algal assemblages and their relationship with water quality in tropical streams with different land...

7/27/2019 Algal Assemblages and Their Relationship With Water Quality in Tropical Streams With Different Land Uses 2011 G

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P R I M A R Y R E S E A R C H P A P E R

Algal assemblages and their relationship with water quality

in tropical Mexican streams with different land usesG. Vazquez J. A. Ake-Castillo M. E. Favila

Received: 3 September 2009 / Revised: 12 February 2011 / Accepted: 19 February 2011 / Published online: 9 March 2011

Springer Science+Business Media B.V. 2011

Abstract This study analyzes the relationship

between physical and chemical factors and the algal

communities in tropical streams in micro-watersheds

where [70% of their area has different land uses,

specifically, cloud mountain forest, coffee planta-

tions, and livestock pastures. Physical, chemical, and

biological variables were measured monthly in each

stream over a 1-year period. The concentrations of

nitrates ? nitrites, total suspended solids (TSS), and

silica in the streams were found to differ during the

dry and rainy seasons. Coffee-plantation streamsshowed the highest levels of suspended solids,

nitrates ? nitrites, and sulfates. Based on chlorophyll

a concentration, the forest and coffee-plantation

streams are oligo-mesotrophic, while pasture streams

are meso-eutrophic. Forest streams displayed the

lowest levels of richness and algal diversity, followed

by coffee-plantation streams, whereas pasture streams

were the most diverse. Chlorophyll a concentration

and species richness depended on land use and

season. Forest coverage was positively correlated

with acidophilous and oligo-eutraphentic diatom

species. Coffee coverage displayed a significant

positive correlation with motile species and a signif-

icant negative correlation with pollution-sensitivediatom taxa. The results show that diatom assem-

blages responded to micro-watershed conditions and

can be used to monitor the effects of land use on

streams in tropical regions.

Keywords Tropical streams Land use Diatoms

Cloud forest CCA Mexico

Introduction

Water quality and stream communities have been

severely affected by anthropogenic changes in land

use, including deforestation (Johnson et al., 1997;

Herlihy et al., 1998; Neill et al., 2001; Williams et al.,

2005). The removal of forest vegetation from riverine

ecosystems can change stream structure, discharge,

nutrient concentrations, light availability and stream

water temperature (Neill et al., 2001; Biggs et al.,

2004; Pan et al., 2004; Stevenson et al., 2006;

Electronic supplementary material The online version ofthis article (doi:10.1007/s10750-011-0633-4) containssupplementary material, which is available to authorized users.

Handling editor: David Dudgeon

G. Vazquez (&) M. E. FavilaInstituto de Ecologa, A.C., Carretera antigua a Coatepec

No. 351 El Haya, 91070 Xalapa, Veracruz, Mexico

e-mail: [email protected]

M. E. Favila


J. A. Ake-Castillo

Instituto de Ciencias Marinas y Pesqueras, Universidad

Veracruzana, Calle Hidalgo No. 617, Col. Ro Jamapa,

94290 Boca del Ro, Veracruz, Mexico


123

Hydrobiologia (2011) 667:173189

DOI 10.1007/s10750-011-0633-4
http://dx.doi.org/10.1007/s10750-011-0633-4http://dx.doi.org/10.1007/s10750-011-0633-4


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Schiller et al., 2007). In catchments that include a

large incidence of agricultural land use, significant

positive correlations have been found with nutrient

concentrations (Neill et al., 2001). Streams sur-

rounded by forest show higher nitrate concentrations

than streams surrounded by pastures, but the latter

can have higher concentrations of organic carbon andorganic nitrogen (Neill et al., 2001; Schiller et al.,

2007). Light input is another important factor that can

be modified by deforestation (Larned & Santos, 2000;

Mosisch et al., 2001; Bixby et al., 2009). Stream

channels covered by forests have lower light inputs

than those without such plant coverage (Larned &

Santos, 2000). When riparian vegetation is removed,

the production of benthic biomass may increase as a

response to increased light levels (Mosisch et al.,

2001; Stevenson et al., 2006; Schiller et al., 2007),

which is a situation that can lead to eutrophication.The relationship between land use and water

quality in streams has been investigated through

observations of a number of different animal species,

including macrophytes, fish and macroinvertebrates

(Hering et al., 2006; Lorion & Kennedy, 2009). Algae

have been used less frequently for this purpose,

though they have been considered to be ideal

biological indicators (Hill et al., 2001; Juttner et al.,

2003; Stevenson et al., 2006; Porter, 2008) due to

their (1) position at the base of the food chain;

(2) sessility; (3) high diversity; (4) extremely short lifecycles (in some species, cells may divide more than

twice daily, Lowe & Pan, 1996); (5) ready response to

alterations in water quality and (6) ubiquitous nature.

These characteristics have allowed regional compar-

isons of algal diversity to be made (Van Dam et al.,

1994; Hill et al., 2001; Bellinger et al., 2006).

The benthic algal communities of small rivers or

streams are commonly composed of diatoms, which

respond to many environmental variables and have

historically been good environmental indicators (Van

Dam et al., 1994). Riverine alterations derived fromdeforestation can modify the growth of such algae, as

well as the structure and species composition of their

communities. This is due in part to the different

tolerances and physiological requirements of diatom

species to environmental variables (Bixby et al.,

2009). Such differences between species allow them

to be grouped into metrics or auto-ecological classes

that indicate environmental conditions. These types

of metrics have often been used to assess changes in

stream communities in relation to anthropogenic

perturbations (Bahls, 1993; Van Dam et al., 1994;

Porter, 2008; Porter et al., 2008).

Relationships between stream diatom assemblages

and water quality can change with spatial scale and

with the occurrence of the wet and dry seasons. In

Willamette Valley, the importance of spatial scale inthe evaluation of the effects of soil use on river

conditions is most evident in the wet season, but the

stream water chemistry during the dry season is, to a

greater extent, a function of catchment-wide biogeo-

chemical processes and land use patterns (Pan et al.,

2004). In catchments in Michigan, the superficial

geology, but not the land use, was strongly correlated

with stream water chemistry in the summer, and the

effects of land use on stream water chemistry were

more evident when the basins and streams were more

hydrologically connected in the autumn (Johnsonet al., 1997).

Compared to temperate areas, there have been few

studies in tropical regions to assess the relationships

between stream algal community structure, biomass,

and growth form and stream conditions in micro-

watersheds under deforestation for different land

uses, such as agriculture and pastures (Silva-

Benavides, 1996; Larned & Santos, 2000; Neill

et al., 2001; Juttner et al., 2003; Bellinger et al.,

2006; Bixby et al., 2009). In Mexico, tropical

montane cloud forest (TMCF) has a very importantecological and hydrological role (Holdridge et al.,

1971), supports high species diversity, and is a refuge

for many endemic species (Williams-Linera, 1994).

The TMCF of central Veracruz has been subjected to

modification for a quite long time. The original forest

has been reduced to small patches within a matrix of

coffee plantations, pastures, old fields, and human

settlements (Garca-Franco et al., 2008). There are

many tropical streams in this region, but they have

been strongly perturbed by human activities. How-

ever, the efficacy of stream algal communities asecological indicators relative to water-quality vari-

ables and land use characteristics has not been tested

in this tropical region.

The purpose of this study was to assess the

relationships between temporal variations in the

physical and chemical variables and the relative

abundance of diatom species of streams located in

micro-watersheds within the cloud forest and areas of

different land uses (coffee plantations and livestock

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pastures). We also evaluated whether there are

seasonal variations in the effects of different land

uses on species richness, diversity, and the different

metrics of the algal community (tolerance to pH,

tolerance to nutrient concentrations, pollution toler-

ance and algal morphology). To our knowledge, this

is the first study to examine indicators of ecologyconditions in these streams.

We hypothesized that the streams in conserved

micro-basins with a large amount of cloud forest

coverage would be oligotrophic and exhibit a high

diversity and dominance of diatom species with poor

tolerance to both pollution (sensitive) and high

nutrient concentrations (representing eutrophic con-

ditions). Taxa better adapted to oligotrophic condi-

tions will be intolerant of increased environmental

stress. In contrast, a greater dominance of species

tolerant to eutrophic conditions and high nutrientconcentrations would be expected to be found in the

streams of coffee plantations and pasturelands, as

these land uses are found in deforested watersheds

where fertilizers (mainly N, P, and K) are applied.

