains few species but represents about the
70% of the diatom community in both samples: Nitzschia palea, Caloneis sublinearis, the
Achnanthidium minutissimum complex, Synedra ulna, Gomphonema parvulum, Synedra
rumpens and S. vaucheriae (Table 3). Most of these taxa are indicators of water quality
but also its high relative abundance can be influenced by other environmental stressors.
For example, the Achnanthidium minutissimum complex (including A. saprobicum and
A. macrocephalum) and Synedra vaucheriae have been reported growing in other heavy-
metal polluted streams (Rushforth et al., 1981; Medley and Clements, 1998) and lakes
(Ruggiu et al., 1998), but it is unclear if this development is due to the ability of taking
advantage of empty niches for being an early succession k-species or because they are
tolerant to metal pollution.
On the other hand, similar valve deformation in the benthic genera Fragilaria and
Synedra was also documented in streams impacted by mine drainage from Eagle River,
Colorado, Southern Rocky Mountains. A regression model between abnormal Fragilaria
valves and concentration of dissolved Cd, Cu, Fe and Zn suggests that the abundance of
deformed cells may be used as an indicator of elevated metal concentration in streams
(MacFarland et al., 1997).
A distinct organic-tolerant group is then encountered in this diatom community
indicating that a second type of pollution is affecting the water quality in the Mantaro
River. A large relative abundance of organic tolerant diatoms (up to 64%) in the samples
is a good indicator of organic pollution in the studied site. The release of elevated
amounts of waste waters and nutrients to the river stream made unhealthy the ecosystem
and thus inducing the river to a eutrophication state.
90 P.M. Tapia

In conclusion, the combination of diatom populations both tolerant to organic

pollution and abnormal morphology in the algal samples indicates a low water quality of
the Mantaro River at Site 1 (downstream the La Oroya town), most likely as a product of
raw domestic water discharge and metallurgic-derived heavy metals carried along the
stream.

Acknowledgments

I am grateful to Colin Cooke and William Hobbs from the Earth and Atmospheric
Science Department, University of Alberta at Edmonton, Canada for field support and
assistance. This is a contribution to the Environmental Science Section of the Biological
Science Department at the Cayetano Heredia Peruvian University in Lima, Peru.

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