We also expected that during the rainy season, the

effect of land use on stream conditions would be

more evident than during the dry season, mostly in

deforested watersheds, due to the runoff of terrestrial

nutrients and sediments into streams.

Methods

Study area

The study area is located in the headwaters of the La

Antigua river watershed, Veracruz (Fig. 1). The total

area of the watershed is 1,322 km2. The predominant

soil types in this region are andosols, andic lithosols

and highly porous muddy soils. The climate istemperate humid, with an average temperature of

18C and mean annual precipitation of 1,500 mm

Fig. 1 Location of

sampling sites within La

Antigua high river basin,

Mexico

Hydrobiologia (2011) 667:173189 175

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(Williams-Linera, 2007). Although the dominant

vegetation in the region is montane cloud forest,

there has been an extremely high rate of conversion

from the original forest to various land uses in

recent years. As a result, the region is characterized

by a fragmented landscape comprising cloud forest,

agricultural plots, livestock pastures, coffee planta-tions, and human settlements (Garca-Franco et al.,

2008).

The study was conducted in eight micro-water-

sheds located at between 1,117 and 2,171 m a.s.l.

within the larger La Antigua watershed (Table 1).

Streams were chosen as follows: two were located in

micro-watersheds with cloud forest (F1 and F2, in the

La Cortadura Reserve Zone, Municipality of Coate-

pec); three in coffee plantation areas (C1, C2, and C3,

Municipality of Xico); and three were surrounded by

livestock pastures (P1, P2, and P3, Municipality ofTeocelo-Cosautlan) (Fig. 1). The selected micro-

watersheds were characterized by the land use of

interest in over 70% of their total area. In the case of

the forest micro-watersheds, field work was possible

at only two locations because of the inaccessibility of

these well-conserved areas. Some features of the

micro-watersheds and streams studied were obtained

from a Geographic Information System of the area

(Rosario Landgrave, unpublished data, Table 1).

Sampling and laboratory analysis

Field work was carried out from June 2005 to May

2006. During this period, the highest rainfall in the

region occurred from August to October 2005

([200 mm); the driest period was from November

2005 to May 2006 (\100 mm) (Munoz-Villers,2008). Two sampling sites were established 100 m

apart in zones of rapids in each stream. Monthly

measurements, with the exception of the month of

December, were recorded in situ, and water samples

were collected for chemical analysis. At each sam-

pling site, depth and instantaneous velocity were

measured through a perpendicular (transversal) tran-

sect of the stream with a meter and a flow meter,

respectively (Flow Probe 101-FP201). Discharge

(Q) was calculated as Q = Av, where A is the

transversal area, and v is the flow (m3 s-1) (Hauer &Lamberti, 1996). The following physical and chem-

ical variables were determined at each site using a

portable Yellow Spring Instruments meter (YSI,

Mod. 85): stream depth and width (cm), temperature

(T, C), dissolved oxygen (DO, mg l-1), and electric

conductance (EC, lS cm-1). A potentiometer

(Barnant Mod. 20) was used for measuring pH.

Using 1-l polyethylene bottles, water samples were

collected for the determination of the following

Table 1 Characteristics of the micro-watersheds and streams studied at the high La Antigua river catchment

Streams

Forest 1 Forest 2 Coffee 1 Coffee 2 Coffee 3 Pasture 1 Pasture 2 Pasture 3

Micro-watersheds

Elevation (m) 1975 2171 1176 1117 1327 1579 1653 1523

Area (km2) 0.50 0.72 1.01 1.56 4.72 0.36 1.07 0.41

Land use (%)

Cloud forest 94 72 3 4 9 25 18 18

Coffee plantation 0 1 87 84 52 4 24 1Pasture 6 24 4 5 36 71 79 79

Urban zone 0 2 5 7 3 0 1 1

Streams

Width (cm) 73.9

(47.5100)

80.0

(50100)

96.7

(30220)

132.1

(80200)

206.3

(140270)

146.7

(110200)

203.8

(70290)

192.1

(40270)

Depth (cm) 4.3

(2.78.3)

6.1

(3.89.4)

5.8

(1.817.3)

7.0

(4.510.9)

13.3

(8.420.1)

9.3

(613.5)

14.4

(6.918.7)

9.9

(115.5)

The mean values are the average of the two sites sampled in each stream from June 2005 to May 2006. Maximum and minimum

values in brackets

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physical and chemical variables: total suspended

solids (TSS, dry weight), alkalinity (as CaCO3,

phenolphthalein), ammonium (NH4?, Nessler), nitrites

(NO2-, diazotization), nitrates (NO3

-, brucine), silica

(SiO2, molybdate), chlorides (Cl-, titration with

AgNO3), and sulfates (SO42-, turbidimetric tech-

nique). Samples were collected in 250-ml glass bottlesfor measuring total phosphorus (TP, persulfate diges-

tion and ascorbic acid) and reactive phosphorus (RP,

ascorbic acid). Analyses were conducted by spectro-

photometric techniques (AOAC, 1990; APHA, 1998).

All samples were stored at 4C until analysis. Calcium

(Ca2?) and magnesium (Mg2?) were measured using

an atomic absorption spectrophotometer (Shimadzu

Mod. AA6501); sodium (Na?) and potassium (K?)

were measured with a flame photometer (Corning

Mod. 410). Nutrients (NO3-, NO2

-, NH4?, TP, and

RP) were determined within 48 h of sample collection.For chlorophyll a measurement, three stones were

collected monthly from each site (six per stream) and

placed in separate bottles containing 90% methanol

for chlorophyll a extraction. Samples were kept

refrigerated in the dark and were analyzed within

24 h in the laboratory. Chlorophyll a was measured

spectrophotometrically, and its concentration (mg m-2)

was determined through Holdens equations (Meeks,

1974).

Epilithon samples were collected bimonthly from

the same sites used for water-quality analysis duringthe wet (August and October) and dry (January, March,

and May) seasons. Three stones (10 cm2

approx.) were

collected at random, scrubbed with a toothbrush and

rinsed with 250 ml of water. A subsample was fixed in

4% formaldehyde for subsequent taxonomic identifi-

cation. A portion of the sample was used to prepare

permanent slides of diatoms in synthetic resin

(Naphrax) (Hasle, 1978). Diatom species were identi-

fied based on the method of Kramer & Lange-Bertalot

(1991a, b, 1997, 1999). In addition, the most abundant

soft algae were identified based on Bourrelly (1966,1970). Species were quantified using sedimentation

chambers and an inverted microscope. The relative

abundance of each species was obtained based on the

quantification of at least two crossed diameter tran-

sects. When cells in a sample were sparse, we repeated

the procedure incrementing the number of transects

and, in some cases, the volume of sedimentation to

assure that we were counting more than 500 cells of the

most frequent species (Venrick, 1978).

Data analysis

Differences in discharge, chlorophyll a, species

richness and Shannon diversity among land uses

(three levels: forest, coffee plantations, and pastures)

and between seasons (two levels: rainy season and

dry season) were assessed using a two-way analysisof variance. The locations in each land use were used

as replicates, and the streams were nested into each

location. Species richness values were square-root

transformed to normalize the distribution and to make

the variance independent of the means (Sokal &

Rohlf, 1981). We also calculated the coefficient of

variation (CV) of the arithmetic mean of monthly

chlorophyll a values.

To compare changes in the composition of species

between streams (beta diversity), a cluster analysis was

applied using a species presenceabsence matrix, theJaccard index and the Unweighted Pair Group Method

with Arithmetic Mean (UPGMA) grouping method

with the Multi-Variate Statistical Package program

(MVSP). To analyze the relationship between diatom

assemblages and environmental variables, species

abundance was analyzed with a Canonical Correspon-

dence Analysis (CCA) using PC-ORD software (ver-

sion 4.34). A species abundance matrix was produced

using log10(x ? 1) transformation to stabilize vari-

ances, and a physical and chemical data matrix was

produced using log10(x ? 1) transformation, exceptfor pH. This matrix included 13 variables: discharge,

chlorophyll a concentrations, water temperature, pH,

alkalinity, conductivity, TSS, Cl-, RP, NO3-?

NO2-, NH4

?, SiO2, and SO42-. The statistical signif-

icance of the identified gradients was tested using a

Monte Carlo permutation test (999 permutations,

P = 0.05). We performed the Monte Carlo test with

a null hypothesis of no linear relationship between

matrices. Variables, such as cations, with a high

colinearity as indicated by high inflation factors

(VIF[10) were discarded. Rare species wereassigned low weights in the analysis.

Diatom metrics

Diatom species were classified according to their pH

tolerance in acidophilous (mainly occurring at

pH\7), circumneutral (mainly occurring at pH

values about 7), alkaliphilous (mainly occurring at

pH[7) and alkalibiontic (exclusively occurring at

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pH[7) (Van Dam et al., 1994). According to their

tolerance to nutrient concentrations, diatoms were

classified as oligotraphentic (with an affinity for

nutrient-poor environments), mesotraphentic (from

intermediate enriched environments), eutraphentic

(with an affinity for nutrient-enriched environments),

and oligo-eutraphentic species (indifferent species)(Van Dam et al., 1994). Regarding whether a spe-

cies was tolerant of a variety of pollution types,

species were classified according to Bahls (1993) as

the following: (1) very tolerant of a variety of pollution

types, (2) less tolerant to pollution, or (3) sensitive. We

only report the sensitive species here because they

showed the greatest contrasts between land uses.

Because diatom growth forms represent morpho-

logical adaptation to environmental conditions (Ste-

venson & Bahls, 1999; Wang et al., 2005), we included

certain metrics related to algal morphology. Accordingto the different ways in which species are attached to

the substrate, we evaluated the percentages of pros-

trate, stalked, and erect individuals; variable and

unattached species were scantly present in the streams

and they were not considered in this analysis. Erect and

stalked diatoms are susceptible to hydraulic distur-

bance, whereas prostrate diatoms may indicate high

levels of grazing and hydraulic disturbance (Wang

et al., 2005). Motile species include species that move

in unstable substrates (percentage ofNavicula, Nitzs-

chia, Surirella, and Gyrosigma) and may showincreased abundances with high sedimentation (Wang

et al., 2005). The percentages of the different metrics

were calculated by adding the relative abundance of the

species arranged into the different groups that were

considered (Stevenson & Bahls, 1999). We used

Pearsons correlations of land use percentages with

13 diatom metrics to assess how specific components

of stream diatom communities fit with the effects of the

land use on the water quality of the streams.

Results

Physical and chemical variables

The average stream water temperature in the forest was

lower (13C) than that recorded in the pastures and

coffee plantations (1719C) (Table 2). All of the

streams were well oxygenated ([4.5 mg l-1). A nearly

circumneutral pH was recorded in virtually all of the

streams; the most acidic pH was found in forest stream

1 in July (5.4), while the most alkaline pH was

observed in coffee plantation stream 3 (7.4). Forest

streams exhibited the lowest conductivities and alka-

linities, and streams in pastures and coffee plantations

displayed higher values in both of these variables.

The highest TSS concentrations were observed in thecoffee plantation streams and pasture stream 1. The

coffee plantation streams displayed the highest nitra-

te ? nitrite concentrations. Pasture streams displayed

the lowest mean nitrate ? nitrite and ammonium

concentrations, followed by forest streams. Very low

TP and RP were recorded at most sites; the sites in

forest stream 2 and coffee plantation stream 3

presented the highest concentrations of these variables.

Silica was highest in the pasture streams, followed by

those in the coffee plantations, and finally, in forest

stream 1; forest stream 2 had higher concentrations ofsilica than coffee plantation stream 1.

The average discharge values were not significantly

different between streams of the three land uses

analyzed (F2 = 2.87, P = 0.103). However, some

trends were evident during the rainy season: discharge

variations in streams flowing through forests were

lower than in coffee-plantation and pasture streams. In

streams flowing through these latter two land uses, the

heaviest discharges were registered from August to

October (rainy season) (Fig. 2).

Chlorophyll a

Land use and season had a significant effect on

chlorophyll a concentration (F2 = 22.012, P\0.001;

F1 = 11.26, P\0.05). The land use-season interaction

was also significant (F2 = 4.29, P\0.05). Pasture

streams displayed higher chlorophyll a concentrations

than forest and coffee plantation streams (P\0.001)

(Fig. 3). The chlorophyll a concentration was similar in

forest and coffee plantation streams (P = 0.37) and was

significantlyhigher in thedry season relative to the rainyseason. During the rainy season, the chlorophyll a con-

centration in pasture streams was significantly higher

than in coffee streams (P\0.05), but it was not

different from that in forests streams (P = 0.09). The

chlorophyll a concentration was not significantly

different between forest and coffee plantation streams

in either season. During the dry season, the chlorophyll

a concentrations in pasture streams were significantly

higher than in forest and coffee plantation streams

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Table2

Meanphysical,chemical,andchlorophylla

valuesineachstrea

m

atthehighLaAntiguarivercatchment

Streams

Forest1

Forest2

Coffee1

Coffee2

Co

ffee3

Pasture1

Pasture

2

Pasture3

Discharge(m3

s-1)

0.0

3

(0.0

030.0

8)

0.0

6

(0.0

20.1

4)

0.1

0

(0.0

10.3

9)

0.1

0

(0.0

20.1

5)

0.4

0

(0.050.7

4)

0.1

5

(0.0

30.2

9)

0.3

9

(0.0

50

.79)

0.1

9

(0.0

10.5

8)

Temperature(C)

13.1

(11.414.6

)

13.2

(11.515.1

)

17.7

(12.219.9

)

18.3

(12.720.8

)

19.8

(16

.721.7

)

17.7

(15.918.9

)

17.7

(1618.7

)

19.8

(18.522.4

)

Oxygen(mgl-1)

7.1(6.57.6

)

7.8(78.3

)

5.3(1.27.2

)

7.3(5.88.4

)

7.2 (6.67.6

)

7.1(67.9

)

6.7c

(4.97.7)

6.5c

(4.57.4

)

pH

6.3(5.46.8

)

6.9(6.47.4

)

6.6(6.37.1

)

7.2(6.37.7

)

7.4 (6.87.8

)

7.0(6.57.3

)

7.0(6.47.6)

6.9(6.57.3

)

Electricconductance(lScm-1)

19.7

(17.422.7

)

42.0

(29.9

59.3

)

92.2

(66125)

92.7

(62.4148.3

)

110.7

(68

.3165)

62.5

(53.469.3

)

54.6

(37.76

4.5

)

90.6

(85.994.7

)

Totalsuspendedsolids(mgl-1)

3.9(09.5

)

2.4(011)

7.5(023.2

)

12.2

(045.8

)

16.4

(0.0135.3

)

8.1(028.8

)

1.1(03.2)

3.2(013.6

)

Alkalinity(mgCaCO3

l-1)

9.9(8.712.8

)

20.0

(14.422.8

)

32.6

(11.8

54.7

)

41.6

(20.266.5

)

49.9

(29

.274.1

)

32.1

b

(25.636)

28.1

(20.43

3.8

)

45.1

(3847.2

)

NO3-

?

NO2-

(mgl-1)

1.4(0.34.1

)

1.4(0.32.7

)

4.2(0.29.1

)

3.1(0.1

17.3

)

3.9 (0.57.2

)

0.4(0.0

30.7

)

0.3(0.10.7)

0.3(0.10.9

)

NH4

?

(mgl-1)

0.2(01)

0.2(00.8

)

0.5(0.0

71.3

7)

0.4(0.11)

0.2 (0.030.5

)

0.1(00.5

)

0.2(01.5)

0.2(00.7

)

TP(mgl-1)

0.0

3

(00.0

6)

0.0

7

(0.0

30.0

8)

0.0

4

(00.3

)

0.0

4

(00.1

)

0.1 (0.020.2

)

0.0

4

(00.1

)

0.0

4

(00.1)

0.0

5

(0.0

20.0

8)

RP(mgl-1)

0.0

2

(00.0

5)

0.0

4

(00.0

6)

0.0

2

(00.0

7)

0.0

2

(00.0

4)

0.0

5

(0

0.1

)

0.0

1

(00.0

4)

0.0

2

(00.04

)

0.0

3

(00.0

5)

SiO2

(mgl-1)

17.4

(10.235.5

)

27.3

(18.337.9

)

22.9

(15.245.2

)

42.1

(20.573.8

)

30.8

(18

46.4

)

34.0

(21.548.1

)

32.5

(17.24

9.1

)

44.5

(24.260.6

)

Cl-(mgl-1)

4.4(3.16)

4.3(3.2

5.3

)

6.2(5.47.5

)

5.1(3.96.5

)

5.0

7

(2.

56.3

)

4.4

6

(3.46)

4.2

0

(3.25.7)

4.2

3

(3.26)

SO4

2-

(mgl-1)

2.0(1.33)

2.2(1.53.2

)

2.2(1.43.1

)

2.8(1.33.6

)

2.2 (1.

43.3

)

2.1(1.43.2

)

2.3(1.43.7)

1.8(1.22.9

)

Ca2?

(mgl-1)

3.7(1.811.4

)

4.6(2.96.7

)

11.9

(917.5

)

11.2

(7.820.7

)

13.0

(8.

918)

6.7(3.58.3

)

6.9(213.3

)

9.9(313)

Hydrobiologia (2011) 667:173189 179

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(P\0.001, Fig. 3). The variation in chlorophyll a con-

centration was lower in forest streams (CV: F1 = 41%,

F2 = 63%) than in pasture streams (CV: P = 65%,

P2 = 78%, P3 = 53%). The highest variation in chlo-rophyll a concentrations was found in coffee plantation

streams 2 and 3 (CV: C1 = 44%, C2 = 123%,

C3 = 120%).

General features of diatom assemblages, richness,

and diversity

A total of 32 diatom species were recorded belonging

to 14 genera (Appendix 1Supplementary material).

Jun Jul Aug Sept Oct Nov Jan Feb Mar Apr May

Discharge(m3

s-1)

0.0

0.1

0.2

0.3

0.4

0.5

0.6

0.7

ForestCoffeePasture

Fig. 2 Monthly average dischargesfor the streams found in eight

micro-watersheds according to land use: forest (n = 2 streams),

coffee-plantation (n = 3 streams), pasture (n = 3 streams) at the

La Antigua high river basin. Bars indicate standard error

Land use

Forest Coffee Pasture

Chlorophylla(mgm

-2)

0

5

10

15

20

25

30

35

Rainy

Dry

Fig. 3 Mean chlorophyll a values for each land use during therainy and dry seasons. The values shown are the average of the

streams found in each micro-watershed according to land use:

forest (n = 2 streams), coffee-plantation (n = 3 streams),

pasture (n = 3 streams). Bars indicate standard error

Table2

continued

Streams

Forest1

Forest2

Coffee1

Coffee2

Co

ffee3

Pasture1

Pasture

2

Pasture3

Na?

(mgl-1)

2.7(1.3

5.2

)

4.5(2.97.4

)

5.7(3.99.6

)

7.6(5.511.5

)

6.8 (3.

911.1

)

5.5(4.28)

5.4(3.78.3)

7.4(5.59.5

)

Mg

2?

(mgl-1)

0.6(0.31.1

)

1.6(11.9

)

5.2(3.79.4

)

4.5(310.4

)

6.5 (4.

98.3

)

3.3(2.74)

2.8(23.2)

4.6(3.8

5.9

)

K?

(mgl-1)

1.1(0.81.6

)

1.5(1.12)

2.8(1.54.5

)

2.4(1.63.6

)

2.4 (1.53.6

)

1.9(1.52.4

)

2.0(1.53.1)

3.2(2.64.1

)

Chlorophylla

(mgm-2)

3.5(1.0

54.9

)

8.5(1.517.7

)

3.0(0.6

64.7

)

2.2(0.910.1

)

5.6

a

(1.223.9

)

14.0

(1.328.8

)

17.6

(1.246

.8)

22.9

(6.642.1

)

Themeanvaluesaretheaverageo

fthetwositessampledineachstream

from

June2005toMay2006.

Maximu

m

andminimum

valuesinbrackets

180 Hydrobiologia (2011) 667:173189

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Richness ranged from 9 to 27 species in all of the

streams analyzed. The genera with the highest

number of species were Achnanthes (6 spp.), Navic-

ula (4 spp.), Nitzschia (4 spp.), and Gomphonema

(3 spp.). The dominant algae from other groups were

Chlorophyceae, such as Closterium monoliferum and

Cosmarium sp., and the cyanobacteria Oscillatoriacrassa, O. sancta, and Phormidium diguetii. Both of

these groups were observed only in pastures. Seven

diatom taxa were found at all sites during the dry and

wet seasons (Achnanthes lanceolata, Achnanthidium

minutissimum, Amphipleura lindheimeri, Cocconeis

placentula, Eunotia pectinalis, Gomphonema oliva-

ceum, and Rhoicosphenia abbreviata).

In terms of beta diversity, the forest streams were

separated by their species composition from the

coffee plantations and pastures streams. Then, coffee

stream 3 was separated from coffee streams 1 and 2and from pasture streams. Finally, the three pasture

streams were separated by their species composition

from the coffee plantation streams 1 and 2 (Fig. 4). In

the coffee plantation and pasture streams, species

were observed that were not found in the forest

streams, such as Achnanthes rupestris, Cymbella

tumida, Gyrosigma scalproides, Melosira varians,

Navicula viridula, Nitzschia obtusa, and Surirella

biseriata (Appendix 1Supplementary material).

Land use and season had a significant effect on

diatom richness (F2 = 27.99, P\0.001; F1 =

14.051, P\ 0.05) (Fig. 5a). The land use-season

interaction was not statistically significant (F2 = 1.5,

P = 0.27). Forest streams displayed lower species

richness than coffee-plantation and pasture streams

(P\0.017). The species richness in forest streams

was lower during the rainy season than during the dry

season (P\0.05). Land use had a significant effect

on algae diversity (F2 = 8.46, P\ 0.05), as opposed

to season (F1 = 4.73, P[ 0.05) (Fig. 5b). Forest

streams showed a lower algal diversity than coffee-

plantation and pasture streams (P\ 0.02 andP\ 0.002, respectively). Algal diversity was similar

between coffee-plantation and pasture streams

(P = 0.16).

Relationship between diatom assemblages

and environmental variables

The first axis of the CCA was significant (Monte Carlo

test, P\ 0.002), and axes 1 and 2 accounted for 18.8%

Jaccard's Coefficient

F1

F2

C1

C2

P1

P2

P3

C3

0.52 0.6 0.68 0.76 0.84 0.92 1

Fig. 4 Cluster analyses of the streams studied in eight micro-

watersheds with different land use according to the presence

absence of diatom species, recorded from June 2005 to May

2006 at La Antigua high river basin. Forest streams F1 and F2;

coffee-plantation streams C1, C2, and C3; pasture streams P1,

P2, and P3

Land use


Ric

hness

0

2

4

6

8

10

12

14

16

18

RainyDry

Land use


Diversity(H,ShannonIndex)

0.0

0.2

0.4

0.6

0.8

1.0

RainyDry

(b)

(a)

Fig. 5 Species richness (a) and diversity (Shannon index, H0)

(b) in the rainy and dry seasons in streams found in eight

micro-watersheds with different land use studied across the La

Antigua high river basin

Hydrobiologia (2011) 667:173189 181

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of the total data variance (Table 3). The ordination

(CCA) based on species density (ind cm-2) revealed a

clear grouping of streams according to land use andnutrient concentration (Fig. 6a). The first axis was

positively correlated with nitrates ? nitrites, temper-

ature and conductivity; the second axis showed a

strong positive correlation with TSS, chlorides, sul-

fates, and ammonium, and it showed a negative

correlation with chlorophyll a, silica and discharge

(Table 3).

The coffee plantation streams were grouped in the

right quadrant in the rainy season (August and

October) when there were higher concentrations of

NO3- ? NO2-, TSS, NH4?, Cl-, and SO42-. Asso-ciated with these conditions, motile species were

observed that are indicative of eutrophic conditions,

such as G. scalproides, N. obtusa, Surirella tenera,

Navicula schroeteri, and N. contenta (Fig. 6b). The

forest streams were located on the far left of the first

axis throughout the sampling period, with those of the

coffee plantations and pastures principally during

the dry season (MarchMay); these sites showed the

lowest concentrations of all of the variables

positively correlated with axis 1, such as

NO3-? NO2

-, and NH4? (Fig. 6a). Pollution-intol-

erant species, such as Fragilaria construens, were

associated with these conditions, but Frustulia vul-

garis, a mesotraphentic species, was also found in

this cluster. A characteristic species of the forest

streams was Achnanthes subsalsa, although we could

not find ecological information for this species.

Associated with axis 2, the pasture streams were

grouped based on seasons: during the dry season

(MarchMay), there were high concentrations ofchlorophyll a and silica, and the important species

were Achnanthes exigua, M. varians, and Pinnularia

gibba, which are all tolerant to eutrophication; in the

wet season (August and October), these streams were

characterized by high values of discharge, tempera-

ture and alkalinity, and in these conditions, Navicula

cryptocephala, A. rupestris, Melosira lineata, Gom-

phonema parvulum, and Gomphonema intricatum

were abundant (Fig. 6b).

Some species were present throughout the cycle

but were only abundant in some streams. G. oliva-ceum, C. placentula, and Nitzschia amphibia were

most abundant in March and May in the pasture

streams. During the dry season, the forest streams

exhibited abundant A. minutissimum, R. abbreviata,

and E. pectinalis. A. lanceolata was found in all of

the streams, but was particularly abundant in pasture

stream 3 in August and October.

Diatom metrics

The classification of diatoms species according totheir ecological preferences are presented in Appen-

dix 2 (Supplementary material). With regard to pH,

forest stream 1 displayed the highest proportion of

acidophilic species (pH 5.5 and 7) in both the wet

(18.67%) and dry (54.23%) seasons (Table 4). How-

ever, alkaliphilous ? alkalibiontic species prevailed

in the other streams in both seasons (49.596%). In

the wet season, oligo-eutraphentic species dominated

in forest stream 1 (72%); whereas in forest stream 2,

Table 3 Summary statistics for canonical correspondence

analysis (CCA) axes conducted to analyze the relationships

between diatom assemblage and environmental variables in the

eight streams at the high La Antigua river catchment

Axis 1 Axis 2

Eigenvalue 0.181 0.116

Variance in species data

Cumulative % explained 11.4 18.8

Pearson correlation, Spp-Envt. 0.869 0.833

Intraset correlation for environmental variables

Temperature 0.336 -0.125

pH -0.028 -0.034

Electric conductance 0.288 0.001

TSS 0.036 0.737

Alkalinity 0.070 -0.226

NH4?

0.200 0.304

NO3-?

NO2-

0.723 0.528RP 0.332 -0.058

SiO2 -0.397 -0.496

Cl-

-0.055 0.375

SO42- 0.158 0.315

Discharge 0.277 -0.294

The strongest correlations between the environmental variables

and the axis are shown in bold characters

Fig. 6 Canonical Correspondence Analysis (CCA) ordination

of diatom assemblages in streams found in eight micro-

watersheds with different land use studied across the La

Antigua high river basin: a Ordination of sampling streams and

environmental variables (represented by arrows), b ordination

of diatom species. Forest streams F1 and F2; coffee plantation

streams C1, C2, and C3; pasture streams P1, P2, and P3.

August A, October O, January J, March Mr, May My

c

182 Hydrobiologia (2011) 667:173189

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(a)

(b)

Temp.

Cond

TSS

Alk

NH4NO3+NO2

Si

Cl SO4

Discharge

Chlorophyll

Axis 1

Ax

is2

Gyrosigma scalproidesNitzschia obtusa

Surirella tenera

Frustulia vulgaris

Nitzschia palea

Achnanthes subsalsa

Fragilaria construens

Navicula schroeteri

Navicula contenta

Amphipleura lindheimeri

Achnanthidium minutissimum

Gomphonema olivaceum

Achnanthes lanceolata

Nitzschia linearis

Surirella biseriata

Fragilaria ulna

Achnanthessp.

Achnanthes rupestoides

Navicula cryptocephala

Achnanthes exigua

Melosira varians

Pinnularia gibba

Gomphonema parvulum

Gomphonema intricatum

Achnanthes inflata

Melosira lineata

Navicula viridula

Rhoicosphenia abbreviata

Cocconeis placentula

Eunotiapectinalis

F1A

F2A

C1A

C2A

C3A

P1A

P2A

P3A

F1O

F2O

C1O

C2O C3O

P1O

P2O

P3O

F1J

F2J

C1J

C2J

C3J

P1J

P2J

P3J

F1Mr

F2Mr

C1Mr

C2Mr

C3Mr

P1Mr

P2Mr

P3Mr

F1MyF2My

C1My

C2My

C3My

P1My

P2My

P3My

Temp.Cond

TSS

Alk

NH4

NO3+NO2

Si

ClSO4

Discharge

Chlorophyll

Axis 1

Axis 2

Hydrobiologia (2011) 667:173189 183

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50% of the diatoms were mesotraphentic. During the

dry season, forest stream 1 showed a higher percent-

age of mesotraphentic species (54.2%), while the

species in forest stream 2 were mostly eutraphentic

(82.7%). In the wet and dry seasons, the coffee

plantation and pasture streams displayed the highest

percentages of eutraphentic diatoms (wet: 5593%,

dry: 47.682.7%). During the wet season, foreststreams displayed the highest proportion of sensitive

species (5593.13%) compared to the other streams

(14.6662.23%, Table 4). In the dry season the

proportion of sensitive species increased in most

streams (32.5796%). Motile or sediment-tolerant

species prevailed in the coffee plantation streams,

mainly during the wet season (39.465.1%). The

dominant growth forms in all streams during the wet

season were prostrate (73.997.4%). Erect species

dominated in forest stream 1 during the dry season

(54.2%), while stalked species dominated in forest

stream 2 (63.94%). Prostrate species were dominant

in the coffee plantation and pasture streams, regard-

less of season (51 and 91.47%, respectively).

The forest percentage was only positively corre-

lated with % acidophilous, mesotraphentic, oligo-

eutraphentic, erect and sensitive species in the wetseason; no significant correlation was detected for the

dry season (Table 5). E. pectinalis (acidophilous,

mesotraphentic and erect) and F. vulgaris (mesot-

raphentic) had the highest densities in the forest

streams during the wet season. A. subsalsa, A. exigua,

and A. minutissimum were predominant among the

oligo-eutraphentic species in the forest streams. In

contrast, the correlation with alkaliphilous ? alkali-

biontic, eutraphentic and motile species was negative

Table 4 Diatom metrics (%) obtained for rainy and dry seasons in the eight streams at the high La Antigua river catchment

Diatom metrics (%) Streams

Season Forest 1 Forest 2 Coffee 1 Coffee 2 Coffee 3 Pasture 1 Pasture 2 Pasture 3

Acidophilous Rainy 18.67 2.01 0.61 0.19 0.69 2.07 0.71 4.68

Dry 54.23 2.14 19.55 0.08 2.23 0.88 0.97 16.73

Circumneutral Rainy 0.0 5.18 10.12 2.21 1.27 7.8 19.26 6.86

Dry 28.61 4.17 0.73 19.80 2.24 19.45 24.19 32.71

Alkaliphilous ? alkalibiontic Rainy 13.23 72.48 74.31 83.36 96.39 87.86 79.72 88.40

Dry 5.60 86.94 74.77 63.09 92.33 74.92 74.51 49.55

Oligotraphentic Rainy 0.0 0.0 1.7 0.0 1.3 5.7 15.4 0.0

Dry 0.0 0.0 0.0 0.5 0.1 6.7 16.2 17.6

Mesotraphentic Rainy 18.7 50.1 4.5 0.2 0.8 2.1 0.7 4.7

Dry 54.2 2.1 20.0 15.6 2.3 2.3 1.0 16.7

Eutraphentic Rainy 9.1 14.6 77.0 74.5 93.1 73.0 78.5 55.4

Dry 15.2 82.7 73.7 47.6 57.2 57.9 63.5 17.7

Oligo-eutraphentic Rainy 72.1 35.3 16.3 23.9 4.2 18.7 5.4 39.9Dry 30.4 15.1 5.4 35.6 40.1 28.8 19.2 47.7

Sensitive species Rainy 93.1 51.8 28.3 14.6 37.9 38.4 62.2 51.3

Dry 86.3 76.7 39.7 77.5 89.3 32.6 96.0 94.2

Prostrate Rainy 77.91 92.15 85.60 97.46 92.54 91.18 84.69 73.90

Dry 31.75 33.82 51.04 61.52 61.52 69.09 91.47 68.51

Stalked Rainy 2.28 5.80 13.48 1.87 6.31 6.09 13.91 20.63

Dry 13.71 63.94 29.07 38.05 1.67 6.61 6.89 2.17

Erect Rainy 18.67 2.01 0.61 0.19 0.69 2.07 0.71 4.68

Dry 54.23 2.14 19.55 0.08 2.23 0.88 0.97 16.73

Motile diatoms Rainy 0.0 0.0 65.1 54.7 39.4 40.7 11.1 2.3

Dry 0.1 0.7 30.9 2.9 9.1 71.7 3.3 5.0

The classification of diatom species was obtained according to their ecological preferences as presented in Appendix 2

(Supplementary material)

184 Hydrobiologia (2011) 667:173189

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and was also significant for the wet season, as the

lowest percentages of these species were present at

that time; eutraphentic species, such as N. schroeteri,N. contenta, G. olivaceum, and A. lanceolata, were

more abundant in the coffee plantation and pasture

streams. Coffee plantation streams only displayed a

significant positive correlation with motile species,

such as G. scalproides, Nitszchia obtusa, N. schro-

eteri, and a significant negative correlation with

sensitive species in the wet season. Pasture streams

were only correlated with oligotraphentic and pros-

trate species during the dry season (Table 5).

C. placentula and A. rupestris were dominant among

the prostrate species in these streams.

Discussion

Our findings reveal that it was possible to detect the

effects of land use on water physical and chemical

characteristics in small micro-watersheds associated

with over 70% of a specific land use within the larger

La Antigua river watershed. The effect of land use

has been observed in streams draining watersheds

with over 75% deforestation (Biggs et al., 2004).

The physical and chemical variables of the waterthat exhibited the greatest differences between the

study streams were nitrates ? nitrites, reactive phos-

phorous, and TSS. The highest concentrations of

nitrates ? nitrites were recorded in the coffee plan-

tation streams compared to those of the forest and

pastures. This concurs with the findings of other

studies in which the highest output of nitrates ?

nitrites was observed in predominantly agricultural

watersheds (Schiller et al., 2007). Furthermore, in the

forest streams, nitrates ? nitrites displayed higher

concentrations than in the pasture streams. The highproduction of NO3

- in the forest soils of the Amazon

results in high concentrations of NO3- in its stream

waters (Neill et al., 2001), which was not seen in the

pasture streams. In general, the humus in the forest

soils has higher nitrogen content than the humus from

the pasture soils (unpublished data). This suggests

that the presence of large amounts of leaf litter

derived from the conserved vegetation of the forests

results in the transportation of nitrogen to the streams.

Table 5 Pearsons correlation coefficients (rs) between metrics of diatoms and percentage of land use in the micro-watersheds

studied during the rainy and dry seasons at the high La Antigua river catchment

% land use % land use

Forest Coffee Pasture Forest Coffee Pasture

Acidophilous Oligo-eutraphentic

Rainy 0.784 0.434 0.251 Rainy 0.802 0.4 0.32

Dry 0.617 0.658 0.347 Dry 0.116 0.174 0.33

Circumneutral Sensitive species

Rainy 0.350 0.019 0.575 Rainy 0.798 0.748 0.121

Dry 0.201 0.496 0.448 Dry 0.189 0.296 0.167

Alkaliphilous ? alkalibiontic Prostrate

Rainy 0.811 0.276 0.475 Rainy 0.291 0.486 0.31

Dry 0.557 0.284 0.211 Dry 0.701 0.0294 0.747

Oligotraphentic Stalked

Rainy 0.231 0.29 0.596 Rainy 0.403 0.16 0.603

Dry 0.261 0.507 0.887 Dry 0.3 0.208 0.575

Mesotraphentic Erect

Rainy 0.751 0.392 0.286 Rainy 0.784 0.434 0.251

Dry 0.539 0.021 0.514 Dry 0.616 0.187 0.385

Eutraphentic Motile diatoms

Rainy 0.939 0.54 0.291 Rainy 0.71 0.876 0.356

Dry 0.238 0.278 0.104 Dry 0.264 0.0142 0.26

Significant correlations (P\0.01) are shown in bold characters

Hydrobiologia (2011) 667:173189 185

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The coffee plantation streams investigated in this

study did not exhibit differences compared to the

forest and pasture streams in terms of RP and TP

concentrations, which is in agreement with the results

of other studies reporting significant effects of

agriculture on N but not on P (Jordan et al., 1997;

Neill et al., 2001).Silica is more associated with the geological

weathering of a substrate than any particular land

use (Williams et al., 2005). The high silicate

concentrations recorded in all of the streams of La

Antigua are due to the volcanic origin of the substrate

of this area. Soils found in pastures are characterized

by high clay and aluminumsilicate content, and they

undergo strong weathering that promotes the release

of Si into streams (Munoz-Villers, 2008). The silica

concentrations recorded in this study concur with

those reported for other tropical streams located involcanic basins in Mexico (Ramos-Escobedo &

Vazquez, 2001).

Discharge was similar among streams from the

three land uses analyzed according to the ANOVA.

However, the CCA suggested that the discharge

during the rainy season in pasture streams and one

coffee plantation stream affected the abundance and

species composition of diatoms. These streams are

the widest and deepest of all of the streams analyzed

during the rainy season.

Based on the oligotrophiceutrophic boundary formean chlorophyll a values reported by Dodds et al.

(1998), the forest and coffee plantation streams at La

Antigua can be categorized as oligo-mesotrophic

(020 mg m-2); and pasture streams can be desig-

nated meso-eutrophic (2070 mg m-2

), particularly

in the dry season. Forest streams showed the lowest

values for chlorophyll a, richness, and diversity. The

canopy cover associated with the forest streams

included in our study was extremely high ([90%)

(Garca-Franco et al., 2008), and the amount of light

reaching the stream surface was correspondingly low.In contrast, the highest richness and diversity values

were recorded in the pasture and coffee streams. This

could be related to higher nutrient concentrations

coupled with the greater amount of light reaching the

streams, given the scarce canopy cover in pastures.

Other studies have also shown that levels of chloro-

phyll a are related to light availability and intensity

and nutrient concentrations, such as that of silica

(Larned & Santos, 2000; Mosisch et al., 2001;

Schiller et al., 2007). Despite the fact that the coffee

plantation streams had the highest nutrient concen-

trations, they had intermediate chlorophyll a values.

This might be due to the high suspended solid

concentrations in these streams, particularly during

the wet season, which may cause a decrease in algal

abundance (Harding et al., 1999). The large quantityof sediments in La Antigua could have favored more

variation in the seasonal fluctuation of chlorophyll

a in the coffee plantation streams compared to those

of the forest and pastures, which showed lower

fluctuations of chlorophyll (as indicated by the CV).

Although the effects of light availability on algal

communities were not studied directly, the recording

of cyanobacteria and green algae in the pasture

streams suggests that conditions of greater defores-

tation in the pastures compared to the coffee plan-

tations and forests favor the introduction of thesefilamentous species, which are tolerant to high

intensities of light and high concentrations of nutri-

ents. In contrast, only diatoms were found in the

forest and coffee plantation streams. Similar results

were reported by Mosisch et al. (2001) who found

that diatoms dominate in shaded streams and that

green filamentous algae are the species most com-

monly found in open streams.

Our results show that the algal richness, diversity

and composition in the streams at La Antigua are

good predictors of changes in habitat related tocatchment land use. Richness and diversity were

found to be lowest in forest streams. The dominant

species in forest streams were species frequently

associated with shady conditions and oligotrophic

waters (Van Dam et al., 1994; Weilhoefer & Pan,

2006). In particular, E. pectinalis is considered a key

indicator of acidic and oligotrophic waters (Van Dam

et al., 1994; Hill et al., 2001). A. subsalsa is also

found in these conditions. Achnanthes species have

frequently been associated with the headwaters of

shaded streams (Carpenter & Waite, 2000; Weilhoefer& Pan, 2006). Similar species assemblages were

found in the forest, coffee plantation and pasture

streams in the dry season when the lowest concen-

tration of nutrients was recorded, suggesting that

land use has a lower influence at this time than it

does in the wet season. The dominant species found

were broadly distributed diatoms that are common

in tropical streams and typical of meso-eutrophic

streams.

186 Hydrobiologia (2011) 667:173189

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The CCA showed that pasture streams 2 and 3

differed from the other streams during the dry season

in their higher concentrations of Si and of chlorophyll

a, as well as in the dominance of species that are

indicators of disturbance. The high concentrations of

Si and chlorophyll a suggest that there was a clear

influence of the geological substrate that fostered astate of eutrophication. The prevailing species in

the pasture streams, such as M. varians, M. lineata,

N. amphibia, N. linearis, and N. cryptocephala, are

common in eutrophic waters (Van Dam et al., 1994;

Fore & Grafe, 2002) and, according to Bahls (1993),

are tolerant to pollution. However, in the wet season

(August and October) and in January, there was a

clear influence of land use that differentiated the

coffee plantation streams, due to their high concen-

trations of nitrates and TSS, and the pasture streams

based on their higher discharge, alkalinity, andconductivity. These conditions influenced the domi-

nant species present: the eutrophic diatoms found in

coffee plantations and pastures, such as G. scalpro-

ides, have been reported in polluted streams with high

nutrient and sediment levels (Van Dam et al., 1994;

Juttner et al., 2003; Bona et al., 2007). Specifically,

G. scalproides has been associated with high nutrient

and TSS concentrations (Bona et al., 2007). The

predominant species in these streams were those that

were motile and resistant to excess sediments, such as

G. scalproides, Navicula contenta, N. schroeteri, andN. obtusa.

The algal metrics used in this investigation

allowed the differentiation of well-preserved streams

from those modified by land use. Certain metrics,

such as the percentage of acidophilic species, mes-

otraphentic species, and oligo-eutraphentic species,

together with the percentage of taxa sensitive to

disturbance, allowed us to differentiate between the

forest streams and those with greater concentrations

of nutrients in the coffee plantations and pastures.

Conversely, the percentages of alkaliphilous ? alka-libiontic taxa, eutraphentic taxa, and motile species

taxa (all associated with greater levels of disturbance)

were higher in the coffee plantation and pasture

streams than in those of the forest. Eutraphentic

diatoms displayed a significant negative correlation

with forests, suggesting that the greater the forest

cover, the lower the percentage of eutraphentic

species. One of the clearest algal metrics related to

disturbance was the percentage of motile species,

which was very high in the coffee plantation streams

with high TSS concentrations, especially in the wet

season. These species are capable of moving up and

around biofilms to optimize photosynthesis and are

resistant to excess sediments, as they can use their

motility to avoid burial by siltation (Fore & Grafe,

2002). The higher percentage of prostrate species inthe coffee plantation and pasture streams with the

highest discharge values could be considered an

indicator of disturbance, as they include species that

withstand hydraulic disturbances by adhering hori-

zontally to the substrate (Fore & Grafe, 2002).

Conversely, the forest streams with more stable

currents are dominated by erect and stalked diatoms,

which are intolerant to fast currents.

Thus, diatom assemblages responded to micro-

watershed conditions and can be used to monitor the

effects of land uses on streams in tropical regions. Toour knowledge, this is the first study in Mexico using

diatoms as indicators of water quality related to

deforestation.

Acknowledgments We thank Ariadna Martnez for laboratory

analyses, Rosario Landgrave for the GIS analysis of the study

area, and Javier Tolome for providing support in the field. Ma.

Elena Sanchez andKeithMacmillan translated andreviseda first

English version of the manuscript. We thank three anonymous

reviewers for their comments and constructive suggestions. This

study was supported by CONACYT-Mexico (43082).

References

American Public Health Association (APHA), 1998. Standard

Methods for Examination of Water and Waste Water.

American Public Health Association, Washington, DC.

Association of Official Analytical Chemists (AOAC), 1990.

Official Methods of Analysis of the Association of Offi-

cial Analytical Chemists, 15th ed. W. Byrds Press,

Virginia.

Bahls, L. L., 1993. Periphyton Bioassessment Method for

Montana Streams. Water Quality Bureau, Department of

Health and Environmental Services, Helena, MT.

Bellinger, B. J., C. Cocquyt & C. M. O. Reilly, 2006. Benthic

diatoms as indicators of eutrophication in tropical streams.

Hydrobiologia 573: 7587.

Biggs, T. W., T. Dunne & L. A. Martinelli, 2004. Natural

controls and human impacts on stream nutrient concen-

trations in a deforested region of the Brazilian Amazon

basin. Biogeochemistry 68: 227257.

Bixby, R. J., J. P. Benstead, M. M. Douglas & C. M. Pringle,

2009. Relationships of stream algal community structure

to catchment deforestation in eastern Madagascar. Journal

of North American Benthological Society 28: 466479.

Hydrobiologia (2011) 667:173189 187

123


16/17

Bona, F., E. Falasco, S. Fassina, B. Grisselli & G. Badino,

2007. Characterization of diatom assemblages in mid-

altitude streams of NW Italy. Hydrobiologia 583:

265274.

Bourrelly, P., 1966. Les algues d0eau douce. Initiation a la

systematique. Tome I. Les algues vertes. N. Boubee &

Cie, Paris, France.

Bourrelly, P., 1970. Les algues d0eau douce. Initiation a la

systematique. Tome III. Les algues bleues et rouges : les

Eugleniens, Peridiniens et Cryptomonadines. N. Boubee

& Cie, Paris, France.

Carpenter, K. D. & I. R. Waite, 2000. Relations of habitat-

specific algal assemblages to land use and water chemistry

in the Willamette basin, Oregon. Environmental Moni-

toring and Assessment 64: 247257.

Dodds, W. K., J. R. Jones & E. B. Welch, 1998. Suggested

classification of stream trophic state: distributions of

temperate stream types by chlorophyll, total nitrogen and

phosphorus. Water Resources 32: 14551462.

Fore, L. S. & C. Grafe, 2002. Using diatoms to assess the

biological condition of large rivers in Idaho (USA).

Freshwater Biology 47: 20152037.Garca-Franco, J. G., G. Castillo-Campos, K. Mehltreter, M.

L. Martnez & G. Vazquez, 2008. Composicion florstica

de un bosque mesofilo del centro de Veracruz, Mexico.

Boletn de la Sociedad Botanica de Mexico 83: 3752.

Harding, J. S., R. G. Young, J. W. Hayes, K. A. Shearer & J.

D. Stark, 1999. Changes in agricultural intensity and river

health along a river continuum. Freshwater Biology 42:

345357.

Hasle, G. R., 1978. Diatoms. In Sournia, A. (ed.), Phyto-

plankton Manual. UNESCO, Paris: 136142.

Hauer, R. M. & G. L. Lamberti, 1996. Methods in Stream

Ecology. Academic Press, Inc., San Diego, CA.

Hering, D., R. K. Johnson, S. Kramm, S. Schmutz, K. Szosz-

kiewicz & P. M. Verdonschot, 2006. Assessment ofEuropean streams with diatoms, machrophytes, macroin-

vertebrates and fish: a comparative metric-based analysis

of organism response to stress. Freshwater Biology 51:

17571785.

Herlihy, A. T., J. L. Stoddard & C. B. Johnson, 1998. The

relationship between stream chemistry and watershed land

cover data in the Mid-Atlantic region U.S. Water, Air, and

Soil Pollution 105: 377386.

Hill, B. H., R. J. Stevenson, Y. Pan, A. T. Herlihy, P. R. Ka-

ufmann & C. B. Johnson, 2001. Comparison of correla-

tions between environmental characteristics and stream

diatom assemblages characterized at genus and species

levels. Journal of North American Benthological Society

20: 299310.

Holdridge, L. R., W. C. Grenke, W. H. Hatheway, T. Lang & J.

A. Tosi, 1971. Forest Environments in Tropical Life

Zones: A Pilot Study. Pergamon Press, Oxford.

Johnson, L. B., C. Richards, G. E. Host & J. W. Arthur, 1997.

Landscapes influences on water chemistry in Midwestern

stream ecosystems. Freshwater Biology 37: 193208.

Jordan, T. E., D. L. Correll & D. E. Weller, 1997. Effects of

agriculture on discharges of nutrients from Coastal Plain

watersheds of Chesapeake Bay. Journal of Environmental

Quality 26: 836848.

Juttner, I., S. Sharma, B. M. Dahal, S. J. Ormerod, P.

J. Chimonides & E. J. Cox, 2003. Diatoms as indicators of

stream quality in Kathmandu Valley and Middle Hills of

Nepal and India. Freshwater Biology 48: 20652084.

Kramer, K. & H. Lange-Bertalot, 1991a. Bacillariophyceae. 3.

Teil: Centrales, Fragilariaceae, Eunotiaceae. 166 tafeln mit

2180 figuren. Gustav Fischer Verlag Stuttgart, Germany.

Kramer, K. & H. Lange-Bertalot, 1991b. Bacillariophyceae. 4.

Teil: Achnanthaceae, Kriticsche Erganzungen zu Navic-

ula (Lineolatae) und Gomphonema Gesamliter-atu-

verzeichnis Teil 1-4-88 tafeln mit 2048 figuren. Gustav

Fischer Verlag Stuttgart, Germany.

Kramer, K. & H. Lange-Bertalot, 1997. Bacillariophyceae. 2.

Teil: Bacillariaceae, Epithemiaceae, Surirellaceae. 184

Tafeln mit 1914 Figuren. Spektrum Akademischer Verlag,

Germany.

Kramer, K. & H. Lange-Bertalot, 1999. Bacillariophyceae. 1.

Teil: Naviculaceae. 206 tafeln mit 2976 figuren. Spektrum

Akademischer Verlag, Germany.

Larned, S. T. & S. R. Santos, 2000. Light- and nutrient-limited

periphyton in low order streams of Oahu, Hawaii.

Hydrobiologia 432: 101111.Lorion, C. M. & B. P. Kennedy, 2009. Relationships between

deforestation, riparian forest buffers and benthic macro-

invertebrates in Neotropical headwater streams. Fresh-

water Biology 54: 165180.

Lowe, R. L. & Y. Pan, 1996. Benthic algal communities as

biological monitors. In Stevenson, R. J., M. L. Bothwell &

R. L. Lowe (eds), Algal Ecology. Freshwater Benthic

Systems. Academic Press, San Diego: 705739.

Meeks, C. J., 1974. Chlorophylls. In Stewart, P. D. W. (ed.),

Algal Physiology and Biochemistry. Blackwell Scientific

Publications Ltd., Great Britain: 161174.

Mosisch, T. D., S. E. Bunn & P. M. Davies, 2001. The relative

importance of shading and nutrients on algal production in

subtropical streams. Freshwater Biology 46: 12691278.Munoz-Villers, L. E., 2008. Efecto del cambio en el uso de

suelo sobre la dinamica hidrologica y calidad de agua en

el tropico humedo del centro de Veracruz, Mexico. Doc-

toral Thesis. Universidad Autonoma Metropolitana.

Neill, C., L. A. Deegan, S. M. Thomas & C. C. Cerri, 2001.

Deforestation for pasture alters nitrogen and phosphorus

in small Amazonian streams. Ecological Applications 11:

18171828.

Pan, Y., A. Herlihy, P. Kaufmann, J. Wiginton, J. van Sicklle &

T. Moser, 2004. Linkages among land-use, water quality,

physical habitat conditions and lotic diatom assemblages:

a multi-spatial scale assessment. Hydrobiologia 515:

5973.

Porter, S. D., 2008. Algal attributes: an autoecological classi-

fication of algal taxa collected by the National Water-

Quality Assessment Program: U.S. Geological Survey

Data Series 329 [available on internet at http://pubs.usgs.

gov/ds/ds329/].

Porter, S. D., D. K. Mueller, N. E. Spahr, M. D. Munn & N.

M. Dubrovsky, 2008. Efficacy of algal metrics for

assessing nutrient and organic enrichment in flowing

waters. Freshwater Biology 53: 10361054.

Ramos-Escobedo, M. & G. Vazquez, 2001. Major ions, nutri-

ents and primary productivity in volcanic Neotropical

188 Hydrobiologia (2011) 667:173189

123
http://pubs.usgs.gov/ds/ds329/http://pubs.usgs.gov/ds/ds329/http://pubs.usgs.gov/ds/ds329/http://pubs.usgs.gov/ds/ds329/


17/17

streams draining rainforest and pasture catchments at Los

Tuxtlas, Veracruz, Mexico. Hydrobiologia 445: 6776.

Schiller, V. D., E. Mart, J. L. Riera & F. Sabater, 2007. Effects

of nutrients and light on periphyton biomass and nitrogen

uptake in Mediterranean streams with contrasting land

uses. Freshwater Biology 52: 891906.

Silva-Benavides, A. M., 1996. The use of water chemistry and

benthic diatom communities for qualification of a polluted

tropical river in Costa Rica. Revista de Biologa Tropical

44: 395416.

Sokal, R. R. & F. J. Rohlf, 1981. Biometry, 2nd ed. Freeman,

New York.

Stevenson, J. & L. L. Bahls, 1999. Periphyton protocols. In

Barbour, M. T., J. Lerritsen, B. D. Snyder & J. B. Stribling

(eds), Rapid Bioassessment Protocols for Use in Wade-

able Streams, Rivers: Periphyton, Benthic Macroinverte-

brates, Fish, 2nd ed. Environmental Protection Agency,

Office Water, Washington.

Stevenson, R. J., S. T. Rier, C. M. Riseng, R. E. Schultz & M.

J. Wiley, 2006. Comparing effects of nutrients on algal

biomass in two regions with different disturbance and

with applications for developing nutrient criteria. Hydro-biologia 561: 149165.

Van Dam, H., A. Mertens & J. Sinkeldam, 1994. A coded

checklist and ecological indicator values of freshwater

diatoms from the Netherlands. Netherlands Journal of

Aquatic Ecology 28: 117133.

Venrick, E. L., 1978. How many cells to count? In Sournia, A.

(ed.), Phytoplankton Manual. UNESCO, United King-

dom: 167180.

Wang, Y., J. Stevenson & L. Metzmeier, 2005. Development

and evaluation of a diatom-based Index of Biotic Integrity

for the Interior Plateau Ecoregion, USA.

Weilhoefer, C. L. & Y. Pan, 2006. Diatom assemblages and

their associations with environmental variables in Oregon

Coast Range streams, USA. Hydrobiologia 561: 207219.

Williams, M., C. Hopkinson, E. Rastetter, J. Vallino &

L. Claessens, 2005. Relationships of land use and stream

solute concentrations in the Ipswich river basin, north-

eastern Massachusetts. Water, Air, and Soil Pollution 161:

5574.

Williams-Linera, G., 1994. El bosque de montana: un ecosis-

tema muy fragil. In Castillo-Campos, G. & T. Meja-Sa-

ules (eds), Los recursos vegetales. Problematica ambiental

en el estado de Veracruz. Universidad Veracruzana,

Mexico: 5158.

Williams-Linera, G., 2007. El Bosque de niebla del centro deVeracruz: Ecologa, historia y destino en tiempos de

fragmentacion y cambio climatico. INECOL-CONABIO,

Xalapa, Ver.

Hydrobiologia (2011) 667:173189 189

123

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